Abstract
In this chapter, the taxonomical complexities of the genus Triticum are presented. Following the biological concept of species, the genus contains six species, two diploids, two tetraploid, and two hexaploids. The characteristic morphology of the genus and that of the wild forms, their geographic distribution, and ecological affinities, as well as their preadaptation for domestication and the processes leading to wheat domestication are reported. The origin and evolution of the diploid species, and the genome analysis of the allopolyploids are reviewed. Origin of the A, B, and D subgenomes of allopolyploid wheats, are presented. The relationships between Triticum species and other Triticineae are discussed.
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10.1 Description of the Genus
10.1.1 Taxonomic Complexities
At all times human strived to recognize, define and control the plants and animals around them and, as the first step in this endeavor, they named and classified them. This is well reflected in the biblical story in which God asked Adam to name all animals and plants, … “And the Lord God … brought them unto Adam to see what he would call them: and whatsoever Adam called every living creature, that was the name thereof” (Genesis 2, 19). Already in ancient times, at the end of the second millennium BC, the domesticated wheats were divided into two major groups: free-threshing wheats and hulled wheats, referred to in the bible (e.g., Exodus 9: 32) as wheat (probably a free-threshing form of tetraploid wheat) and as emmer (hulled form of tetraploid wheat; spelt was not grown in ancient Egypt), respectively. This classification was also accepted by the early Greek taxonomists of the fourth century BC, Aristoteles and Theophrastus, and by the first century Latin agronomist Columella, who classified the domesticated wheats in two sections, namely: Triticum—wheats whose spikes have a tough rachis and grain so loosely invested by the chaff that they fall out when the spikes are threshed (free-threshing types), and Zea—wheats whose spikes have a semi-fragile rachis, which, when pressed, breaks into spikelets, and whose grains are so firmly enclosed by the glumes that they are separated with difficulty (hulled wheats). The Zea section includes the present-day “spelt” wheats, namely, small spelt (Triticum monococcum ssp. monococcum), Emmer (T. turgidum ssp. dicoccon) and common spelt (T. aestivum ssp. spelta).
This classification was more or less in use until the eighteenth century, when Linnaeus (1753) suggested the classification of the wheats based on the binaric system. He was the first to place all the domesticated wheats under a single genus, Triticum, and included the following five different species in this genus: T. aestivum (bearded spring wheat), T. hybernum (bearded winter wheat), T. turgidum, T. spelta and T. monococcum. In the third edition of his Species Plantarum (Linnaeus 1764), he added T. polonicum. All the six species were domesticated forms.
Since then, the scientific name of bread (common) wheat has been changed by several taxonomists, e.g., T. sativum Lamarck (1786), T. vulgare Villars (1787), T. cereale Schrank (1789), T. vulgare subsp. vulgare Körnicke (1885), Frumentum triticum Krause (1898), T. vulgare Percival (1921), T. aestivum Schiemann (1948), T. aestivum cultivar group aestivum Bowden (1959), and T. aestivum ssp. aestivum Mac key (1966, 1988), van Slageren (1994) (for details see Bálint et al. 2000).
The discovery of the wild one-grained wheat, T. monococcum ssp. aegilopoides, and the two-grained T. turgidum ssp. dicoccoides, in the nineteenth century and in the beginning of the twentieth century, respectively, enabled Schultz (1913b) to assemble the first natural classification of the wheats (Table 10.1). He divided the genus Triticum into three major taxonomic groups, namely, einkorn, emmer and dinkel. Each group was subdivided further into wild and domesticated species and the domesticated species further separated into hulled and naked (free-threshing) types. Schultz (1913b) assumed that the domesticated naked types derived from the domesticated hulled species, which, in turn, derived from the wild prototypes. He postulated the existence of three different types of wild wheats, i.e., prototypes of the einkorn, the emmer and the dinkel. The prototypes of einkorn and emmer were known, and Shultz believed that the wild progenitor of the dinkel wheats would also be found.
The data collected by von Tschermak (1914) on the fertility of the various interspecific F1 hybrids of wheats supported Schultz’s classification of three major groups of wheat. Schultz’s grouping is also in accord with the serological relationships as determined by Zade (1914). Thellung (1918a, b) disagreed with the morphological species classification approach and used a broader definition of species in the genus Triticum, a definition that was based on genetic relatedness. Thus, Thellung recognized only three wheat species, namely, T. monococcum, T. turgidum and T. aestivum. The natural classifications of Schultz and Thellung were also supported by the pioneering cytological studies of Sakamura (1918) who showed that the three groups of wheat differ in their chromosome number: the einkorns (T. monococcum) are diploids (2n = 14), the emmers (T. turgidum) are tetraploids (2n = 28), and the dinkels (T. aestivum) are hexaploids (2n = 42). Thus, the wheat species form a polyploid series based on X = 7 chromosome number. Of note, Sakamura (1918) was the first to determine the correct chromosome number of the wheats. Additional significant support for Schultz’s and Thellung’s classification came from the cytogenetic analysis of meiotic chromosome pairing in interspecific F1 hybrids between the various wheats, e.g., the studies of Sax (1918, 1921, 1922), Kihara (1919, 1924), Sax and Sax (1924). These studies showed that the polyploid species of the wheats are allopolyploids, i.e., containing subgenomes that derived from different species, and that the tetraploid wheat contains a subgenome of diploid wheat plus an additional subgenome and that allohexaploid wheat comprises the genome of tetraploid wheat plus an additional subgenome.
Since then, several new domesticated and wild taxa were discovered and a better understanding of the taxonomical, as well as of the cytogenetic and phylogenetic relationships among the various wheat taxa, has been gained; the classification of wheat was then modified accordingly. Not only the species names, but also their classification have been a matter of disagreement. The lack of agreement among wheat taxonomists have led to various classification proposals of the genus Triticum, each comprising a different number of sections and species. Percival (1921) described only two species in this genus, while Bowden (1959) listed three, Mac Key (1966) six, Miller (1987) 22, Jackubziner and Dorofeev (1968) 24, Dorofeev et al. (1980) 27, and Goncharov (2011) and Goncharov et al. 2009) 29. Obviously, one proper and acceptable classification of the Triticum species is essential for the study of their genetic structure, origin and evolutionary relationships as well as for efficient use of their gene pools to improve the domesticated forms (van Slageren 1994).
Classification of the Triticum species is complicated for several reasons: (i) The allopolyploid species of wheat contain subgenomes originating from two different genera, Triticum and Aegilops (e.g., hexaploid wheat, Triticum aestivum, contains one subgenome from Triticum and two from Aegilops). (ii) Both cultivated and wild forms occur in a single biological taxon. (iii) The genus Triticum and its related genera are relatively young, with possibilities of inter-specific and inter-generic hybridization leading to introgression. (iv) Over the 10,000 years of cultivation, numerous forms of domesticated wheats have evolved under human selection. This great diversity has led to much confusion in the taxonomical treatment of wheats. The above taxonomical complications have raised the following problems: (a) Is separation of the Triticum and Aegilops genera taxonomically justified? (b) Is it appropriate to group wild and domesticated forms under one biological species or to separate them into different taxonomic species? (c) How should new intergeneric hybrids and synthetic amphiploids be regarded?
In spite of the fact that Aegilops species contributed genome(s) to allopolyploid species of Triticum, their separation into two different genera is justified on the basis of morphological differences and the different evolutionary trajectories of these two genera. Mac Key (1966, 1968, 1981) claimed that Aegilops, especially the allopolyploid species, are developing towards increased weediness, whereas the domesticated taxa of Triticum, are taking a different evolutionary route, due to selection by man towards tough rachis, naked grains, rapid and uniform germination, reduced competition with neighboring wheat plants, long grain filling period, higher yield, and other traits. This evolutionary route has caused the domesticated wheat to be completely dependent on man for its survival.
The traditional taxonomists (e.g., Dorofeev et al. 1980; Goncharov et al. 2009; Goncharov 2011) do not consider the presence of reproductive barriers as an essential criterion for definition of a species, whether cultivated or wild. They claim that even though some wheat species readily cross with each other and form fertile progeny under experimental conditions, they fail to do so in nature because they do not grow in the same locations. Moreover, wild forms are under different selection pressure than domesticated ones, and consequently, have a different evolutionary trajectory. This means, according to the traditional taxonomists, that wild and domesticated forms cannot be included in the same species. The traditional taxonomist tends to overclassify; they find conspicuous characters, often without intermediates, and frequently use them to define new species (Mac Key 1981, 1989). The characters may be controlled by one or a few genes of little biological significance. As a result, too many species are defined, and then, to accommodate the enormous variability, unreasonable numbers of intra-specific categories are often established (Mac Key 1981, 1989; van Slageren 1994). Several classifications of the genus Triticum, such as those of Dorofeev et al. (1980), Goncharov (2011), subdivide it into a large number of species defined on the basis of a single major gene that affects the morphology of the spike. These classifications were built upon Körnicke’s (1885) morphological research, and were strongly influenced by Flaksberger’s classification (1935), both of which emphasized morphological differences. The classification of Dorofeev et al. (1980) (Table 10.2) divides the genus into two subgenera, Triticum and Boeoticum Migusch. et Dorof., each containing three sections; one subgenus comprises 19 and the other, eight different species. Within each section, crossability between species is perfect and the hybrids are fully fertile, borders are often indistinct and clearly only depend on individual major genes that affect spike morphology (Mac Key 1966, 1968, 1981). Among the species recognized by Dorofeev et al. (1980), there were several that are best regarded as mutant forms of other species. For instance, T. militinae Zhuk. & Migush. is a mutant form of T. timopheevii, T. jakubzineri (Udachin & Shakhm.) of T. turgidum, and T. sinskajae Filat. & Kurk. of T. monococcum (Goncharov 2011; van Slageren 1994). Moreoer, the division into two subgenera is based on the wrong concept that T. monococcum ssp. aegilopoides (= boeoticum; genome Ab) is the donor of the A subgenome to the T. timopheevii and T. kiharae instead of T. urartu. The classification proposed by Goncharov (Goncharov 2011; Goncharov et al. 2009) (Table 10.3) includes 29 species in five sections (the fifth section is of synthetic amphiploids).
The concept “biological species” has a cytogenetic and evolutionary (biosystematic) meaning and bears great relevance when genetic resources are considered (van Slageren 1994). On the other hand, “taxonomic species” is of great relevance when classification and nomenclature are considered. On this basis, and since this book adopts the cytogenetic and evolutionary approaches, the wild and domesticated forms will be included as sub-species under one species, even though they are under different selection pressure and consequently, different evolutionary direction.
According to Mac Key (1989), wheat taxonomy should take the dynamic process of speciation into account. In particular, when working with domesticated forms where breeders accelerate the creating forces, taxonomic decisions must not only be evolutionarily retrospective but also foresighted. Van Slageren and Payne (2013) maintained that a narrow, morphology-based concept is contrasted with a much wider, genome-based one, leading to profound differences in the recognition of taxa at species level and below. The latter concept accepts far fewer taxa. Considerations regarding the nomenclature of taxa are presented by van Slageren and Payne (2013), applying both the International Code for the Nomenclature of Cultivated Plants (ICNCP) and the International Code of Nomenclature for algae, fungi and plants (ICN or the ‘Melbourne Code’).
With the genome types being of obvious importance in any classification of Triticum, and when considering the biphyletic origin of the allopolyploids in this genus, Mac Key (1981, 1989, 2005) proposed a classification of the Triticum species that recognized three sections of wheat and only six biological species two in each section, and includes, in addition to the three wheat sections, also a section of the manmade crop, triticale, named Triticoseale (Wittm. ex Camus) MK, section nov. comprising two species (Table 10.4). The recognition of only six biological species of wheat by Mac Key (1981, 1989) was acceptable by van Slageren (1994) (Table 10.5) who omitted the section of Triticosecale since the triticale species were artificially created. This classification is used in this book (Table 10.5). The six species evolved from the five previously analyzed and enumerated by Mac Key (1966), who originally included T. urartu in T. monococcum ssp. aegilopoides (ssp. aegilopoides was under the name ssp. boeoticum by Mac Key 1966), which was later shown to be a biological species separable from aegilopoides by various morphological characters and reproductive isolation (Johnson and Dhaliwal 1976). Mac Key (1981) rearranged both the wild and cultivated species of the genus into species defined by their genetic relationships. Interspecific genome constitutions were identical in all six species of the genus Triticum. Consequently, species sharing the same genome constitution were ranked subspecies (van Slageren 1994) [convarieties by (Mac Key 1981)] within the same species.
The classification of the genus Triticum suggested by Mac Key (1966, 1975, 1981, 2005, 1954b) and modified by van Slageren (1994), is based on the biological species approach. It includes three sections, each with a different ploidy level, six species, two in each section, and 19 subspecies (Table 10.5). Taxa that differ by a major gene(s) are classified as sub-species. Elevation of Mac Key’s subspecies to a species rank, as suggested by Dotofeev et al. (1980), Miller (1987), Goncharov (2011), is not preferred, as it obscures the genetic relationships. With the exception of aestivum and durum, the other wheats are, in fact, relicts with only local importance, e.g., dicoccon, macha, spelta, compactum and sphaerococcum. This taxonomy technique accounts for genetic barriers and phylogenetic relationships.
The Mac Key’s classification is elegant, simple, flexible, and based on a genetic concept (van Slageren 1994). It stands in remarkable contrast to the highly hierarchical, strictly morphological system of Dorofeev et al. (1980), Goncharov (2011). It is therefore, not surprising that Mac Key’s approach was adopted by Mansfeld’s Encyclopedia of Agricultural and Horticultural Crops (Hanelt 2001) and was used by the (former) International Board for Plant Genetic Resources (IBPGR; now IPGRI).
Van Slageren (1994) preferred the adoption of the subspecies status for the intraspecific taxa instead of the ‘cv. Group’ designation used by Bowden (1959), Morris and Sears (1967). Subspecies designation expresses their classification as a botanical taxon, similar to species and genus (van Slageren 1994). Cultivars should be designated as, for example, T. turgidum L. ssp. durum (Desf.) Husn. ‘Cappelli’, an Italian cultivar.
According to van Slageren (1994), species described only on the basis of a discovered or induced mutation, subsequently selected and multiplied and found to be stable, but never released as a commercial cultivar, should be made synonyms under the cultivated (sub)species from which they were isolated. This applies to the following species:
(1) T. sinskajae A. Filat. & Kurk.—this diploid species (genome AmAm) is a free-threshing mutant of domesticated T. monococcum developed in the Vavilov Institute in Daghestan, Russia; (2) T. militinae Zhuk. & Migush.—this tetraploid species (genome GGAA) is a free-threshing mutant selected from a single specimen (Miller 1987) of cultivated T. timopheevii; (3) T. jakubzineri Udachin & Schachm.—this tetraploid species (genome BBAA) appears to be a form of T. turgidum (Dorofeev and Korovina 1979); (4) T. petropavlovskyi Udachin & Migush.—this hexaploid species (genome BBAADD) is a Chinese landrace, originated from hybridization of hexaploid wheat, ssp. aestivum and tetraploid wheat, ssp. polonicum (Chen et al. 1985; Watanabe and Imamura 2002; (5) T. aethiopicum Jakubz. (Syn: T. abyssinicum Steud.)—this tetraploid species (genome BBAA) presumably arose as a free-threshing mutant from Ethiopian emmer, and was included by Miller (1987) in T. durum. It was classified by Mac Key (1966) in T. turgidum; (6) T. isphahanicum Heslot.—this tetraploid species (genome BBAA) is, according to Mac Key (1966), a form of T. polonicum, and shows a tendency towards a more standard Triticum glume morphology. This taxon may have been cultivated in the Isfahan region of Iran; (7) T. pyramidale Perciv.—this tetraploid species (genome BBAA) was considered by Mac Key (1966) as a special form of T. turgidum ssp durum, but by Miller (1987) as a form of T. turgidum ssp. turgidum. This taxon may have been or is may still be cultivated in Egypt; (8) T. vavilovii (Tumanian) Jakubz—this hexaploid species (genome BBAADD) is a branching mutant found by Tumanian during the 1929–30 autumn–winter season as an admixture in a stand of bread wheat landrace called ‘Dir’, northeast of lake Van, at an altitude of 1780 m. In 1970, it was also found as an admixture in Azerbaijan, by Mustfaev, and in Armenia, by Gandilyan. Plants with branched, vavilovii-type spikes were produced by Mac Key (1966), among others, in progenies of wide interspecific crosses of cultivated wheat groups.
van Slageren (1994) objected to the inclusion of intergeneric synthetic allopolyploids under Triticum. Thus, the synthetic allopolyploids T. kiharae Dorof. & Migush. (Genome GGAADD), resulting from the cross of T. timopheevii x Ae. tauschii, T. x boeoticourarticum Gandilyan et al. (genome AmAmAA), resulting from the cross T. monococcum ssp. aegilopoides x T. urartu, T. x boeoticotayschicum (genome AmAmDD), resulting from the cross T. monococcum ssp. aegilopoides x Ae. tauschii, should not be enumerated under Triticum. Likewise, Mac Key (1968) included two ‘subgroups’ in Triticum: Triticale (Tscherm. seys. ex Müntzing) Mac Key, representing the triticales and Trititrigia Mac Key), representing the Triticum x Elytrigia hybrids. However, according to van Slageren (1994), both subgroups cannot be included in Triticum.
10.1.2 Morphology
The Triticum L species plants are annual, predominantly autogamous and 30–100-cm-tall. Their leaves are flat with a membranous ligule. The spike is determinate or indeterminate, linear, two-rowed, laterally compressed, 8–20-cm-long, and either awned or awnless. The spikelets are solitary at nodes, laterally compressed. There are 2–6(–9) florets in every spikelet. The florets are hermaphrodites, with the 1–2 upper usually sterile. The glumes are sub-equal, ovate or oblong, mostly shorter than the spikelet, veined, more or less keeled, and either with 1–2 teeth on the tip or awned. The lemma is sub-ventricose, boat-shaped, coriaceous, keeled towards the apex, and either with 1–2 teeth or one awn. The palea are membranous, 2-veined, 2-keeled, and ciliated along the keels. The caryopsis is either tightly enclosed by the tough glumes, or free, oblong-elliptic, hairy at the apex, deeply grooved along its adaxial side, and with an embryo about 1/5 its length; the hilum is linear, and as long as the caryopsis.
In contrast to the species of Aegilops that exhibit wide morphological differences, those of Triticum are more or less uniform in their gross morphology. The two diploid wheat species are similar in their spike morphology and all the allopolyploid wheats carry the pivotal A subgenome that determines plant morphology and thus, they resemble diploid wheats in their basic morphology (stature, leaf shape, spike and spikelet morphology, grain shape, free caryopsis, keeled glumes, plant habitus, and growth habit) and in the structure of the seed dispersal unit (Mac Key 2005; Feldman et al. 2012). The differential B, G, and D subgenomes are primarily responsible for the eco-geographical adaptation of the allopolyploids and their resistance to biotic and abiotic stresses (Feldman et al. 2012). The A subgenome also controls the autogamous naure of the allopolyploid wheats (assuming that the donor of the B subgenome is an allogamous species, similar to Ae. speltoides) and harbors many domestication genes, such as the genes for non-brittle spike on 3AS (Rong et al. 1999; Nalam et al. 2006), free-threshing on 5AL (Sears 1954), QTIs for kernel size predominantly on A subgenome, i.e., on chromosomes 1A, 2A, 3A, 4A, 7A, 5B, and 7B) (Elias et al. 1996), and for grain size and grain form on chromosomes 1A, 3A, 4B, 5A, and 6A (Gegas et al. 2010), and a number of domestication-related QTLs (Peng et al. 2003a, b).
There are four wild wheat taxa, whereas all the other taxa are domesticated (Table 10.5). The wild and domesticated taxa are inter-fertile and only a small number of genes control the traits that distinguish them. The wild wheats, namely, diploid T. monococcum ssp. aegilopoides and T. urartu, and tetraploids T. timopheevii ssp. armeniacum and T. turgidum ssp. dicoccoides, have a brittle rachis that disarticulates into arrowhead-shaped spikelets upon maturity, each with the rachis segment below it (wedge-type dispersal unit). This type of seed dispersal unit facilitates self-burial in the soil, hence, protection during the hot summer and successful germination after the beginning of the rainy season.
10.1.3 Geographic Distribution and Ecological Affinities
Following the discovery of wild diploid wheat during the second half of the nineteenth century and wild tetraploid wheats in the beginning of the twentieth century, the putative progenitors of the domesticated diploid and tetraploid wheats were identified and their distribution area and ecological affinities have become well known. It was then relatively simple to establish the geographical regions from which the various wheat taxa were taken into cultivation.
The wild progenitors of domesticated wheats are natural constituents of some of the open oak-park belts and the herbaceous plant formations in southwest Asia. Their center of origin, proposed based on ample archaeological evidence (Feldman and Kislev 2007), and current center of distribution and diversity is in the “Fertile Crescent” arc—a hilly and mountainous region extending from the foothills of the Zagros Mountains in south-western Iran, through the Tigris and Euphrates basins in northern Iraq and southeastern Turkey, continuing southwestward over Syria to the Mediterranean, and extending to Israel, Palestinian Territory and Jordan. The four wild wheat taxa and 17 species of the closely-related genus Aegilops, as well as several genera and species of other Triticeae, are endogenous to this region.
The Fertile Crescent is bound by the Mediterranean in the west, by chains of large and high mountain ranges in the north and east (the Amanos in north-western Syria, the Taurus in southern Turkey, Ararat in north-eastern Turkey and the Zagros in western Iran), and in the East and south by the Syrio-Arabian desert, with its western extension (e.g., Paran desert) in the Sinai Peninsula. Situated between the sea, mountains, and the desert, the Fertile Crescent is under the influence of several different climates: on the one hand, it enjoys the temperate Mediterranean climate with a short, mild and rainy winter and long, hot and dry summer. On the other hand, it is influenced by the more extreme steppical climate of the Iranian and Anatolian plateaus in the northeast and north, and by the desert climate in the east and south. Consequently, the Fertile Crescent encompasses two different phytogeographical regions, the Mediterranean in the western part and the steppical (Irano-Turanian) in the northeastern part, and is affected by two other regions, the Saharo-Arabian in the south and the Euro-Siberian in the north. The Mediterranean part of the Fertile Crescent includes Israel, the Palestinian Territory, Jordan, Lebanon, Syria and the western part of southeastern Turkey and it centers around the Syrio-African rift (the Jordan rift valley in the south, the Beqa Valley of Lebanon and the Orentos valley in Syria). The Irano-Turanian part includes the eastern part of southeastern Turkey, northern Iraq, and southwestern Iran, and is influenced by the continental climate of the Iranian and Central Asiatic steppes.
It is no wonder, therefore, that this region is very ecologically diversified, comprising a wide array of different habitats. These versatile ecological conditions are manifested by the wide display of different plant formations, ranging from well-developed Mediterranean forests and maquis, through open parks, shrubs (garrigue) and herbaceous (batha) formations, to small shrub and steppical plant formations. Many annual grasses and legumes occupy the open habitats in these formations, which presumably served in the pre-agricultural era as the main pasture area for wild sheep, goats and gazelles—the game of the pre-Neolithic hunter and plant collector.
Like de Candolle (1886), Braidwood (1960), Harlan and Zohary (1966), Zohary and Hopf (2000), Zohary et al. (2012), and others thought that Near Eastern agriculture originated within or near the distribution area of the wild progenitors in the Fertile Crescent region. New geological, climatic and archaeological data from the east Mediterranean region indicate that the Younger Dryas climatic event, which was characterized by a cold and dry climate, occurred from 12,900 to 11,700 years Cal-BP (for details see Hillman 1996; Bar-Yosef 1998). Hillman (1996), using palaeobotanical data, reconstructed the phytogeographical belts of this region during the Younger Dryas and concluded that the habitats of the annual cereals lie mainly in the open areas of the oak-park maquis, in a relatively narrow strip of the east Mediterranean. This narrow strip, called the “Levantine Corridor”, begins in the Taurus foothills (Diyarbakir area) in southeastern Turkey and extends along the Mediterranean southward, incorporating the middle Euphrates through the Damascus basin, the Lebanese mountains, the two sides of the Jordan Rift Valley into the Sinai Peninsula (Bar-Yosef 1998). In the central-southern part of the corridor (from north of Damascus to southern Judea), tetraploid wild wheat, T. turgidum ssp. dicoccoides, has massive stands, while diploid wild wheats, T. monococcum ssp. aegilopoides, and T. urartu, and also another tetraploid wild wheat, T. timopheevi ssp. armeniacum, occupy the northern part. The diploid species also grow in the central part of the corridor. These wild taxa mainly grow on terra-rossa and basalt soils and are adapted to a variety of habitats and a wide range of altitudes (from 100 to 1600 m asl) (Kimber and Feldman 1987; Zohary and Hopf 2000; Mac Key 2005).
The accumulating archaeological data indicate that agriculture originated in the Levantine Corridor of the Fertile Crescent. This is clearly apparent from the distribution of the earliest Neolithic sites 10,300–9500 BP: Tell Mureybit and Tell Abu Hureyra in the Middle Euphrates in the northern part of the corridor, Tell Aswad and Tell Ghoraife in the Damascus basin, and Netiv Hagdud, Dhra, Gilgal, and Jericho in the Jordan Valley, between the Lake of Galilee and the Dead Sea (Bar-Yosef and Kislev, 1989; Hillman, 1996; Bar-Yosef, 1998). All these settlements were established along the ecotone between the relatively temperate Mediterranean phytogeographical region and the steppical Irano-Turanian region. The predominant plant formations in this transitional zone are open parks and herbaceous covers containing a large number of annual grasses and legumes.
The present distribution of the wild forms of wheat could provide important information on the place(s) of origin of Neolithic agriculture. For example, emmer was probably taken into agriculture in the upper Jordan watershed and einkorn was domesticated in southeast Turkey (Harlan and Zohary 1966; Feldman and Kislev 2007). It seems likely therefore, that, while these wild wheats were domesticated within the Fertile Crescent, each was domesticated in a different sub-region of the zone. Yet, any interpretation of modern distribution must take into account (i) the possibility that the climate likely changed in the last 12,000 years, and (ii) the possibility that the wild progenitors themselves changed location, producing weed races whose ranges expanded after the spread of agriculture (Harlan and Zohary 1966).
10.1.4 Preadaptation for Domestication
In many respects, wheat was well preadapted for domestication. Its massive stands in some regions and large seeds that are nutritious and storable, rendered it attractive to the ancient collector. Its annual growth habit, by which it escaped the dry season, made it suitable for dryland farming. In addition, wheat’s predominant self-pollination could have helped in the fixation of desirable mutants and of recombinants resulting from rare outcrossing events. Moreover, while the wild wheats occupy poor, thin, rocky soils in their natural sites, they respond well when transferred to richer habitats.
Of the various species of cereals that grew in the Fertile Crescent and which were harvested by the pre-neolithic (Natufian) people, only wild emmer, einkorn, rye and barley (and possibly also wild timopheevii) were cultivated by the early farmers (van Zeist and Bakker-Heeres 1985; Kislev et al. 1986). Assuming that the amount of grain collected per unit time was the most important criterion (Evans 1981), wild stands of wheat and barley were preferred over other cereals, because their large, heavy grains borne in spikes, facilitated their harvesting. Indeed, Harlan (1967) in wild einkorn and Ladizinsky (1975) in wild emmer, succeeded in gathering considerable amounts of grains per hour of harvesting. Wild emmer, having larger grains and two grains in each dispersal unit, was a better candidate for domestication than barley, which only has one grain. Indeed, over a 3-h period, Ladizinsky (1975) harvested twice as many wild emmer grains as wild barley from a site in the upper Jordan Valley, Israel, (1950 g vs. 1040 g). More specifically, 247 wild emmer grains per hour were collected as compared to 107 barley grains per hour. Being a tetraploid, wild emmer exhibits greater and more rapid adaptability to cultivation conditions than barley. The taste of wheat, its high nutritional quality, and its large grain might have also contributed to its preference over barley. In addition, judging from today’s pattern of distribution, barley was probably very common and grew in abundance within a short distance from the early Neolithic settlements, while the dense stands of wild emmer were somewhat more distant. This might have created additional pressure to cultivate wheat, as sufficient quantities of barley could have been harvested from nearby wild stands.
10.2 Section Monococcon Dumort. (2n = 2x = 14)
10.2.1 Description of the Section
This section [Syn.: Crithodium Link; Triticum L. sect. Crithodium (Link) Nevski; Triticum L. ‘congregatio’ Diploidea Flaksb.] contains two species, T. monococcum L. and T. urartu Tum. ex Gand. Both species are morphologically similar, diploids (2n = 2x = 14), with closely related genomes. The T. monococcum genome is designated Am (modified A) and that of T. urartu is designated A. T. monococcum contains two subspecies, ssp. aegilopoides and ssp. monococcum, with the former being a wild form with a wide distribution in the northeastern Mediterranean and western Asia, while the latter is a domesticated form which is still cultivated in certain regions in southern Europe, North Africa and Asia. ssp. aegilopoides is the wild ancestor of the domesticated ssp. monococcum. The second diploid species, T. urartu, grows sympatrically with ssp. aegilopoides in southeastern Turkey, northern Iraq, northwestern Iran and Armenia.
10.2.2 T. monococcum L. (Genome AmAm)
10.2.2.1 Description of the Species
T. monococcum L., commonly known as einkorn, one-grained wheat, and small spelt, is an annual, predominantly autogamous, 30–70(–80)-cm-tall (excluding spikes) plant. It has a small number of tillers of which the upper parts are upright or erect. The spike is indeterminate, bilaterally compressed, tow-rowed, 8–12-cm-long (excluding awns) and awned. In the wild form the entire spike disarticulates at maturity into individual spikelets, each with its associated rachis segment (wedge–type dispersal unit) while in the domesticated form the spike remains intact on the culm. The rachis internodes are covered with hairs. The spikelets are compressed, with the top spikelet being fertile and generally in the same plane as those below. There are 8–16 spikelets, and 2–3 basal rudimentary spikelets. Each fertile spikelet contains 3 florets, the upper 1–2 are sterile. Usually, there is one grain per spikelet, sometimes two in the center of the spike or, more rarely, in the whole spike. The glumes with well-developed keels, two unequal teeth which usually do not develop into awns. The lemma tapers into a long awn, with a lateral tooth. The palea is membranous split along the keel at maturity. The caryopsis is free and laterally compressed (Fig. 10.1).
Plants and spikes of diploid species of Triticum; a T. monococcum L. ssp. aegilopoides (Link) Thell. (Wild einkorn); b T. monococcum L. ssp. monococcum (domesticated einkorn); c T. urartu Tum. Ex Gand
T. monococcum contains two subspecies, wild ssp. aegilopoides (Fig. 10.1a) and domesticated ssp. monococcum (Fig. 10.1b). The two subspecies are morphologically similar and genetically closely related (Smith 1936). Genetic divergence between these species has been accompanied by few or minor rearrangements in chromosome structure, and most characters differentiating between the two subspecies are dominant in the wild versus the domesticated form (Smith 1936).
The most distinguishing traits between the wild and domesticated subspecies are spike fragility, which does not disarticulate at maturity in the domesticated form, and the seeds, which are larger and wider in the domesticated as compared to the wild form. The wild forms have a brittle rachis, and the individual spikelets disarticulate at maturity to disperse the seed. The spikelets have one or two awns and a sharp rachis segment below each spikelet. These arrow-head like structure are very effective devices for seed dispersal and self-planting under wild conditions (Zohary et al. 1969). In domesticated monococcum, the mature spike remains intact and breaks into individual spikelets only on pressure. A mutation(s) for a tough rachis, that may occasionally occur in the wild, prevents the dispersal of seeds and thus, has a negative adaptive value and consequently, is soon selected against. In contrast, under cultivation, it has a positive value, facilitating easy harvesting, and has thus been preferred by the early farmers.
Non-brittleness in the domesticated form, ssp. monococcum, is determined by two complementary recessive genes (Sharma and Waines 1980). Pourkheirandish et al. (2018) identified non-brittle rachis 1 (btr1) and non-brittle rachis 2 (btr2) in einkorn as homologous to those of barley. Re-sequencing of the dominant and the recessive alleles of the Btr1 and Btr2 genes in a collection of 53 lines of wild and domesticated T. monococcum, showed that a single non-synonymous amino acid substitution (alanine to threonine) at position 119 of btr1, is responsible for the non-brittle rachis trait in domesticated einkorn. However, the rachis is not very tough and when pressure is applied, e. g., during threshing, it breaks into segments similar to the breakage obtained with the wild form. Evans and Dunstone (1970) found that increases in grain and leaf size accompanied the development of domesticated T. monococcum as a result of selection for increased yield, and that larger grains led to faster seedling development.
T. monococcum is a polymorphic taxon with variation involving spike and spikelet size, color, hairiness, number of grains per spikelet, and awn count, color and length. It features delicate spikes and spikelets, and has either spring or winter lines, with heading in the latter delayed until the plant experiences vernalization, usually a period of 30–60 days of cold winter temperatures (0°–5 °C). Both the wild and the domesticated forms are hulled types, i.e., their grains are tightly invested by the tough glumes, and therefore, the product of threshing is spikelets rather than grains. While several authors reported wide variation among domesticated varieties of T. monococcum (e.g., Smith 1936; Sharma and Waines 1980; Empilli et al. 2000), Dhaliwal (1977b) found that accessions from different sources were remarkably similar in their growth habit and some morphological characteristics. Likewise, Kuspira et al. (1989) investigated 460 true-breeding lines and reported on observations that supported Dhaliwal’s conclusion that phenotypic and genetic variability in T. monococcum is limited.
Smith-Huerta et al. (1989), using starch gel electrophoresis of extracts of young leaves, found low genetic diversity in the wild subspecies of T. monococcum and in the second diploid wheat, T. urartu. Both taxa had a small number of alleles per locus, as well as a low percentage of polymorphic loci, and mean gene diversity. The intra- and inter-populations affinity of both taxa, computed using Nei’s identity index (NI), were highly uniform on a genetic level. However, using starch gel electrophoresis of extracts of young leaves, but with several different enzymes Kuspira et al. (1989) detected a higher level of genetic diversity in these two wild taxa.
In contrast to the above, study of variations at the gliadin loci, Gli-1 and Gli-2, of the diploid wheats, revealed a remarkable allelic variation in these two loci (Ciaffi et al. 1997). The gliadin patterns of the wild and domesticated subspecies of T. monococcum were very similar but differed substantially from those of T. urartu. The gliadin composition of T. urartu resembled that of the A subgenome of polyploid wheats, supporting the hypothesis that T. urartu is the donor of this subgenome to the polyploid wheats. Similarly, Waines and Payne (1987), Ciaffi et al. (1998) studied variation in the high-molecular weight (HMW) glutenin subunit composition in wild and domesticated diploid wheats and found that all the taxa analyzed were characterized by high intraspecific variation. Yet, the biochemical characteristics of the HMW-glutenin subunits of wild and domesticated T. monococcum were very similar but distinctly different from those of T. urartu, which is consistent with their classification as two different species. High intraspecific allelic variation at the Glu-A1 locus of T. monococcum was also reported by Li et al. (2015a).
Using PCR with random primers, Vierling and Nguyen (1992) detected polymorphisms in ssp. monococcum, namely, out of 103 amplified products 41 showed polymorphism. Nasernakhaei et al. (2015), using single-strand conformation polymorphism to evaluate the nucleotide diversity in the Acc-1 and Pgk-1 loci of Iranian wild diploid wheats, detected a meaningful inter-population variation in wild T. monococcum. Mizumoto et al. (2002) studied genetic diversities of nuclear and chloroplast genomes using AFLP and simple sequence length polymorphism (SSLP) analyses, in the wild and domesticated subspecies of T. monococcum as well as in the second wild diploid species of wheat, T. urartu. The diploid wheats showed high nuclear and chloroplast DNA variation. In addition, nuclear AFLP and chloroplast SSLP analyses demonstrated a clear distinction between T. urartu and the wild and domesticated forms of T. monococcum.
10.2.2.2 Ssp. aegilopoides (Link) Thell. (Wild Einkorn)
T. monococcum ssp. aegilopoides (Link) Thell. [Syn.: T. boeoticum Boiss. ssp. aegilopoides (Link) E. Sciem.; Crithodium aegilopoides Link; Crithodium monococcum (L.) Á. Löve; T. monococcum ssp. boeoticum (Boiss.) Hayek; T. aegilopoides (Link) Balansa ex Körn.; T. spontaneum ssp. aegilopoides (Link) Flaksb.; T. thaoudar Reut.] was first described under the name Crithodium aegilopoides by Link, who found it in Greece between Nauplia and Corinth in 1833 (see Boissier 1884). In 1854, a similar specimen was discovered by Balanza on Mount Siphylus in Anatolia, Turkey, and was identified by Gay in 1860 as a wild T. monococcum aegilopoides (see Boissier 1884). Boissier collected another specimen of this taxon in Boeotica, Greece, and named it T. baeoticum Boiss. [Boissier’s original spelling of the new species was ‘bæoticum’ which is transcribed as ‘baeoticum’ (see van Slageren 1994)]. Thellung (1918a, b), however, decided that there is no justification to rank it at the species level and named it T. monococcum ssp. aegilopoides.
This wild subspecies is found in the northeastern Mediterranean and west Asia. It grows in primary habitats in the Fertile Crescent arc, namely, in Syria, Lebanon, southeastern Turkey, northern Iraq and northwestern Iran. Aaronsohn (1910) found ssp. aegilopoides on Mount Hermon, in southwestern Syria, and in southeastern Lebanon and later, it was also found in Georgia by Zhukovsky in 1923, in Armenia by Tumanian in 1930, and in Nakhichevan by Jakubziner in 1932 (Jakubziner 1932a).
From the Fertile Crescent region, it spread as weed with the expansion of the Neolithic agriculture into central, western, and northern Turkey, Greece (Thessaly and Achaia), Albania, southern Bulgaria, and southern Serbia, Crimea, and Ciscaucasia. In this region, it mainly grows as a segetal plant in somewhat disturbed, secondary habitats. ssp. aegilopoides thrives on terra rossa, basalt and several types of alluvial soils in degraded deciduous oak forests and maquis, deciduous steppe maquis, open herbaceous and dwarf shrub formations, pastures, abandoned fields, edges of cultivation and roadsides. Over much of its present range, it is a weedy plant growing along roadsides, field margins, and paths, and often invading wheat fields in quantity (Harlan and Zohary 1966). It is very common and locally abundant in the northern part of the Fertile Crescent. ssp. aegilopoides grows at altitudes of 600–2000 m. It is more mesophytic and tolerant of cold than wild emmer wheat and occurs in massive stands at altitudes of as high as 2000 m in southeastern Turkey and Iran. Its center of distribution is in the Taurus-Zagros arc. In southeast Turkey, there are almost pure stands of ssp. aegilopoides in the Karacadag Mountains and several other areas in southeastern Turkey (Harlan and Zohary 1966). These massive stands range from elevations of 2000 m down to the edge of the plains in Urfa and Gaziantep, in southeastern Turkey (about 600 m). Massive stands of ssp. aegilopoides also occur, but less extensively, in northern Iraq and here and there in the Zagros of Iran.
Wild monococcum has a relatively large distribution in the central part of the distribution of the genus. It is an east Mediterranean element extending to the steppical (Irano-Turanian) region. It grows sympatrically with Amblyopyrum muticum, Ae. speltoides, Ae. searsii, Ae, caudata, Ae. umbellulata, T. urartu, the wild form of T. timopheevii, the wild form of T. turgidum, Ae. geniculata, Ae. biuncialis, Ae. neglecta, Ae. columnaris, Ae. triuncialis and Ae. cylindrica. It grows allopatrically with Ae. comosa, Ae. uniaristata, Ae, perigrina, Ae. kotschyi, Ae. tauschyii, Ae. crassa and Ae. juvenalis.
This subspecies contains two varieties, var. boeoticum that is characterized by a relatively small spike, spikelets mostly with one grain and with one awn, its second flower, ontogenetically the first, may be developed but is usually sterile and awnless lemma. This variety prefers less-extreme climates and grows more in the northern and northwestern part of the endemic region. The second variety, var. thaoudar, is more robust, has larger spikes, spikelets usually with two grains and two awns. The seed developing in the second floret is usually larger than the seed of the first floret, with the latter generally being half as big, richer in protein, and darker in color. While the larger seeds germinate in the first winter, the germination of the smaller darker seeds is delayed to the second winter (Harlan and Zohary 1966; Mac Key 1975). Var. boeoticum is common to the Balkan, the Anatolian Plateau and the parts of the Fertile Crescent arc, while var. thaoudar is found mainly in southeastern Turkey, Iraq and Iran. In central Anatolia and in Transcaucasia, many intermediates between the two races occur.
10.2.2.3 Ssp. monococcum (Domesticated Einkorn or Small Spelt)
Soon after its discovery, it became apparent that ssp. aegilopoides is the progenitor of domesticated einkorn (Schulz 1913b). This idea, that was mainly based on morphological evidence, was later supported by Blaringhem (1927), Kihara et al. 1929), who reported on complete fertility of hybrids between the wild and domesticated forms of T. monococcum, as well as by cytological data, namely, formation of seven ring bivalents at first meiotic metaphase of the F1 hybrids between these forms (Smith 1936). In addition, a survey of variation in alpha- and beta–amylase isosymes of dry and germinating seeds showed that ssp. monococcum, derived from its wild form ssp. aegilopoides, either from var. boeoticum or var. thaoudar (Nishikawa 1983). Further evidence from morphology and cross-compatibility of diploid wheats and fertility of the F1 hybrids among them, suggested that domesticated T. monococcum derived only once from a population of ssp. aegilopoides and underwent limited introgression from T. urartu (Dhaliwal 1977a). Experimental evidence showed that introgression could have only been possible from T. urartu to T. monococcum ssp. aegilopoides but not in the opposite direction (Dhaliwal 1977a).
Kilian et al. (2007) investigated haplotype variation among > 12 million nucleotide sequences at 18 loci across 321 wild and 92 domesticated lines of T. monococcum. Studies of the wild lines revealed that this taxon underwent a process of genetic differentiation prior to domestication, which led to formation of three genetically distinct races, designated α, β, and γ (Kilian et al. 2007). Only β was domesticated by the Neolithic farmers. Nucleotide and haplotype diversity in domesticated T. monococcum was higher than in its wild ancestral race, the β race, indicating that the domesticated form did not undergo reduction of diversity during domestication.
The domesticated subspecies was obviously preferred by the ancient farmers. Heun et al. (1997, 2008) analyzed domesticated and wild T. monococcum from the Fertile Crescent and beyond, and found that T. monococcum was domesticated in the Karacadağ Mountains in southeast Turkey. The findings also supported the assumption of its monophyletic origin. These findings were recently supported by Kilian et al. (2007).
It was only natural that the domestication of diploid wheat took place in the northern part of the Fertile Crescent arc, the distribution center of the wild progenitor during the Late Epipalaeolithic–early Neolithic period, as has been confirmed by archaeological and genetic data (review in Feldman 2001). Wild monococcum was collected by plant gatherers throughout its distribution area long before it was cultivated. The earliest known carbonized grains of brittle einkorn wheat were found in the prehistoric settlement of Tell Mureybit, the northern Levantine Corridor, about 10,000 years BP, where it was apparently collected or harvested from wild stands (Renfrew 1973). Indeed, the phylogenetic analysis by Heun et al. (1997) pinpoints the Karacadağ region of southeastern Turkey, in the northern part of the Levantine Corridor, as the region where einkorn was domesticated. At somewhat later archaeological sites in this area, non-brittle monococcum occurred side by side with a brittle type and gradually replaced it: in Ali Kosh in Iranian Khuzistan, 9500–8750 BP, Jarmo in Iraqi Kurdistan, ca. 8750 BP, Cayonu Tepesi in southeastern Turkey, ca. 9000 BP, Tell Abu Hureyra, northern Syria, ca. 9000 BP, and Hacilar in west-central Anatolia, ca. 9000 BP (for review see Hillman 1975, 1996; Kislev 1984, 1992; Bar-Yosef 1998; Bar-Yosef and Kislev 1989).
Harlan (1967) reported that, today, much of the Karacadağ Mountains is covered with vast stands of wild diploid wheats, together with a few wild barleys and other grasses. Most abundant are var. thaoudar of the wild einkorn and Ae. speltoides. Wild emmer was found scattered as a minor component in patches among the vast seas of the diploid wild wheats.
It is assumed that the natural massive stands of wild einkorn were attractive to the pre-Neolithic plant-gatherer. To obtain an idea of the quantity of grains of wild einkorn that the ancient gatherer could harvest in a day or a season, Harlan (1967), using a reconstructed sickle with flint sickle blades, was able to harvest 2.45 kg grains per hour. The actual grain content, free of glumes, palea, lemma, rachis segment, and awns, of the harvested material was 46% by weight, i.e., approximately 1 kg. Chemical analysis of the harvested grains showed that they contained 7.91% water, 2.77% ash, 2.64% other extract, 2.33% crude fiber, 22.83% crude protein and 60.04% nitrogen-free extract (Harlan 1967). The wild wheat is far higher in protein content than modern bread wheat cultivars that contain 12–14% protein. Hence, according to Harlan (1967), the ancient man would have had no difficulty in collecting about 227 g (1/2 lb) of protein per hour during the wild wheat harvesting season. One of the conspicuous advantages of obtaining food from wild cereal harvest is that grain stored in a dry place can be kept several years and still preserve its nutritive value.
ssp. monococcum is one of the earliest cultivated forms of wheat, alongside domesticated emmer wheat (T. turgidum ssp. dicoccon). According to archaeological evidence from the Fertile Crescent region (e.g., Arranz-Otaegui et al. 2018), hunter gatherers in the Fertile Crescent may have started harvesting einkorn as long as 30,000 years ago. Although gathered from the wild for thousands of years, einkorn wheat was first domesticated approximately 10,000 years BP in the Pre-Pottery Neolithic A (PPNA) or B (PPNB) periods (Zohary et al. 2012).
The predominantly autogamous nature of T. monococcum made domestication of this species easier. Desirable gene combinations of domesticated forms could be selected and maintained due to self-fertilization. Since autogamy is not absolute, inter-genotypic hybridization, resulting in the formation of numerous new recombinant genetic combinations, ensures sufficient genetic flexibility. The annual growth habit also aided in the domestication of T. monococcum since it enables passing the hot, dry season as seeds. The combination of annual growth habit and autogamy facilitated fixation and effective exploitation of combination with desirable genes by the rapid generation shift (Mac Key 2005).
Zohary (1999) assumed that comparison of domesticated T. monococcum with its wild relative may provide clues for discriminating between monophyletic and polyphyletic origins of the domesticated form. After such a comparison, he arrived at the conclusion that it is very likely that domesticated T. monococcum was taken into cultivation only once or, at most, very few times. Dhaliwal (1977a) concluded from morphological and cytological evidence that T. monococcum was domesticated only once from a population of ssp. aegilopoides, with a limited introgression from the second diploid wild wheat, T. urartu, that is found in southeastern Turkey, the site of T. monococcum domestication. In contrast, Kilian et al. (2007), based on molecular studies and archaeological findings from the Fertile Crescent, concluded that T. monococcum was domesticated in several independent events.
The cultivation of einkorn wheat spread from the northern part of the Fertile Crescent into several other regions in Eurasia. It spread westwards to central, northern and western Turkey, the Balkans, Italy, Spain, central, western and northern Europe, Morocco, north of Caucasia, and Southern Russia, and eastwards to Iran, Turkmenistan, and India. The cultivation of einkorn was never extensive in most of these regions. No remains of either wild or domesticated T. monococcum have been found in irrigated settlements in the lowlands of the Mesopotamian plains or in the Nile valley, to which emmer wheat farming spread in the 8th and 6th millennium BP, respectively (Feldman 2001). This might be due to the cooler and moister climate required by einkorn compared to emmer. On the other hand, domesticated einkorn spread into central and Western Europe through the Danube and Rhine valleys. In subsequent eras (Bronze Age), einkorn wheat attained a wide distribution in Europe and in the Near East. However, later on it was replaced by free-threshing polyploid wheats (Zaharieva and Monneveux 2014). Nowadays, traditional einkorn crops can still be found in very small areas on poor soil in marginal mountain areas of Turkey, Balkan countries, southern Italy, southern France, Spain and Morocco (Brandolini and Hidalgo 2011; Zaharieva and Monneveux 2014) and in few locations in central Asia.
An additional domesticated type of T. monococcum was recently found in a restricted area in Daghestan, central Asia. This type, var. sinskajae A. Filat & Kurk. differs from ssp. monococcum and aegilopoides by its softer glumes and free-threshing habit, a character controlled by a single recessive allele (Waines 1983). The glumes of this variety, however, are very long, resulting in somewhat more difficult threshing.
Domesticated T. monococcum contains lines with spring and winter growth habit. Kuspira et al. (1986) studied the mode of inheritance of this trait in T. monococcum and found that only one major gene determined growth habit in this species; the allele determining spring growth habit is dominant over that determining winter growth habit. They suggested that this locus is homoeoallelic to the VrnI locus of the A subgenome of T. aestivum.
The domesticated forms of T. monococcum are low-yielding but produce a reasonable quantity of grains when grown on poor, marginal soils where other wheats usually fail (Castagna et al. 1995; Borghi et al. 1996). Most domesticated einkorn varieties produce one grain per spikelet, hence its name, but cultivars with two grains exist as well (Schiemann 1948; Harlan 1981). Domesticated T. monococcum has a higher percentage of protein than most modern domesticated wheats and is considered more nutritious because it has also higher levels of fat, phosphorus, potassium, pyridoxine, vitamin A, beta-carotene, lutein and more riboflavin than other wheats. Because its flour lacks the rising characteristics desirable for bread, einkorn is primarily consumed as boiled whole grains, porridge, bulgur or as animal feed.
Yet, interest in T. monococcum is growing due to the demand for high quality wheat and the awareness of its agronomic potential and nutritional qualities. Attempts have been made to improve it to a more prolific and nutritious crop (Waines 1983; Vallega 1992; Castagna et al. 1995; Borghi et al. 1996; Brandolini and Hidalgo 2011;). Photosynthesis rates in diploid wheats exceed those of polyploid wheat (Austin et al. 1982) and there is considerable variation in several traits such as flag-leaf size, plant-height, and seed protein content and composition, that may be exploited for the improvement of diploid wheats. Many new sources of disease and pest resistance have been identified in diploid wheats which would be immediately usable at the diploid level. T. monococcum could become an important crop for the production of baked foods rich in carotenoids and proteins (Waines 1983; Borghi et al. 1996). Its adaptation to low-input agriculture and high level of resistance to pests and diseases represent advantages for organic farming and its gene pools may serve as a valuable reservoir of desirable genes for improvement of durum and bread wheat (Sharma et al. 1981; Megyeri et al. 2012; Zaharieva and Monneveux 2014). Since diploid wheats may be easier to manipulate than polyploid wheats in conventional breeding programs, it has gradually been recognized as an attractive diploid model for exploitation of useful traits, discovery of novel genes and variant alleles, and functional genomics (Jing et al. 2009). Currently, natural and artificially mutagenized T. monococcum are being used to identify and map genes of agronomic importance (Bullrich et al. 2002; Kuraparthy et al. 2007). Furthermore, new technologies for studying functional genomics, e.g., TILLING (Targeting Induced Local Lesions in Genomes), VIGS (Virus-Induced Gene Silencing) and DArT (Diversity Arrays Technology), are currently in use in T. monococcum (Jing et al. 2009).
Lines of T. monococcum are resistant to powdery mildew (Saponaro et al. 1995; Lebedeva and Peusha 2006), to leaf rust (Gill et al. 1983; Dyck and Bartos 1994; Saponaro et al. 1995; Anker et al. 2001), to stem rust (Gerechter-Amitai et al. 1971; Kerber and Dyck 1973; Chen et al. 2018), to eyespot (Cadle and Murray 1997), green bug (Gill et al. 1983), Russian aphid (Potgieter et al. 1991), Hessian fly (Gill et al. 1983), and wheat streak mosaic virus (Gill et al. 1983). T. monococcum has genes conferring resistance to pre-harvest sprouting (Sodkiewicz 2002).
10.2.2.4 Cytology, Cytogenetics and Evolution
T. monococcum is a diploid species (2n = 2x = 14). Its nuclear genome is a modified A genome and designated Am (Kimber and Tsunewaki 1988; Dvorak 1998), and its organellar genome is designated A in certain lines and A2, a subset of the A organellar genome, in others (Ogihara and Tsunewaki 1982, 1988; Wang et al. 1997; Tsunewaki 2009). The organellar genome of T. monococcum differs considerably from the organellar genomes of all the diploid and polyploid Aegilops species, as well as from those of the polyploid wheats (Tsunewaki 2009).
Hybrids between the two subspecies of T. monococcum, the wild ssp. aegilopoides and the domesticated ssp. monococcum, showed seven ring bivalents at meiotic first metaphase and were fully fertile (Kihara et al. 1929; Percival 1932; Smith 1936), and no differences in the restriction profiles of repeated nucleotide sequences (Dvorak et al. 1988). On the other hand, genetic, cytological and molecular evidence indicated that the two diploid wheat species, T. monococcum and T. urartu, diverged from one another. Studies of male and female fertility in hybrids and backcrosses showed that the interspecific F1 hybrid between either wild or domesticated T. monococcum (as male), and T. urartu (as female) were completely sterile and backcrosses were completely to partially sterile, indicating that T. urartu is a separate species (Sharma and Waines 1981; Waines and Payne 1987; Ciaffi et al. 1998; Castagna et al. 1994).
Takumi et al. (1993) performed RFLP analyses of the nuclear DNAs of diploid wheats and calculated the genetic distances between all the pairs of accessions from the RFLP data. Using the UPGMA method, all the accessions of T. urartu were found to cluster in one group, whereas those of wild and domesticated T. monococcum were in a second group. Similar results were obtained by Le Corre and Bernard (1995). Hammer et al. (2000) noted that microsatellite markers differentiated the wild form of T. monococcum from T. urartu. The existence of genome divergence between T. monococcum and T. urartu is also evident from extensive differences in the restriction profiles of repeated nucleotide sequences and the promoter region of the 18S-5.8S-26S rRNA genes, which show very little intraspecific variation in the Triticum species (Dvorak et al. 1993). This indication of divergence between the genome of T. monococcum and the A genome of T. urartu led Dvorak et al. (1993) to propose re-designating the genome of T. monococcum as Am.
The divergence between the two diploid wheat species, T. monococcum and T. urartu, at the molecular level is also apparent from the pattern of chromosome pairing in hybrids between them. Johnson and Dhaliwal (1978) observed a mean 6.97 bivalents at first meiotic metaphase of the F1 hybrid between T. monococcum and T. urartu and Shang et al. (1989) described 5.03 bivalents and 0.94 quadrivalents per cell in hybrids between different lines of these species, indicating that some chromosome differentiation occurred between the two species.
Meiotic pairing between T. monococcum chromosomes, when individually substituted in common wheat, and the wheat chromosomes of the A subgenome, is low in the presence of the homoeologous pairing suppressor Ph1 (Paull et al. 1994; Dubcovsky et al. 1995). Paull et al. (1994) reported on a very low level of recombination between chromosome 7Am of T. monococcum ssp. aegilopoides and 7A of T. aestivum. Likewise, Dubcovsky et al. (1995) noted that recombination between T. aestivum chromosome 1A and its closely related homoeologous chromosome 1Am of ssp. monococcum was low in the presence of the Ph1 gene. Chromosomes 1A and 1Am were shown to be colinear, and consequently, Dubcovsky et al. (1995) concluded that the Am genome of T. monococcum and subgenome A of hexaploid wheat diverged from one another by small chromosomal segments, and this amount of chromosomal differentiation is already recognized by the Ph1 gene. In the absence of Ph1, the distribution and frequencies of crossing over between the 1A and 1Am homoeologues were similar to the distribution and frequencies of crossover between 1A homologues. This indicates that some distinction exists between the chromosomes of the Am genome of T. monococcum and those of the A subgenome of common wheat.
Additional evidence on divergence between chromosome 1Am and chromosome 1A of T. aestivum was reached by Wicker et al. (2003), who sequenced and compared two-large physical contigs of 285 and 142 kb, covering orthologous low molecular weight (LMW) glutenin loci on the short arm of chromosome 1Am of domesticated T. monococcum and on the short arm of chromosome 1A of tetraploid wheat, T. turgidum ssp. durum. Sequence conservation between the two species was restricted to small regions containing the orthologous LMW glutenin genes, whereas > 90% of the compared sequences were not conserved. Dramatic sequence rearrangements occurred in the regions rich in repetitive elements. Dating of long terminal repeat retrotransposon insertions revealed different insertion events occurring in the past 5.5 million years in both genomes. These insertions are partially responsible for the lack of homology between the intergenic regions. In addition, the gene space was conserved only partially, as demonstrated by several predicted genes identified on both contigs. Duplications and deletions of large fragments that might be attributable to illegitimate recombination, also contributed to the differentiation of this region in both genomes. The striking differences in the intergenic landscape of the A subgenome versus the Am genomes, that diverged 1.28 million years ago (Li et al. 2011), provide evidence of dynamic and rapid genome evolution in wheat species.
Despite domestication of diploid wheat, both the wild and domesticated forms of T. monococcum contain a similar amount of 1C DNA (6.45 ± 0.103 pg and 6.48 ± 0.043 pg, respectively; Eilam et al. 2007). T. monococcum features one of the large genomes among the diploid species of the wheat group (the genera Ambliopyrum, Aegilops and Triticum). Only Emarginata species of Aegilops, namely, Ae. bicornis, Ae searsii, Ae. sharonensis and Ae. longissima, have larger genomes than that of T. monococcum (Eilam et al. 2007). T. urartu, the second diploid species of the genus Triticum, has a significantly smaller genome (1C DNA = 6.02 ± 0.062 pg) than that of T. monococcum (Eilam et al. 2007). The estimated amount of 1C DNA of the A subgenome of wild tetraploid wheat, T. turgidum ssp. dicoccoides, is 4.9 Gbp (= 4.79 pg) (Avni et al. 2017) and that of T. aestivum is 5.95 Gbp (=5.81 pg) (IWGSC 2018) (see Table 3.1). The A subgenome of polyploid wheat is thus smaller than that of T. urartu.
The karyotype of wild and domesticated forms of T. monococcum was studied by many cytologists. Kagawa (1929) classified the chromosomes in five groups, two-chromosome pairs had a secondary constriction. Subsequent works described only one chromosome pair with satellites, e.g., Levitsky et al. (1939), Riley et al. (1958), Upadhya and Swaminathan (1963a), Coucoli and Skorda (1966), or two pairs of satellited chromosomes, e.g., Smith (1936), Pathak (1940), Camara (1943), Oinuma (1953), Giorgi and Bozzini (1969b). Yet, it is possible that some lines of T. monococcum have only one satellited pair, as was found by Waines and Kimber (1973). These authors surveyed six biotypes of wild and domesticated T. monococcum from Europe and Iran and found variations in the number and size of the satellites. Biotypes with both one and two pairs of satellites were found, and the satellite size varied both within and between biotypes.
Giorgi and Bozzini (1969b) reported that the karyotypes of T. monococcum ssp. aegilopoides and T. urartu are very similar. Both have two chromosome pairs with small satellites. These chromosome pairs are the most hetero-brachial in the complement, with SAT 1 bearing a slightly more subterminal centromere than SAT 2. Three submedian and two median chromosome pairs were found in both species (Giorgi and Bozzini 1969b). There is good agreement between the ideogram drawn by Giorgi and Bozzini and that reported by Pathak (1940). The presence of the satellites, together with the differences in total length, relative arm length, and position of secondary constrictions, make the identification of individual chromosomes possible (Smith 1936; Giorgi and Bozzini 1969b).
Gerlach et al. (1980) hybridized labelled RNA, transcribed in vitro from wheat ribosomal DNA cloned in a bacterial plasmid, to metaphase chromosomes of accessions of diploid wheats, including the two varieties of wild T. monococcum (var. boeoticum and var. thaoudar), domesticated T. monococcum and T. urartu. Autoradiography of the chromosomes provided unequivocal evidence that these taxa possess two pairs of nucleolus organizer (NOR) chromosomes. Yet, the diploid wheat accessions used possessed widely differing numbers of ribosomal RNA genes. The two chromosomes carrying the (NORs) of T. monococcum were identified as 1Am and 5Am by the combination of in situ hybridization and cytological markers (Miller et al. 1983). Later, Dvorak et al. (1989) found that the short arms of chromosomes 1Am and 5Am of both subspecies of T. monococcum also carry the 5S rRNA genes. The locus on chromosome 1Am contains the 5S DNA subfamily with short spacers, while the locus on chromosome 5Am contains 5S DNA subfamily with long spacers. Thus, in T. monococcum, 1Am contains 360-bp units which belong to the short-unit subfamily, whereas 5Am contains 500-bp units, belonging to the long-unit subfamily. The location of the 5S DNA in the short arms of chromosomes 1Am and 5Am suggests an ancestral linkage between the NORs and the 5S DNA loci.
Evidence that the loci carrying the 5S rRNA and 18S + 26S rRNA genes are located close to one another was also obtained by Kim et al. (1993) who performed FISH with the pScT7 (5S rDNA probe from Secale cereale) and pTa80 (18S + 26S rDNA probe from T. aestivum) and observed that both probes hybridized to the sub-terminal regions of the short arms of chromosomes 1Am and 5Am in T. monococcum. Both probes labelled the pair of 1Am more heavily than those on 5Am, indicating that in T. monococcum, chromosomes 1Am carry more copies of rRNA genes than chromosomes 5Am (Kim et al. 1993). The close linkage between 18S + 26S and 5S rDNA genes in diploid wheats, (as well as in several other Triticeae species), may be due to the fact that RNAs specified by these two types of genes, which are transcribed by different RNA polymerases, are required in approximately the same amount for ribosomal formation. Hence, one advantage of them being in close proximity may be that a common regulatory mechanism ensures such equality (Kim et al. 1993).
No differences were found in the 5S rRNA restriction sites among the 12 accessions of T. monococcum and T. urartu studied with several restriction enzymes (Kim et al. 1993). Similar to the finding of Dvorak et al. (1989), Southern analysis of 5S rRNA with BamHI-digested DNA from the 12 accessions, yielded two superimposed ladders of approximate sizes of 500 and 330 bp (Kim et al. 1993). The 500-bp ladder derived from chromosome 5Am and the 330-bp ladder from chromosome 1Am.
Megyeri et al. (2012), performing FISH with the repetitive DNA probes pSc119.2, Afa family and pTa71 (rDNA probe) on mitotic chromosomes of T. monococcum, showed that the pSc119.2 probe was not suitable for the identification of T. monococcum chromosomes. On the other hand, all chromosomes were distinguishable by their Afa family signals that were observed on all chromosomes in the intercalary and distal regions, albeit, with different intensities. Strong fluorescent pTa71 signals were observed on the sub-telomeric region of the short arms of chromosomes 1Am and 5Am. A similar FISH hybridization pattern was observed in T. urartu (Molnar et al. 2014). Comparison of the hybridization pattern of the chromosomes of T. monococcum and T. urartu with those of the A subgenome chromosomes of tetra- and hexa-ploid wheat, using the same hybridization probes, showed that the chromosomes of the diploid species have more complex Afa family and pTa71 hybridization patterns than the A-subgenome chromosomes of the polyploid wheats (Molnar et al. 2014). On the other hand, the pSc119.2 signals located on chromosomes 4A and 5A of tetra-and hexa-ploid wheat were not observed on these chromosomes of the diploid wheats.
The results of Megyeri et al. (2012), Molnar et al. (2014) showed that the entire set of T. monococcum chromosomes (especially chromosomes 1, 4, 5 and 7) could be discriminated by their hybridization patterns of pTa71 and Afa family. In situ hybridization with the microsatellite motifs GAA, CAG, AAC and AGG, demonstrated that these SSRs represented additional landmarks for the identification of T. monococcum chromosomes. The most promising SSR probes were the GAA and CAG motifs, which when used in combination with the Afa family and pTa71 probes, allowed for reliable identification of the entire set of T. monococcum chromosomes and for their discrimination from the A subgenome chromosomes of polyploid wheat background (Megyeri et al. 2012).
In order to improve the identification of and localization to chromosomes useful genes, a series of primary trisomics of T. monococcum was generated from autotriploids derived from crosses between induced autotetraploids and diploids (Friebe et al. 1990). All trisomics differed phenotypically from their diploid progenitor, but only two of the seven possible trisomic types exhibited a distinct morphology enabling their identification. C-banding, Ag–NOR staining and FISH, using rDNA probes, were employed to identify the chromosomes and the trisomics of T. monococcum. A comparison of the C-banding patterns of the chromosomes of T. monococcum with those of the A subgenome of T. aestivum, enabled identification of five monococcum chromosomes, viz., 1Am, 2Am, 3Am, 5Am, and 7Am. The two remaining chromosomes, 4Am and 6Am, showed C-banding patterns that were not equivalent to those of any of the chromosomes in the A subgenome of bread wheat. When one of these undesignated chromosomes from ssp. aegilopoides var. boeoticum was substituted for chromosome 4A of T. turgidum, it compensated well phenotypically for the loss of chromosome 4A in the recipient species. Because this T. monococcum chromosome appeared to be homoeologous to the group 4 chromosomes of polyploid wheats, it was designated 4Am, and the second undesignated chromosome in T. monococcum was designated 6Am (Friebe et al. 1990).
Haploid plants (1n = 1x = 7) may be present among T. monococcum progeny (Smith 1936). Kihara and Katayama (1932, 1933), Chizaki (1934) studied meiosis in haploids of this species and found that the chromosomes often become attached end-to-end, especially during the meiotic phase of diakinesis. Kostoff and Arutiunian (1938) assumed that this phenomenon is due to associations between heterochromatic regions of non-homologous chromosomes rather than to the presence of duplications or interchanges. Indeed, Kostoff (1938) showed that the distal ends of almost all chromosomes of T. monococcum stained very dark with Newton’s gentian violet, while all the other chromosomal parts were stained much lighter. This differential staining indicates the presence of heterochromatin at the chromosome ends.
The presence of genes that either prevent crossability of lines of wild and domesticated T. monococcum with other species or that cause death of interspecific or intergeneric hybrids, was demonstrated with several hybridization events. The F1 hybrids from the T. monococcum ssp. aegilopoides (as female) x T. urartu (as male) cross yielded small, plump and viable seeds, while the reciprocal cross had long, shriveled and non-viable seeds (Johnson and Dhaliwal 1976; Dhaliwal 1977a; Fricano et al. 2014). Alloplasmic lines, where a nucleus of one species was introduced into the cytoplasm of another species, were developed through repeated backcrossing, which were then crossed as female parents with respective non-recurrent parents that were the cytoplasm donors (Dhaliwal 1977a). It was concluded that the difference between the reciprocal crosses was presumably attributable to different ssp. aegilopoides-urartu genomic ratios in the triploid endosperm rather than to cytoplasmic differences between the diploid wheats. The endosperm with two doses of the aegilopoides and one of the urartu genome resulted in small, plump and viable seeds while the endosperm of the reciprocal cross with two doses of the urartu and one of the aegilopoides genome, developed into large but shriveled and non-viable seeds irrespective of the cytoplasmic type (Dhaliwal 1977a).
Gill and Waines (1978) performed diallel crosses among four lines of T. monococcum ssp. aegilopoides from different geographical areas, with T. urartu, Ae. tauschii and Ae. speltoides and observed reciprocal differences in hybrid seed morphology, endosperm development, and embryo viability. T. urartu and Ae. tauschii as females, crossed with ssp. aegilopoides and Ae. speltoides, led to the production of shriveled inviable seed. ssp. aegilopoides accessions as female, crossed with Ae. speltoides also led to shriveled seeds. The reciprocal crosses produced plump seeds which either resembled the maternal parent or showed size differences. Altering the endospermic genome ratios was achieved by crossing an autotetraploid line of ssp. aegilopoides (2n = 4x = 28), either as female or as male, with diploid T. urartu, Ae. tauschii or Ae. speltoides. When the autotetraploid ssp. aegilopoides was the male parent and any of the diploid species was the female parent, the hybrid endosperms contained two doses from the female parent genome and two doses from the male parent genome and consequently, the seeds showed extreme shriveling. On the other hand, when the autopolyploid was the female parent and each of the diploid species was the male parent, the hybrid endosperm contained four doses from the female parent genome and one dose from the male parent genome, and consequently, the seeds were moderately shriveled to plump. Genetic experiments involving hybrids of T. monococcum (wild and domesticated forms), and T. urartu showed that a factor showing a dosage effect is present in male gametes, which, by interacting with the maternal genome, leads to endosperm abortion (Gill and Waines 1978).
Endosperm development and embryo lethality were studied in hybrids of different accessions of Ae. tauschii (as female) and the diploid wheats, i.e., wild and domesticated T. monococcum and T. urartu (Gill et al. 1981), that produced shriveled and non-viable seed. Ae. tauschii x T. urartu hybrids showed good seed development but embryos were semi-lethal and seedling death resulted. Ae. tauschii x T. monococcum ssp. monococcum hybrids showed endosperm abortion and embryos were lethal or semi-lethal. Ae. tauschii x T. monococcum ssp. aegilopoides hybrid seeds were dead by day 14. However, using embryo culture from day 10 of seed development, Gill et al. (1981) obtained viable F1 tauschii x ssp. aegilopoides plants. These authors found that the block that leads to hybrid endosperm abortion is effective between days 5 and 10 of seed development. Seed abortion in tauschii x ssp. aegilopoides crosses were seemingly primarily the result of faster, rather than abnormal, nuclear division in the hybrid endosperm. The lack of storage protein synthesis indicates that abortion of the hybrid endosperm is complete by day 10. This rapid endosperm degeneration almost certainly adversely affects the viability of hybrid embryos (Gill et al. 1981).
Sears (1944a) identified two alleles in a domesticated line of T. monococcum which acted as dominant lethals in hybrids with Ae. umbellulata, but which induced no effect in T. monococcum itself. The two alleles differed in the earliness with which they caused death. A third, normal allele that did not cause death in hybrids with Ae. umbellulata, was present in the wild form, ssp. aegilopoides . Semi-lethality occurred in hybrids of Ae. bicornis with certain varieties of domesticated T. monococcum, while hybrids with another variety of T. monococcum were viable (Sears 1944a). This effect on viability was apparently mono-factorially determined. Non-crossability of domesticated T. monococcum with Dasypyrum villosum also appears to be simply inherited (Sears 1944a).
The modes of inheritance of 12 morphological characters were investigated in domesticated T. monococcum by crosses, complementation studies, and observations of phenotypes of F1s and F2s from crosses between lines expressing the different traits (Kuspira et al. 1989). All studied traits were found to be controlled by single genes. The genes for six of these 12 characters fall into two closely linked groups; Bg (glume color) and Hg (Hairy glume) are the same distance apart in T. monococcum as in in T. aestivum, indicating that this segment has been highly conserved. The genes Sg (glume hardness), La (lemma awn length), Fg (false glume), and Lh (head type) were also very closely linked, with the outside markers being only 4 map units apart. Tentative assignments of genes and linkage groups identified in this investigation, to specific chromosomes of T. monococcum have been made on the basis of known chromosomal locations in A subgenome genes of T. aestivum (Kuspira et al. 1989).
Since cultivated and wild genotypes of T. monococcum show high levels of restriction fragment length polymorphism (RFLP) (Castagna et al. 1994; Le Corre and Bernard 1995), T. monococcum can be used to produce high-density RFLP maps that would complement the genetic maps of the A subgenome of T. aestivum. RFLP and AFLP markers have been developed and used to generate genetic linkage maps, for map-based cloning, and genome synteny comparisons in T. monococcum (Dubcovsky et al. 1995, 1996; Faris et al. 2008).
Singh et al. (2007) produced an integrated molecular linkage map of the Am genome based on 93 recombinant inbred lines (RILs) derived from a cross of wild x domesticated T. monococcum. The parental lines were analyzed with SSRs and RFLP markers, and bin-mapped ESTs. The polymorphic markers, that were assayed on the RILs, mapped on the seven linkage groups with a total map length of 1262 cM. About 58 loci, mostly mapping on chromosome 2Am, showed distorted segregation. With a few exceptions, the position and order of the markers was similar to the ones in maps of the A subgenome of polyploid wheat. Chromosome 1Am of ssp. monococcum and ssp. aegilopoides showed a small paracentric inversion relative to the A subgenome of hexaploid wheat.
Partial genetic maps of chromosomes 1Am and 5Am, constructed based on crosses between winter and spring lines of ssp. aegilopoides and between ssp. aegilopoides and ssp. monococcum, showed the same order of markers and similar interval lengths between markers (Dubcovsky et al. 1995). A map of the ssp. aegilopoides chromosome 1Am, constructed based on a winter x spring F2 population, has a similar genetic length as a map of chromosome 1A of T. aestivum (Dubcovsky et al. 1995). Additional genetic map of F2 progeny of a cross between domesticated and wild subspecies of T. monococcum involving 335 markers, including RFLP DNA markers, isozymes, seed storage proteins, rRNA, and morphological loci, was constructed by Dubcovsky et al. (1996). These authors reported that T. monococcum and barley linkage groups are remarkably conserved. They differ by a reciprocal translocation involving the long arms of chromosomes 4 and 5, and paracentric inversions in the long arm of chromosomes 1 and 4; the latter is in a segment of chromosome arm 4L translocated to 5L in T. monococcum.
Jing et al. (2007, 2009) developed Diversity Arrays Technology (DArT), consisting of 2304 hexaploid wheat, 1536 tetraploid wheat, 1536 domesticated and 1536 representative wild T. monococcum genomic clones, to assess genetic diversity in T. monococcum, and to construct a genetic linkage map integrating DArT and microsatellite markers. In total, 846 polymorphic DArT markers were identified and used to fingerprint 16 T. monococcum accessions of diverse geographical origins. The fingerprinting data showed a partial correlation between the geographic origin of T. monococcum accessions and their genetic variation. Using DArT and SSR markers, Jing et al. (2007, 2009) constructed a linkage map in F2 progeny from a cross between two different accessions of T. monococcum. In total, 356 (274 DArTs and 82 SSRs) molecular markers were mapped and formed nine linkage groups. Two morphological traits, namely awn color and leaf hairiness, were found to segregate in a 1:3 ratio in the T. monococcum mapping population. These two traits, Ba (black awn) and Hl (hairy leaf), each controlled by a single gene, were also included in the linkage analysis. The linkage map derived from the combined data set spanned 1062.72 cM, with an average length of 151.82 cM per chromosome and an average density of one marker per 2.97 cM. Each of the seven chromosomes contained both DArT and SSR markers. Six of the linkage groups corresponded to six T. monococcum chromosomes, but chromosome 4Am was formed by three linkage groups.
10.2.2.5 Crosses with Other Species of the Wheat Group
Chromosomal pairing at meiosis of both wild and domesticated forms of T. monococcum, is complete, namely, seven ring bivalents. A similar level of pairing was observed in F1 hybrids between the two subspecies of T. monococcum (Kihara et al. 1929; Perecival 1932; Smith 1936), indicating that their genomes are fully homologous. On the other hand, F1 hybrids between wild T. monococcum, ssp. aegilopoides x T. urartu (hybrid genome AmA) (Table 10.6) had somewhat reduced pairing indicates a small scale of chromosomal differentiation between the chromosomes of these two diploid wheats. Chromosome pairing in hybrids between wild or domesticated forms of T. monococcum with diploid Aegilops species of section Sitopsis (Table 9.8), showed greater genomic differentiation. The F1 hybrid between a high-pairing type of Ae. speltoides and domesticated T. monococcum (hybrid genome SAm) has more pairing than the hybrid with intermediate pairing type (Sears 1941b). This difference resulted from the promotion of homoeologous pairing by the high-pairing gene(s) of Ae. speltoides. Chromosome pairing in the F1 hybrids Ae. longissima x ssp. monococcum (hybrid genome SlAm), Ae. sharonensis x ssp. monococcum (hybrid genome SshAm), and Ae. bicornis x ssp. monococcum (hybrid genome SbAm) exhibited much reduced pairing than the hybrid with the intermediate -pairing type of Ae. speltoides (Table 9.8). While genome Am of T. monococcum diverged relatively little from the S genome of Ae. speltoides, it differed quite considerably from those of the other Sitopsis species.
Sears (1941b) studied chromosome pairing in F1 hybrids between domesticated and wild T. monococcum x several other diploid Aegilops species (Table 9.8). The domesticated T. monococcum x Ae. tauschii hybrid (hybrid genome AmD), exhibited more pairing than the hybrid with wild monococcum. The lower level of chromosomal pairing in the hybrid with wild T. monococcum may result from the presence of gene(s) affecting pairing in the wild line used for this cross. The F1 hybrids between ssp. monococcum x Ae. caudata, ssp. aegilopoides x Ae. caudata (hybrid genome AmC), ssp. monococcum x Ae. comosa, ssp. aegilopoides x Ae. comosa (hybrid genome AmM), a ssp. monococcum x Ae. uniaristata, ssp. aegilopoides x Ae. uniaristata (hybrid genome AmN), and ssp. aegilopoides x Ae. umbellulata (hybrid genome AmU) had reduced pairing (Table 9.8). The above data showed that genome Am of T. monococcum, either domesticated or wild, had extensively diverged from these genomes of Aegilops.
Chromosome pairing between alltetraploid wheat, i.e., various subspecies of T. turgidum and T. monococcum, either ssp. monococcum or ssp. aegilopoides, (hybrid genome BAAm), domesticated T. timopheevii x ssp. monococcum (hybrid genome GAAm), and ssp. aestivum x ssp. monococcum (hybrid genome BADAm) was studied by several cytogeneticists (Table 10.6). Pairing in all these F1 hybrids show that the allotetraploids and the allohexaploid wheats contain a subgenome related to the Am genome of T. monococcum.
10.2.3 T. urartu Tum. ex Gand. (Donor of the A Subgenome to Allopolyploid Wheats)
10.2.3.1 Description of the Species
T. urartu Tum. ex Gand., common names red wild einkorn and urartu wheat [Syn.: T. boeoticum ssp. urartu Dorof.; T. monococcum ssp. urartu (Tum. ex Gand.) Á. Löve and D. Löve; Crithodium urartu (Gandilyan) Á. Löve], is an annual, predominantly autogamous, 60–90-cm-tall (excluding spikes) plant. Its culms are first geniculated and then ascending upright. Culm internodes are distally glabrous. The leaf sheaths are pubescent, their auricles are curved, and the ligule is membranous. Leaf blades are 30–45-cm-long. The spike is indeterminate, bilaterally compressed, two-rowed, 7–11(–13) cm-long (excluding awns) and awned. The entire spike disarticulates at maturity into individual spikelets, each with its associated rachis segment (wedge–type dispersal unit). The rachis is densely hairy on margins and sparsely hairy at nodes. The spikelets are laterally compressed, 17–20-mm-long, the top one being fertile and generally in the same plane as those below it. There are 8–16 fertile spikelets per spike, and 1–2 basal rudimentary spikelets. There are 3 florets, the upper one being sterile. The spikelets usually have two grains and two 2.5–5.5 cm-long awns. The glumes are shorter than the spikelet, 11.2–11.6-mm-long, glabrous, with two well-developed keels, and 3–5 -veins. There are two unequal teeth, which usually do not develop into awns, with one tooth being well developed and the second less. The lemma are glabrous, 13–15-mm–long, keeled, taper into an awn, and bear a lateral small tooth. The palea is 11–13-mm-long, membranous and splits along the keel at maturity. The anthers are small, 2.0–2.5-mm-long. The caryopsis has a reddish color, is 7.3–9.2-mm-long, and is free but laterally compressed by the tough glumes (Fig. 10.1c).
T. urartu was discovered by Tumanian (1937) in Armenia, who distinguished it from the other wild diploid wheat T. monococcum ssp. aegilopoides, by the following morphological features: its smaller second tooth of the glume, smaller anthers, two-awned two-grained spikelets and red grains (Gandilian 1972; Dorofeev et al. 1980). Johnson (1975), who discovered T. urartu in northern Lebanon, southeastern Turkey, and southwestern Iran, found that this species also differs from ssp. aegilopoides by the electrophoretic pattern of seed Beta albumin. He described additional morphological differences between T. urartu and ssp. aegilopoides, namely, the awns of T. urartu are shorter and slenderer than those of ssp. aegilopoides, they are nearly equal and spread at maturity. T. urartu is most easily identified by the presence of an awn up to 1-cm-long on the lemma of the third floret (Johnson 1975). In several locations, this awn was often reduced to an inconspicuous bristle, but in Johnson’s fields and a greenhouse at Riverside, California, it was discernible in all accessions of this species. With respect to plant and spikelet size, the Turkish populations provide a transition between the Lebanese biotypes and the more robust one of Transcaucasia, Iraq and Iran. Both in the wild and under cultivation, T. urartu from all parts of its range, except Transcaucasia, was found to generally mature earlier than ssp. aegilopoides (Johnson 1975).
The two diploid wheats, T. urartu and the wild and domesticated forms of T. monococcum, also differ by biochemical and molecular markers such as isoenzymes of ACP (Jaaska 1974), EST (Jaaska 1980), SOD (Jaaska 1982), by the composition of the seed storage proteins, namely, the high-molecular weight (HMW) glutenin subunits (Waines and Payne 1987; Ciaffi et al. 1998; Castagna et al. 1994), and Gliadin genes (Ciaffi et al. 1997). In addition, AFLP (Sasanuma et al. 2002; Heun et al. 2008) and RFLP (Takumi et al. 1993; Le Corre and Bernard 1995) analyses of nuclear DNAs of T. urartu and T. monococcum revealed differences between these two species. AFLP and simple sequence length polymorphism (SSLP) analyses clearly showed that T. urartu was greatly differentiated from both the wild and domesticated forms of T. monococcum (Sasanuma et al. 2002). A similar conclusion was reached following chloroplast SSLP analysis (Mizumoto et al. 2002). Comparable results were also obtained by Hammer et al. (2000), who found that microsatellite markers (SSRs) differentiated the wild form of T. monococcum from T. urartu. Furthermore, Baum and Baily (2004) found that T. urartu differs from T. monococcum in the short and long units of the 5S DNA; T. monococcum contained the long A1 and the short A1 unit classes, whereas T. urartu had the long A1 and the short G1 unit classes. Likewise, Dvorak et al. (1988, 1993) found extensive differences between these two species in the restriction profiles of repeated nucleotide sequences and the promoter region of the 18S-5.8S-26S rRNA genes.
Phase-contrast microscopy and scanning electron microscopy measuring the pollen grain diameter and examining the exine (the outer layer of the pollen grain) sculpturing of T. urartu and T. monococcum ssp. aegilopoides var. thaoudar (López-Merino et al. 2015), found that T. urartu pollen is smaller on average than that of var. thaoudar, and its exine sculpturing differs from that of var. thaoudar.
The divergence between T. urartu and T. monococcum is also apparent from the cytogenetic data; chromosome pairing in the F1 hybrids between the two species was somewhat reduced (Johnson and Dhaliwal 1978; Shang et al. 1989) and the hybrid was completely sterile when T. urartu served as the female parent (Johnson and Dhaliwal 1976). Hence, gene flow via hybridization between these two species can occur only from T. urartu into T. monococcum (Johnson and Dhaliwal 1976). Tsunewaki et al. (1999) found that T. urartu, when used as female, showed strong cross incompatibility to emmer wheat, differing, in this respect, from T. monococcum ssp. aegilopoides, which crosses relatively easily with emmer wheat. All the above biochemical, molecular and cytogenetic data revealed the existence of a profound genome divergence between T. urartu and T. monococcum and thus, substantiating their classification into two separate species.
T. urartu exhibits wide morphological variation in spike and spikelet size, color and hairiness (Johnson 1975). This variation is also expressed at the biochemical and molecular levels. While Smith-Huerta et al. (1989), using isoenzymes, observed low genetic diversity, Yaghoobi-Saray (1979), Moghaddam et al. (2000), Hedge et al. (2000) reported a high level of isoenzyme diversity, either within or among populations. Studies at the molecular level also revealed high intra- ad inter-population variation in T. urartu. Sasanuma et al. (2002), Singh et al. (2006), using AFLP, revealed variation in all analyzed accessions of T. urartu. Similar results were obtained by Brunazzi et al. (2018), who genotyped a collection of 352 accession of T. urartu, sampled from Armenia, Iran, Iraq, Jordan, Lebanon, Syria and Turkey, with a large number of high-quality genome-wide single nucleotide polymorphisms (SNPs), and revealed broad molecular variation across the sampled populations. In addition, Brunazzi et al. (2018) obtained phenotypic data that highlighted a wide variation for flowering time and plant height. Storage protein analysis indicated the presence of highly polymorphic protein bands, while SDS sedimentation tests showed broad variability in the dough volume, even including some accessions approaching good bread-making quality (Brunazzi et al. 2018). These researchers used 1.3 million genome‐wide SNPs to assess variation in a large collection of T. urartu accessions. They found a correlation between the amount of genetic diversity and the geographical distance existing between samples from different regions. Using a genome‐wide association approach, they identified several marker-environment associations, such as association of molecular markers with altitude, temperature, and/or association with rainfall measures. The most significant marker–environment associations were observed with genomic loci with adaptive potential, including dormancy and frost resistance loci.
A high level of genetic diversity was found in low-molecular weight (LMW) glutenin subunits from T. urartu, that are coded by the Glu-A3 locus on chromosome 1A, including detection of 11 novel alleles (Cuesta et al. 2015). Wang et al. (2017) investigated the morphological and genetic diversity and population structure of 238 T. urartu accessions collected from different geographic regions. They found wide variation in SSR markers and in HMW-glutenin subunits. Their analysis indicated that the 238 T. urartu accessions could be classified into two subpopulations, of which Cluster I contained accessions from the Eastern Mediterranean coast, while those from Mesopotamia and Transcaucasia belonged to Cluster II. Significant associations were observed between SSRs or HMW-GSs and six morphological traits: heading date, plant height, spike length, spikelet number per spike, tiller angle and grain length.
T. urartu distributes abundantly in southeastern Turkey, Syria and Lebanon and sporadically in northern Iraq, western Iran and Armenia (Johnson 1975). Recently, it was also discovered in the high mountains of southern Jordan. T. urartu is not found west of the Fertile Crescent arc. In this respect, it also differs from ssp. aegilopoides, which spread westwards as a weed. The chorotype (the general range of distribution of a species characterizing its phytogeographical nature) of T. urartu is sub-Mediterranean-west Irano-Turanian. It grows in a relatively large area, in a wide range of altitudes (500–1600 m), occurs naturally in openings of oak park-forests, in open herbaceous formations, and in steppe-like formations. It thrives well on terra rossa, basalt, and on several types of alluvial soils. T. urartu is more adapted to dry climates than ssp. aegilopoides (Mac Key 2005). Studies on heat and cold tolerance in wild and domesticated wheat forms by Damania and Tahir (1993), revealed that T. urartu was significantly more cold-tolerant than other wild wheat taxa.
T. urartu often grows mixed with T. monococcum ssp. aegilopoides and wild emmer, T. turgidum ssp. dicoccoides, in southwestern Syria, southeastern Lebanon and in some sites in southeastern Turkey, and with wild T. timopheevii in southeastern Turkey, northern Iraq, southwestern Iran and Transcaucasia. It also grows sympatrically with Ae. speltoides, Ae. searsii, Ae. caudata, Ae. umbellulata, Ae. geniculata, Ae. biuncialis, Ae. triuncialis and Ae. columnaris and allopatrically with Ae. longissima, Ae. peregrina, Ae. tauschii, Ae cylindrica and Ae. crassa.
Being the donor of the A subgenome to allopolyploid wheats (Chapman et al. 1976; Dvorak 1976), many of the chromosomes of T. urartu pair regularly with their homologous chromosomes of allopolyploid wheats in the F1 hybrids between them, and therefore, desirable genes can be transferred from the wild diploid species to the domesticated allopolyploid species via conventional plant breeding procedures. Thus, searching the germplasm of T. urartu for economically useful traits is very important.
T. urartu contains genes conferring resistance to powdery mildew (Hovhannisyan et al. 2011; Qiu et al. 2005; Ling et al. 2018), leaf rust (Hovhannisyan et al. 2011), stem rust (Rouse and Jin 2011), yellow rust (Xiao et al. 2018), and cereal aphids (Radchenko 2011). T. urartu might provide some glutenin subunit genes to improve the quality of common wheat dough (Luo et al. 2015; Cuesta et al. 2015).
10.2.3.2 Cytology, Cytogenetics and Evolution
T. urartu is a diploid species (2n = 2x = 14). Its nuclear genome is designated A, which differs from the Am genome of T. monococcum (Dvorak 1998). Based on the restriction fragment pattern of its chloroplast DNA, its organellar genome was assigned A (Tsunewaki and Ogihara 1983). The cytoplasm of T. urartu and T. monococcum have identical chloroplast DNA (Tsunewaki and Ogihara 1983).
T. urartu contains 6.02 ± 0.062 pg 1C DNA (Eilam et al. 2007). While there is little variation in the amount of 1C DNA at the intraspecific level, the genome of T. urartu is significantly smaller than that of T. monococcum, Ae. bicornis, Ae. searsii, Ae. sharonensis and Ae. longissima and significantly larger than that of Amblyopyrum muticum, Ae. tauschii, Ae. caudata, Ae. comosa, Ae. uniaristata and Ae. umbellulata (Eilam et al. 2007).
The karyotype of T. urartu is very similar to that of T. monococcum, with small differences in the length of the short and long arms of several chromosome pairs (Giorgi and Bozzini 1969b). It consists of two chromosome pairs with small satellites, and three pairs with submedian and two with median centromeres. A similar karyotype of T. urartu was reported by Kerby and Kuspira (1988). T. urartu possess two pairs of nucleolus organizer (NOR) chromosomes (Gerlach et al. 1980), which were identified as 1A and 5A by the combination of in situ hybridization and cytological markers (Miller et al. 1983). The number of rRNA genes in T. urartu was estimated to be somewhat smaller than 4500 (Gerlach et al. 1980).
The karyotypes of T. urartu and T. monococcum were examined using C-banding and FISH, with DNA probes representing 5S and 45S rDNA families, the microsatellite sequences GAAn and GTTn, the pSc119.2, Spelt52, Fat, pAs1 and pTa535 probes, and a newly identified repeat called Aesp_SAT86 (Badaeva et al. 2015). The C-banding pattern of T. urartu was similar to that of T. monococcum, except for differences in chromosomes 4A and 6A. Besides two major 45S rDNA loci on the short arms of chromosomes 1A and 5A, two-minor polymorphic NORs were observed in the terminal part of the long arm of chromosomes 5A and in the distal part of the short arm of chromosomes 6A in T. urartu and in T. monococcum. An additional minor locus was found in the distal part of the long arm of chromosomes 7A of T. monococcum, but not in T. urartu. Two 5S rDNA loci were observed in the short arms of chromosomes 1A and 5A. The pTa535 probe displayed species- and chromosome-specific hybridization patterns, enabling full identification of all T. urartu chromosomes. The distribution of pTa535 on the chromosomes of T. urartu was more similar to its distribution on the A-subgenome chromosomes of wild T. turgidum and wild T. timopheevii, confirming the origin of these subgenomes from T. urartu. The probe pAs1 allowed for the identification of four chromosomes of T. urartu and two of T. monococcum. The Aesp_SAT86-derived patterns were polymorphic; main clusters were observed on chromosomes 1A and 3A of T. urartu. The study of Badaeva et al. (2015) showed that a set of the above probes proved to be most informative for the analysis of A genomes in diploid and allopolyploid wheat species.
Johnson and Dhaliwal (1976) demonstrated that T. urartu is isolated from T. monococcum through a genetic barrier. ssp. aegilopoides (as female) x T. urartu (as male) produced seeds with germination capacity, whereas the F1 hybrid from the reciprocal cross, produced inviable seeds (Johnson and Dhaliwal 1976; Dhaliwal 1977a). Indeed, the T. urartu x T. monococcum hybrids, involving either wild or domesticated forms, were completely self-sterile (Johnson and Dhaliwal 1976). These authors proposed that the reproductive isolation between T. urartu and T. monococcum is cytoplasmic, but Dhaliwal (1977a), suggested that the difference between the reciprocal crosses can be attributed to different monococcum-urartu genomic ratios in the triploid endosperm of the F1 hybrid rather than to the cytoplasmic difference between these diploid wheats.
Johnson (1975) discovered that the electrophoretic pattern of seed proteins of allotetraploid wheat contains B albumin bands similar to those of T. urartu. He mistakenly proposed that T. urartu is the donor of the B subgenome of the allopolyploid wheats. Chapman et al. (1976), Dvorak (1976), based on chromosome pairing in hybrids between ditelosomic lines of T. aestivum and T. urartu, concluded that the genome of T. urartu is homologous to the A subgenome of allopolyploid wheats, and that it did not correspond, as had been proposed by Johnson (1975), to the B subgenome. In contrast, chromosome pairing in the hybrid ditelosomic lines of T. aestivum x T. monococcum ssp. aegilopoides showed that the genome of T. monococcum is homoeologous, rather than homologous, to the A subgenome of allohexaploid wheat (Chapman et al. 1976). Moreover, from the higher trivalent frequencies observed in the latter hybrids, Chapman et al. (1976) concluded that the genotype of ssp. aegilopoides has the capacity to partly suppress the activity of the Ph1 locus of common wheat, allowing for some homoeologous pairing to occur. Dvorak (1976) noted that pairing of T. urartu chromosomes was significantly reduced in hybrids lacking chromosome arms 5AS or 5BS of T. aestivum. He suggested that this reduction in chromosome pairing resulted from the absence of genes which promote pairing and which are normally present on chromosome arms 5AS and 5BS in cultivar Chinese Spring of T. aestivum.
Further evidence supporting the idea that T. urartu is the donor of the A subgenome of the allopolyploid wheats, came from biochemical and cytogenetic studies. Konarev et al. (1979), Konarev (1983) concluded from immunochemical and electrophoretic studies of seed proteins, that the A subgenome of T. turgidum was contributed by T. urartu, whereas the A subgenome of T. timopheevii was contributed by T. monococcum. Yet, Nishikawa (1983), based on variation in esterases, showed that the A subgenome in both T. turgidum and T. timopheevii was contributed by T. urartu. Kerby et al. (1988) compared the amino acid sequence of T. urartu purothionin to the amino acid sequences of the purothionins in T. monococcum, T. turgidum and T. aestivum, and found that the sequence of the purothionin from T. urartu is identical to the β form specified by a gene in the A subgenome of the allpolyploid wheats and differs by five and six amino acid substitutions, from the α1 and α2 forms coded for by genes in the B and D subgenomes, respectively. Their results showed that T. urartu, rather than T. monococcum, is the source of the A subgenome in T. turgidum and T. aestivum. Phylogenetic analyses based on whole genome sequences suggest that the wheat A sub-genome diverged from T. urartu 1.28 MYA (Li et al. 2022). It might be therefore that an urartu-closely related species, unknown or now extinct, is in fact the progenitor of the A subgenome that hybridized with the B-donor ~ 0.8 MYA.
The data of Dvorak et al (1988, 1993), from variation in repeated nucleotide sequences, substantiated Nishikawa’s (1983) hypothesis, that the A subgenome in both tetraploid and hexaploid wheat is more related to the A genome of T. urartu than to the Am genome of T. monococcum. In T. zhukovskyi, one A subgenome was contributed by T. urartu and the other by T. monococcum (Dvorak et al. 1993). Takumi et al. (1993), using RFLP analysis of diploid and polyploid wheats, also concluded that T. urartu is the donor of the A subgenome to allopolyploid wheats, and Baum and Bailey (2004), based on 5S DNA unit classes, supported the view that the A subgenome of T. turgidum and T. aestivum was donated by T. urartu. Similarly, Badaeva et al. (2015) found that the pattern of FISH sites with the probe pTa535 confirmed the T. urartu origin of the A subgenome in T. turgidum and T. timopheevii. As the donor of one of the subgenomes of polyploid wheat, recognition of the genome structure, function, and diversity of T. urartu may provide important information for understanding the genomes of tetraploid and hexaploid wheats.
Ling et al. (2018), using technologies like bacterial artificial chromosome (BAC)-by-BAC sequencing, single-molecule, real-time, whole-genome shotgun sequencing, linked read sequencing and optical mapping, assembled a high-quality sequence of the T. urartu genome. This genome sequencing very much improved the draft genome of this species published earlier by Ling et al. (2013). See Sect. 3.3 in Chap. 3 and Table 3.1 for details on T. urartu genome structure. The genome of T. urartu includes 37,516 HC genes and 3991 LC genes. On average, the genes have a transcript length of 1453 bp, protein length of 332 amino acids and 4.5 exons per transcript, which is comparable to genes in other Triticeae species. Throughout the genome, Ling et al. (2018) identified 31,269 miRNAs, 5810 lncRNAs), 3620 tRNAs, 80 rRNAs and 2,519 snRNAs. A total of 3.90 Gb (81.42%) of genome sequences was identified as repetitive elements, including 3.44 Gb (71.83%) retrotransposons and 355 Mb (7.41%) DNA transposons. Among long-terminal repeat (LTR) retrotransposons, the Gypsy and Copia super families comprised 42.71% and 24.30% of the genome, respectively. The distribution of Copia elements was enriched at both telomeric and sub-telomeric regions, whereas Gypsy retrotransposons were enriched in the pericentromeric–centromeric regions. Comparative analyses with genomes of other grasses showed gene loss and amplification in the number of transposable elements in the T. urartu genome. T. urartu-specific or wheat-specific amplification of gene families was associated with stress response or vernalization. Large-scale retrotransposon-mediated structural rearrangements occurred during A-genome evolution, as revealed by comparing the A genomes among T. urartu and tetraploid and hexaploid wheat.
Ling et al. (2018) found substantially higher gene density and recombination rates, as well as lower densities of transposable elements and tandem repeats, in the sub-telomeric regions of each chromosome. The accumulated gene expression level was higher in the sub-telomere than in the centromere regions. Analyses of genes in the T. urartu genome, together with those from rice, maize, sorghum and Brachypodium, clustered the genes into 24,860 gene families. Of these, 10,681 families were shared among the five examined cereal genomes, representing a core set of genes across these grass genomes. There were 4610 genes from 1567 gene families that were specific to T. urartu, many of which have functional gene ontology annotations relating to responses to stimulus and stress.
Upon comparison of the T. urartu genome to the draft sequences of three subgenomes of hexaploid wheat, Ling et al. (2018) identified three large structural variations, with clearly defined boundaries, that occurred in either T. urartu or T. aestivum. They aligned the T. urartu genome with sequences from six BACs of the A subgenome of T. turgidum and eleven BACs from the A subgenome of T. aestivum, and found that the unaligned regions between the BAC and the T. urartu genomic sequences resulted from the insertion of LTR retrotransposons in either T. urartu or T. turgidum and/or T. aestivum. Furthermore, they compared the chromosome 7 assembly of the A subgenome of T. aestivum to T. urartu chromosome 7 and found that 655 Mb (91.03%) and 536 Mb (90.06%) of T. urartu 7 and T. aestivum 7A sequences, respectively, were aligned to each other at a minimum identity of 90% or lower, with many unaligned retrotransposon regions. These results show that the different wheat A genomes underwent large-scale rearrangements with other genomes, and experienced independent gain or loss of LTR retrotransposons after the allopolyploidization event.
10.2.3.3 Crosses with Other Species of the Wheat Group
Most F1 hybrids between different accessions of T. urartu exhibited seven bivalents at first meiotic metaphase, of which the greater part was ring bivalents (Shang et al. 1989). As was already stated above, the F1 hybrid between ssp. aegilopoides, the wild form of T. monococcum, and T. urartu (hybrid genome AmA) displayed almost complete chromosomal pairing at meiosis (Table 10.6). Chromosome pairing in the F1 hybrids T. urartu x Ae. tauschii (hybrid genome AD), Ae. comosa x T. urartu (hybrid genome MA), and Ae. umbellulata x T. urartu (hybrid genome UA) was much lower (Table 9.8). The hybrid with Ae. tauschii had somewhat higher pairing that the other two hybrids.
Data on chromosomal pairing in the F1 hybrid between allotetraploid wheat T. turgidum ssp. dicoccon and T. urartu, and between hexaploid wheat T. aestivum ssp. aestivum and T. urartu are presents in Table 10.6. The formation of about six bivalents in these hybrids, that contain the Ph1 gene of the allopolyploid wheats, shows, as was found by Chapman et al. (1976), Dvorak (1976), that most of the chromosomes of T. urartu are homologous to those of the A subgenome of the allopolyploid wheats.
10.3 Section Dicoccoidea Flaksb. (2n = 4x = 28)
10.3.1 Description of the Section
Section Dicoccoidea Flaksb. (Syn.: Triticum L. sect. Spelta Dumort; Triticum L sect. Orthatherum Nevski; Triticum L. ‘congregatio’ Tetraploidea Flaksb.) contains two species, T. turgidum L. and T. timopheevii (Zhuk.) Zhuk., which are morphologically similar (Tanaka and Ishii 1973) but genetically isolated (Lilienfeld and Kihara 1934; Kostoff 1937a; Wagenaar 1961a). The species are allotetraploids, with a shared subgenome A, and differ by the other subgenome, B in T. turgidum and G in T. timopheevii (Lilienfeld and Kihara 1934). Hence, the genome of T. turgidum is designated BBAA and that of T. timopheevii is GGAA. The cytoplasms of the allotetraploids derived from the diploid donors of the B or G subgenome, namely, that of T. turgidum derived from one genotype of Ae. speltoides, or rather, from a species that is closely related to Ae. speltoides, and that of T. timopheevii derived from another genotype of Ae. speltoides (Gornicki et al. 2014). Both species contain wild and domesticated subspecies. T. turgidum contains one wild subspecies, ssp. dicoccoides (Körn. ex Asch. & Graebn.) Thell., one domesticated fossil taxon, ssp. parvicoccum Kislev, and seven domesticated subspecies, including the important crop ssp. durum. T. timopheevii contains one wild subspecies, ssp. armeniacum (Jakubz.) van Slageren, and one domesticated subspecies, ssp. timopheevii. The wild subspecies of T. turgidum grows in the southwestern, central and northeastern part of the Fertile Crescent arc, whereas the wild subspecies of T. timopheevii grows in the northeastern part of the Fertile Crescent arc and in Transcaucasia (Kimber and Feldman 1987; van Slageren 1994). The two-wild subspecies grow sympatrically in some sites in southeastern Turkey, northern Iraq and western Iran (Harlan and Zohary 1966). The domesticated form of T. timopheevii is grown as a small crop in western Georgia. In contrast, ssp. durum of T. turgidum, is the second most cultivated crop of wheat, constituting 5–8% of global wheat production (Boyacioglu 2017). It is cultivated in many regions of the world and mainly used for pasta. The other extant six subspecies of T. turgidum are locally grown.
10.3.2 T. turgidum (L.) Thell. (Genome BBAA)
10.3.2.1 Description of the Species
Triticum turgidum (L.) Thell. is an annual, predominantly autogamous, 40–160-cm-tall (excluding spikes) plant. Culms are erect, stiff, and glabrous, with nodes that are sometimes hairy, hollow lower internodes, and generally solid uppermost nodes. Leaf blades are flat, linear, pointed, and up to 60-cm-long, with short auricles and membranous ligule. Spikes are bilaterally compressed, dense, determinate, two-rowed, parallel, 3–14-cm-long (excluding awns) and awned. In the wild form, the rachis is fragile and the entire spike disarticulates at maturity into individual spikelets, each with its associated rachis segment (wedge-type dispersal unit). In the domesticated forms, the rachis is tough and, consequently, the spike remains intact on the culm. In the wild form, the rachis has hairs on its margins, with a tuft of hair up to 5 mm long at each node, whereas in the domesticated forms, the hairs are shorter or entirely absent. The spikelets are 14–15-mm-long, solitary at nodes, lanceolate, appressed to the rachis, and glabrous or hairy, with the top spikelet being fertile, and at right angles to the plane of the lateral spikelets. There are 5–18 fertile spikelets, with 3 florets in the wild form, and up to 6 florets in several domesticated forms; the upper floret is usually sterile. There are 2–3 basal rudimentary spikelets. The glumes are oblong, similar in size, shorter than the spikelet, usually glabrous, 8–13-mm-long, with 2 strong keels and 5–7 veins, and two teeth on the upper margin, one larger and pointed and separated from the other by an acute angle. Lemma is 10–12-mm-long, without keels, with 9–11 veins, and a central vein prolonged to an awn, 15–20-cm–long, flattened, straight, and with a small basal tooth. The palea is membranous, and splits along the keel at maturity. Usually there are two grains per spikelet, but in several domesticated forms, there are up to 5 grains. Caryopsis is 5–11-mm-long, and free but adherent to the lemma and palea (hulled). In several domesticated forms, the caryopsis is not adherent to the lemma and palea (free-threshing, naked), and is hairy at the apex. The embryo approximately 1/5 the length of the caryopsis (Fig. 10.2).
A natural stand, plant and spike of wild emmer T. turgidum L. ssp. dicoccoides (Körn. Ex Asch. & Graebn.) Thell. and spikelets disseminated on the soil
The T. turgidum species is subdivided into nine subspecies: one wild, ssp. dicoccoides (Körn. ex Asch. & Graebn.) Thell. (Known as wild emmer), and eight domesticated subspecies, namely, two are primitive hulled forms, ssp. dicoccon (Schrank) Thell. (Known as domesticated emmer) and ssp. paleocolchicum (Menabde) Á. Löve and D. Löve (known as Georgian wheat), one currently extinct free-threshing form, ssp. parvicoccum Kislev, one major commercial free-threshing form, ssp. durum (Defs.) Husn. (Known as macaroni, hard wheat, or durum wheat), and four free-threshing forms that are locally cultivated, ssp. turgidum (rivet, cone, or pollard wheat), ssp. polonicum (L.) Thell. (Polish wheat), ssp. turanicum (Jakubz.) Á. Löve and D. Löve (Khorassan wheat), and ssp. carthlicum (Nevski) Á. Löve and D. Löve (Persian wheat). The wild subspecies of T. turgidum is morphologically similar and genetically closely related to the domesticated subspecies, and the F1 hybrids between them are fully or almost fully fertile. Therefore, all these wheats are included in a single biological species, T. turgidum.
Both the wild and the domesticated forms exhibit wide morphological, cytological and molecular variation. The morphological variation involves mainly spike, spikelet size and shape, glume and awn color and hairiness, grain color and size, plant height, and leaf width. In many habitats in north Israel, Jordan, and in south Syria, wild emmer wheat displays a large number of forms assembling conspicuously polymorphic populations that are easily noted by their variation in glume hairiness, spike color, spikelet size, and leaf shape (Poyarkova 1988; Poyarkova and Gerechter-Amitai 1991; Zohary et al. 2012). Hybrids between wild emmer and most of the domesticated subspecies of T. turgidum, are fertile; the chromosomes pair regularly or almost regularly and give every indication of a close relationship (e.g., von Tschermak 1914; Percival 1921; Rao and Smith 1968; Tanaka and Ichikawa 1972; Rawal and Harlan 1975; Dagan and Zohary 1970).
10.3.2.2 Ssp. dicoccoides (Körn. ex Asch. & Graebn.) Thell. (Wild Emmer)
10.3.2.2.1 Description of the Subspecies
T. turgidum ssp. dicoccoides, known as wild emmer wheat, and two-grained wild wheat (called in Hebrew the mother of wheat), [Syn.: T. vulgare Vill. var. dicoccoides Körn.; T. dicoccoides (Körn. ex Asch. & Graebn.) Schweinf.; T. sativum Lam.; T. dicoccon (Schrnk) Schübler var. dicoccoides Körn. ex Ascher. & Graebn.; T. hermonis Cook; T. turgidum L. var. dicoccoides (Körn in Schweinf.) Bowden] is an annual, predominantly autogamous, 65–100-cm-tall (excluding spikes) plant. Culms are prostrated or, rarely, erect, stiff, with a glabrous or pubescent sheath, and with nodes that are sometime hairy, hollow lower internodes and generally solid uppermost internodes. Leaf blades are flat, linear, pointed, and up to 60-cm-long, with short auricles and a membranous ligule. The spike is rigid, bilaterally compressed, dense, determinate, two-rowed, parallel, 3–10-cm-long (excluding awns) and awned. The rachis is brittle and the entire spike disarticulates at maturity into individual spikelets, each with its associated rachis segment (wedge-type dispersal unit). The rachis of the ripe spike disarticulates on the slightest shake, with the spikelets near the apex detaching first, and the others breaking off in orderly succession towards the base. The rachis has hairs on its margins, with a tuft of white, yellow or brown hair, up to 5-mm-long at each node. Spikelets are 14–15-mm-long, solitary at the nodes, lanceolate, appressed to the rachis, and glabrous or hairy, with the top spikelet being fertile and at right angle to the plan of the lateral spikelets. There are 5–15 fertile spikelets, with 3 florets, the upper floret usually being sterile, or rarely fertile. There are 2–3 basal rudimentary spikelets. The glumes are rigid, similar in size, 10–13-mm-long, shorter than the spikelet, with a strong keel and 5–7 veins; the strongest vein converges towards the base of the apical tooth, where it ends in a secondary tooth which, in some specimens is 5 mm long, very short in others. The glume color is either yellow, white, red, uniformly black, or striped along the margins or spotted irregularly with dark brown, and either glabrous or pubescent. The lemma is boat-shaped,10–13-mm-long, without keels, with 9–11 veins, and membranous and slightly divided near the apex, with a central vein prolonged as a strong and long awn, 10–20-cm–long, flattened, straight, and a small basal tooth. Awns are always present on the two lemmas of the fertile spikelets and are often of nearly equal dimensions. The epidermis of the awns is covered with hard and sharp silicified hairs that form a rugose structure, protecting the grains from grazers. Moreover, these hairs serve as a sort of rachet that propels the dispersal unit, the spikelet, into the ground upon cyclic bending of the awns caused by changes in humidity during the day (Elbaum et al. 2007). The palea is as long as the lemmas, and membranous and splits at the tip at maturity, and with two veins and two keels. The flowers have purple or yellow anthers. Usually there are two, rarely three, grains per spikelet. The caryopsis is 7–11-mm-long, free but adherent to the lemma and palea (hulled), hairy at the apex, with white 1–1.5-mm-long hairs. The embryo approximately 1/5 the length of the caryopsis. In each spikelet, the grain of the lower flower is smaller than that of the second flower, and with a somewhat darker color. The upper grain in each spikelet germinates in the first fall, but the lower one remains dormant for one year. This dispersal in time of germination prevents competition between seedlings that derived from seeds of the same spikelet (Fig. 10.2).
Glume color and pubescence led researchers to subdivide wild emmer into several intra-specific forms. Aaronsohn (1909) noted the following forms: white-eared, black-eared with black awns, red-eared, and black-eared with white awns. Flaksberger (1915) subdivided wild emmer into three varieties, but Percival (1921) defined the following five varieties: var. kotschyanum Percival (glumes white and glabrous), var. fulvovillosum Percival (glumes white and pubescent), var. aaronsohni (Flaksb.) Percival (glumes pinkish-red and glabrous), var. spontaneonigrum (Flaksb.) Percival (glumes uniformly black or striped and glabrous), and var. spontaneovillosum (Flaksb.) Percival (glumes black or striped and pubescent). The latter variety is rare. All the varieties grow sympatrically but some populations containing only one or two varieties.
10.3.2.2.2 Geographical Distribution and Ecological Requirements
Geological, climatic, and archaeological data from the east Mediterranean region indicate the presence of wild emmer wheat during periods of changing climates. Indeed, it was found during the Last Glacial Maximum period ~ 23,000 years ago on the shores of the lake of Galilee (Snir et al. 2015). Following this cold period, temperatures raised and dropped again ~ 12,000–10,300 years ago, during the Younger Dryas or “Big Freeze”, an extreme event of rapid change of climate characterized by cold and dry weather, returning to present-day temperatures ~ 10,300 years ago (for details see Hillman 1996; Bar-Matthews et al. 1997; Bar-Yosef 1998). Hillman (1996), using paleo-botanical data, reconstructed the phytogeographic belts of this region during the Younger Dryas, and concluded that the habitats of the annual cereals lay mainly in the open areas of the oak-park forest, in a relatively narrow strip of the east Mediterranean. This narrow strip, known as the “Levantine Corridor”, begins in the southern Taurus foothills (Diyarbakir area) in southeastern Turkey and extends along the Mediterranean southward, incorporating the middle Euphrates through the Damascus basin, the Lebanese mountains, and the two sides of the Jordan Rift Valley into the Sinai Peninsula (Bar-Yosef 1998). At that time, wild emmer was a natural constituent of this corridor, but was more widespread in its central-southern part than in its northern part (if it was there at all).
Currently, wild emmer is a natural constituent of several open oak-forest belts and herbaceous plant formations in southwest Asia. Its distribution area is in the Fertile Crescent—a hilly and mountainous region extending from the foothills of the Zagros Mountains in southwestern Iran, through the Tigris and Euphrates basins in northern Iraq and southeastern Turkey, continuing southwestward over Syria and Lebanon to the Mediterranean, and extending to Israel and Jordan (Aaronsohn 1910; Harlan and Zohary 1966; Dagan and Zohary 1970; Tanaka and Ishii 1973; Johnson 1975). The current distribution area of wild emmer wheat is discontinuous (Zohary and Hopf 2000; Zohary et al. 2012). The “southwestern” (Israel, Jordan, southwestern Syria, and southeastern Lebanon) populations of wild emmer are geographically semi-isolated from the “northeastern” (northern Syria, southeastern Turkey, northern Iraq, and western Iran) populations. There are presumably only sporadic connections (if any) in central-western Syria between populations of the southern and northern wild emmer (Kimber and Feldman 1987; Valkoun et al. 1998; Nevo 2001).
Wild emmer is an east-Mediterranean element extending into marginal sub-Mediterranean regions. It grows in a wide range of ecological conditions, from 200 m below sea level (the Jordan Valley) to 1600 m above sea level (Mt. Hermon). It occurs as a common annual component in the herbaceous cover of the deciduous open oak park-forest belt, as well as in evergreen dwarf shrub formations, in steppe-like herbaceous plant formations, in pastures, abandoned fields, and on the edges of cultivation (Kimber and Feldman 1987; Feldman 2001; Nevo 2001; Zohary et al. 2012). It is a calciferous plant and does not grow on calcareous soils, but thrives well on soils that are formed on hard limestone bedrock (terra rossa soil), on basalt bedrock (basaltic soils), and on soil formed on Nubian sandstone. In rocky places that have not been severely overgrazed, dicoccoides wheat often grows in large stands; with wild barley Hordeum spontaneum and wild oat Avena sterilis, they form ‘fields of wild cereals’ (Zohary et al. 2012).
In Israel, wild emmer grows on Mt. Hermon, in the Golan Heights, the Jordan Valley, eastern Upper and Lower Galilee, Gilboa Mts., Mt. Carmel, the eastern and western slopes of Samaria and Judean Mountains, and southwards up to the Yattir region, in southern Judea. In Jordan, it grows in the Gilead highlands (Irbid Plateau), and southwards, to Moab and Edom Mountains. In Southern Syria, wild emmer grows on the northeastern slopes of Mt. Hermon, extending eastwards the region of Hauran, Daraa, and the Druze Mt. In southeastern Lebanon, it grows on the northwestern slopes of Mt. Hermon and in the southern part of the Beqaa Valley. It is quite common and locally abundant in the catchment area of the upper Jordan Valley, in some sites in northern Jordan and southwestern Syria, where it occupies a variety of primary and secondary habitats. Wild emmer is less frequent in Turkey, Iraq and Iran (Harlan and Zohary 1966; Rawal and Harlan 1975; Johnson 1975; Valkoun et al. 1998). Its distribution in the Euphrates basin is limited because most of the soils there are calcareous (Willcox 2005). In most of its distribution area, it grows in patches, in mixed stands with wild barley, oat, and several legumes; in the northeastern region of the Fertile Crescent, it also grows in mixed stands with a second wild, tetraploid wheat, T. timopheevii ssp. armeniacum, with wild diploid wheat, T. monococcum ssp. aegilopoides and with its putative diploid parent, T. urartu. In this region, it also grows sympatrically with the diploids Ae. speltoides, Ae. caudata, and Ae. umbellulata, and the allotetraploids Ae. geniculata, Ae. biuncialis, Ae. triuncialis, and Ae. peregrina. It has an allopatric distribution with Ae. neglecta, Ae. columnaris and Ae. cylindrica. In the southwestern range of its distribution, wild emmer grows sympatrically with the diploid Ae. searsii, and allotetraploids Ae. geniculata, Ae. biuncialis, Ae. triuncialis and Ae. peregrina.
10.3.2.2.3 Diversity
Upon discovery of wild wheat in nature, Aaronsohn (1909, 1910) pointed out that this taxon exhibits wide variation in spike size, glume size, apical tooth, hairiness, and had different spike colors (i.e., white, red and black). Indeed, in its native habitats, this wild wheat exhibits great morphological diversity in spike and spikelet size, shape, color, hairiness, glume shape and size, color and hairiness, awn shape and size, keel and secondary teeth size and prominence, grain color and size, plant height, leaf sheath pigmentation and hairiness, leaf shape and width, and growth habit (Kimber and Feldman 1987). Phenological differences occur in heading time (Percival 1921; Anikster et al. 1991). The larger size of the ear and the spikelet, the form and size of the grain, and the character of the pubescence of the leaves distinguish it from wild diploid wheat, T. monococcum ssp. aegilopoides, while the exceptionally easy disarticulation of the spike, length and form of the spikelets, the striking abundance of hair on the rachis, and the shape and size of the grain, distinguish it from domesticated emmer (ssp. dicoccon), to which it has the closest affinity (Percival 1921).
Detailed genetic studies of populations of wild emmer indicated that this subspecies of T. turgidum is highly polymorphic (Rawal 1971; Nevo et al. 1982, 1984, 1986; Levy et al. 1988; Nevo and Beiles 1989; Anikster et al. 1991; Felsenburg et al. 1991; Huang et al, 1999; Ozbek et al. 2007a). Electrophoretic studies of nonspecific esterases in germinating seeds of accessions of wild emmer revealed genetic polymorphism, with accessions from Turkey showing heterogeneous isoenzyme patterns (Rawal 1971). Similarly, Nevo et al. (1984, 1986, 1982) studying 457 wild emmer samples, taken from 12 populations across its eco-geographical range in Israel, observed a large allozyme variation both among and within populations. Later, Nevo and Beiles (1989) extended their investigation and studied isosymes encoded by 42 gene loci in 1815 plants representing 37 populations, 33 of which were from Israel and 4 from Turkey. Their results showed that wild emmer is highly polymorphic [15 loci (36%) were locally polymorphic, and 21 loci (50%) were regionally polymorphic], with a mean 1.252 alleles per locus (range: 1.050–1.634); the proportion of polymorphic loci per population averaged 0.220 (range: 0.050–0.415), and genic diversity averaged 0.059 (range: 0.002–0.119). Altogether, there were 119 alleles at the 42 putative loci tested—114 in Israel, and only five in Turkey. Genetic differentiation was primarily regional and local, and not clinal; 70% of the variant alleles were common and rather localized or sporadic, displaying an “archipelago” population genetics and ecology structure (Nevo and Beiles 1989). The coefficients of genetic distance between populations were high and averaged D = 0.134 (0.018–0.297), an indication of sharp genetic differentiation over short distances. Discriminant analyses differentiated Israeli from Turkish populations, and within Israel, between central and three marginal regions, as well as between different soil-type populations. Allozyme diversity, overall and at single loci, was significantly correlated with, and partly predictable by, climatic and edaphic factors. The results of Nevo and Beiles (1989) suggest that during the evolutionary history of wild emmer, diversification of natural selection through climatic and edaphic factors was a major agent of genetic structure and differentiation at both the single and multi-locus levels. In addition, they indicate that wild emmer harbors large amounts of genetic diversity exploitable as genetic markers in sampling as well as abundant genetic resources utilizable for wheat improvement.
Polymorphism of the high molecular weight (HMW) glutenin subunits was studied in 456 accessions of wild emmer wheat, originating from 21 different Israeli populations (Levy and Feldman 1988; Levy et al. 1988). A total of 50 different SDS-PAGE migration patterns were observed, resulting from the combinations of 15 subunit patterns of the A subgenome and 24 subunit patterns of the B subgenome. Migration patterns consisted of between 3 and 6 subunits, with most containing five. The migration patterns of the A subgenome had 0–3 subunits, with most containing two. The migration patterns of the B subgenome had 1–3 subunits, with three being most common. The polymorphism of the HMW glutenin genes found in wild emmer wheat is much higher than that of domesticated wheats. Marginal populations tended to be more uniform than those at the center of distribution. The various HMW glutenin alleles tended to be clustered, both at a regional level and within a single population. Significant correlations were found between the molecular weight of subunits encoded by Glu-A1-1 and population altitude, average temperature and rainfall.
Felsenburg et al. (1991) studied variation in the electrophoretic mobility pattern of the HMW glutenin subunits by different genotypes of the Ammiad wild emmer population studied during a five year period (1984–1988). One-dimensional SDS-PAGE of seed extracts showed that the population was highly polymorphic. The spatial distribution of these genotypes was nonrandom, with each of the 11 habitats characterized by different genotype frequencies. Yearly changes in genotypes had little effect on the total frequencies of the various genotypes. A high affinity was found between specific HMW glutenin genotypes and certain habitats.
Ozbek et al. (2007a) estimated the spatio-temporal genetic variation in populations of wild emmer wheat and assessed the contribution of spatial versus temporal factors to the maintenance of genetic variation in a population. Single spikes were collected in the years 1988 and 2002, from plants that grew in the same sampling points, from six different habitats in the Ammiad conservation site, Eastern Galilee, Israel. DNA was extracted from each plant and analyzed by the AFLP method. Fourteen primer combinations yielded 1545 bands, of which 50.0% and 48.8% were polymorphic in the years 1988 and 2002, respectively. Genetic diversity was much larger within populations than between populations and the temporal genetic diversity was considerably smaller than the spatial genetic diversity. Nevertheless, population genetic structure may vary to some degree in different years, mainly due to fluctuations in population size because of yearly rainfall variations. This may lead to predominance of different genotypes in different years. Clustering the plants by their genetic distances grouped them according to their habitats and demonstrated the existence of genotype-environment affinities.
The characterization of the Ammiad population has continued, starting in 1984 until 2020, sampling plants at the same location during all the years of collection (Dahan-Meir et al. 2022). During these 36 years, temperatures have raised by almost 2 °C and CO2 concentration increased from 340 to 410 ppm. Dense genotyping of 832 individuals along the transect of collections, provided thousands of genetic markers mapped along the reference genome sequenced by Avni et al. (2017). The study by Dahan-Meir et al. (2022) showed that the population was highly variable and that genotypes tended to be clustered to the same ecological microhabitats over the 36 years of collection. Simulations, using realistic demographic parameters of gene flow through outcrossing and seed mobility, and population density, indicate that it is unlikely that neutral processes alone can explain the observed spatial and temporal stability of the population. These results suggested that natural selection together with limited gene flow, explain the remarkable stability of the population. The resilience of this wild emmer wheat population emphasizes the potential importance of such gene pool for the breeding of domesticated wheat in the face of a changing climate. It also shows the importance of in situ conservation over long periods. In fact, the Ammiad population has been declared as a natural reserve for wild-wheat conservation by the Israel nature and parks authority in 2006, which protects it from extinction due to overgrazing or other anthropogenic activities.
RFLP diversity in the nuclear genome was estimated within and among wild emmer wheat populations from several Israeli locations (Huang et al. 1999). Use of 55 enzyme-probe combinations showed high levels of genetic diversity. Population genetic structure in this wild taxon appears to have been influenced by historical founder events as well as selective factors. Multivariate analyses indicated that individuals tend to cluster together according to their population of origin, and that there is little geographical differentiation among populations.
Avivi (1979), Avivi et al. (1983) analyzed 47 different accessions of wild emmer, representing almost the entire eco-geographical range in Israel, for their grain protein percentage (GPP). The GPP range from 17.0 to 27.3%, indicating wide variation between genotypes. The observed GPP was much higher than that of all the domesticated subspecies of T. turgidum. Within a given genotype, the small grains of the first florets exhibited almost the same amount of protein as the large grains of the second florets. Comparison between different genotypes revealed a positive correlation between protein content and grain size.
To study the effect of various habitats on GPP in wild emmer, the trait was determined in 910 accessions collected from 22 different populations representing different eco-geographical conditions in Israel (Levy and Feldman 1988). High values of GPP were found, with population means ranging from 19.7 to 28.0%, and single accession means ranging from 14.1 to 35.1%. Marginal geographical populations usually had a lower GPP and smaller intra-population variations than central ones. Repeated sampling of several central populations for four consecutive years revealed relatively large intra-population GPP fluctuations. No correlation was found between GPP and ecological factors, except for soil type; accessions growing on terra-rossa soil had higher GPP than those growing on basaltic soil. Accessions with black glumes, glabrous auricles, or large grains exhibited high GPP values. Their association with morphological and biochemical markers enabled mapping of genes for high GPP to six chromosomes, namely, 1AS, 1BS, 5A, 5B, 7A and 7B (Levy et al. 1988).
In sharp contrast to the above data on diversity in wild emmer, Haudry et al. (2007) concluded from the mean nucleotide diversity in wild emmer that this subspecies of T. turgidum is not a highly polymorphic taxon. They suggested several possible reasons for this low diversity. First, wild emmer arose through a relatively recent allopolyploidy event (0.7–0.9 MYA; Gornicki et al. 2014; Marcussen et al. 2014; Middleton et al. 2014), that may have resulted in a large decrease in diversity in the new allopolyploid species with respect to its diploid ancestors, and since nucleotide mutation rate is low (Lande and Barrowclough 1987), the time from its formation has not been sufficiently long to restore diversity. Second, the small effective population size of the current population of wild emmer may account for the low level of nucleotide diversity.
10.3.2.2.4 Cytological Variation
Several studies demonstrated the wide occurrence of reciprocal translocations among accessions of wild emmer (Rao and Smith 1968; Dagan and Zohary 1970; Tanaka and Ishii 1973; Rawal and Harlan 1975; Kawahara and Tanaka 1978, 1981, 1983; Kawahara 1984, 1986, 1987; Joppa et al. 1995). Rao and Smith (1968), Rawal and Harlan (1975) reported the presence of one or two reciprocal translocations in hybrids between Turkish accessions as well as between Turkish and Israeli accessions of wild emmer. Cytological analysis of meiosis in the F1 hybrids of two accessions from Iran crossed with Israeli wild emmer showed that the wild Iranian wheats were fully inter-fertile with the Israeli dicoccoides line (Dagan and Zohary 1970). Chromosome pairing was normal and the presence of two reciprocal translocations was observed, between the two Iranian accessions and between one of the Iranian accessionד and the Israeli accession.
Mixed stands of wild emmer and wild timopheevii wheats were found in several sites in southeastern Turkey, northern Iraq and western Iran (Tanaka and Ishii 1973). Morphological differences between plants of wild emmer and those of wild timopheevii were not clear, except that the leaf surface of the former was exclusively glabrous, while that of wild timopheevii was pubescent (Tanaka and Ishii 1973). The F1 hybrids between several accessions of wild emmer and a tester line of wild emmer, exhibited one or two reciprocal translocations, indicating that chromosomal structural differences between accessions is quite common in this wild subspecies of T. turgidum.
A relatively large number of genomes which differ from each other by one or two reciprocal translocations, were identified in wild emmer through hybridization experiments (Kawahara and Tanaka 1978, 1981, 1983; Kawahara 1984, 1986, 1987). Variation in chromosome structure was the highest in Turkey, followed by Israel, whereas wild emmer from Iraq and Iran showed little variation. Consequently, Kawahara (1987) concluded that the center of diversity in chromosome structure is in southeastern Turkey. Nishikawa et al. (1994), using telocentric lines of domesticated emmer wheat, identified the chromosomes involved in seven translocation kinds in wild emmer. Likewise, Joppa et al. (1995), analyzing Israeli accessions of wild emmer, determined 119 genotypes of wild emmer with translocations (as compared to the ordinary chromosome arrangement typified by that in the standard laboratory common wheat cultivar Chinese Spring) in an investigated sample of 171 genotypes (70%). The frequency of translocations in different Israeli populations observed by Joppa et al. (1995) varied from 0.27 to 1.00, and all populations had 1 or more genotypes with one or more translocations. A sample of 17 genotypes from 12 populations were crossed with the Langdon D-genome disomic substitutions to determine the identity of the chromosomes involved in the translocations. There were nine genotypes with translocations and with the exception of a 2A/2B translocation, none of them involved the same homoeologous chromosomes (Joppa et al. 1995). The B-subgenome chromosomes were involved in translocations more frequently than the A-subgenome chromosomes. Translocation frequencies of the various populations were correlated with environmental variables, primarily with water availability and humidity, and possibly also with soil type. In general, translocation frequency was higher in peripheral populations in the ecologically heterogeneous frontiers of wild emmer distribution than in the central populations located in the catchment area of the upper Jordan valley.
To identify accessions of tetraploid wheat in mixed populations of ssp. dicoccoides and wild T. timopheevii, ssp. armeniacum, collected by Jack R. Harlan in Turkey, Rao and Smith (1968) crossed six of the accessions with four Israeli accessions of ssp. dicoccoides and then morphologically and cytogenetically analyzed the F1 hybrids. Both, the accessions of ssp. dicoccoides and ssp. armeniacum were also crossed with a number of domesticated tetraploid wheats, including T. timopheevii ssp. timopheevii, T. turgidum ssp. turgidum, and ssp. dicoccon. Cytogenetically, the four Israeli accessions of wild emmer were similar and exhibited very close relationships with ssp. dicoccon and ssp. turgidum, but their hybrids with ssp. timopheevii showed poor chromosome pairing and were fully sterile. Four of the six Turkish accessions were similar to the Israeli group in pairing relationships and seed set percentages (Rao and Smith 1968). The remaining two Turkish accessions showed considerable cytogenetic differentiation. Turkish accession 11,189 showed a close pairing relationship and some fertility with ssp. timopheevii and exhibited poor pairing and complete sterility in crosses with ssp. dicoccon and the Israeli ssp. dicoccoides group. Surprisingly, Turkish accession 11,191 exhibited almost complete chromosome pairing and some fertility in crosses with both ssp. timopheevii and ssp. dicoccon (Rao and Smith 1968).
Rawal and Harlan (1975) studied chromosome pairing in meiosis of F1 hybrids involving three Israeli accessions of ssp. dicoccoides, six Turkish accessions of tetraploid wheat, and one line of domesticated T. timopheevii. Like Rao and Smith (1968), they found that four of the six Turkish accessions were cytologically similar to the Israeli dicoccoides accessions, and one Turkish accession (# 189) was cytologically similar to T. timopheevii, whereas the other Turkish accession (# 191) showed good chromosome pairing with both all three accessions of ssp. dicoccoides and ssp. timopheevii. Interestingly, the four Turkish accessions that were identified as ssp. dicoccoides had somewhat better chromosomal pairing with T. timopheevii (average number of chromosome association/cell was 22.0–22.8) than did the Israeli accessions (average number of chromosome association/cell was 18.8–21.5).
Studies of chromosomal pairing in F1 hybrids of accessions of either the northern race (the Turkish race) or the southern race (the Israeli race) of wild emmer and wild T. timopheevii showed somewhat better pairing between the northern race and T. timopheevii than between the southern one and T. timopheevii (Rao and Smith 1968; Rawal and Harlan 1975; Tanaka and Kawahara 1976; Tanaka et al. 1978). Actually, the four Turkish accessions with ssp. dicoccoides-like behavior had chromosomes that paired slightly better with ssp. timopheevii as compared to the accessions from Israel (Rawal and Harlan 1975); the differences were small but seemed to be consistent. It is possible that with more collections, forms with a truly intermediate behavior might be found. This indicates that the northern race of wild emmer introgressed with T. timopheevii. According to the hypothesis set forth by Zohary and Feldman (1962), wild emmer and wild T. timopheevii, which share the A subgenome, could have acquired adaptive traits through introgressive hybridization, leading to recombination of their B and G subgenomes. Cytologically intermediate types predicted by this hypothesis were indeed discovered by Sachs (1953), Wagenaar (1961a, 1966), Rao and Smith (1968), Rawal and Harlan (1975), Tanaka and Kawahara (1976), Tanaka et al. (1978). In accord with this, Gornicki et al. (2014) provided molecular evidence that evolution of these two allotetraploid wheats was also accompanied by chloroplast introgression. One accession of T. turgidum ssp. dicoccoides (G4991), for example, which showed high chromosome pairing with both T. turgidum and T. timopheevii (Rawal and Harlan 1975), carries the T. timopheevii chloroplast haplotype (H09) as a result of a cross between wild emmer and wild timopheevii. Conversely, wild T. timopheevii accession TA976 carries the emmer-lineage chloroplast haplotype (H04) (Gornicki et al. 2014).
The pairing homoeologous (Ph1) gene of common wheat has long been considered the main factor responsible for the diploid-like meiotic behavior of polyploid wheat (Riley 1960; Sears 1977). This dominant gene, located on the long arm of chromosome 5B (5BL), suppresses pairing of homoeologous chromosomes in allopolyploid wheat and in their hybrids with related species. Ozkan and Feldman (2001) reported on the existence of genotypic variation among wild emmer wheat in the control of homoeologous pairing, most probably in the Ph1 locus. Compared with the level of homoeologous pairing in hybrids between Aegilops peregrina and the bread wheat cultivar Chinese Spring (CS), significantly higher levels of homoeologous pairing were obtained in hybrids between Ae. peregrina and CS substitution lines in which chromosome 5B of CS was replaced by 5B of several lines of wild emmer. Searching for variation in the control of homoeologous pairing among lines of wild emmer showed that hybrids between Aegilops peregrina and different lines of this wild wheat exhibited three different levels of homoeologous pairing: low, low-intermediate, and intermediate-high. The genotypes with low-intermediate and intermediate-high pairing may possess weak alleles of Ph1. The three different ssp. dicoccoides pairing genotypes were collected from different geographical regions in Israel, indicating that this trait may have an adaptive role (Ozkan and Feldman 2001).
10.3.2.2.5 Intra-Subspecific Differentiation
Wild emmer contains two main races that are morphologically, ecologically, and genetically distinct (Harlan and Zohary 1966; Nishikawa et al. 1994; Joppa et al. 1995; Kawahara and Nevo 1996; Ozkan et al. 2002, 2005; Mori et al. 2003; Luo et al. 2007). The southern race grows in Israel, Jordan, southwest Syria and southeast Lebanon, whereas the norther race grows in southeastern Turkey, northern Iraq and western Iran. The two races are geographically separated by a conspicuous discontinuity in central Syria (Kimber and Feldman 1987; Zohary et al. 2012). In general, the plants of the northern race are characterized by relatively compact heads, fine-textured awns, often hairy spikelets, with sparse pubescence on the rachis and spikelet base. In contrast, the southern race is large and robust, with spikelets featuring coarse awns, dense pubescence on the rachis internode edge and spikelet base, large seeds, wide leaves and thick stems (Harlan and Zohary 1966; Rawal and Harlan 1975). Robust early-maturing types occupy the winter-warm basin around the Sea of Galilee, to altitudes as low as 100 m below sea level, whereas more-slender, late-blooming forms occur higher up in the Galilee mountains, reaching elevations of 1600 m on the east- and south-facing slopes of Mt. Hermon (Zohary et al. 2012). The southern race may occur in massive stands over considerable areas on basaltic and hard limestone slopes of the oak woodland belt of the region. But it was not until the current state of Israel was established and grazing became regulated, that the abundance of these stands was recognized. Where grazing is controlled, non-arable sites support stands as dense as cultivated wheat fields (Harlan and Zohary 1966). In contrast, the northern race is never really abundant and occurs in sporadic, isolated patches and thin, scattered stands in the lower oak-woodland belt, often in association with wild diploid wheat and wild barley (Harlan and Zohary 1966). It is never the dominant species of the grassland flora and is usually found only as a minor component among other cereals. Since it is not a weedy plant, the range and abundance of the northern race may well have become restricted, since the land was disturbed by agriculture (Harlan and Zohary 1966).
Large-grain forms of wild emmer were first noted by Cook (1913) in northeastern Israel (then Palestine). In 1926, Vavilov found in Israel (then Palestine) wild emmer with large spikes and large grains that resemble domesticated T. turgidum, mainly ssp. durum, that was grown in Israel for, at least, 2300 years. Consequently, Vavilov subdivided wild emmer into two major groups: a narrow-spike form and a wide-spike one (Vavilov et al. 1931). Jakubziner (1932) maintained Vavilov’s division of wild emmer, but named the narrow-spike form grex horanum Vav., since it was collected in Hauran, Syria, and the wide-spike form grex judaicum Vav., since it was collected in Israel (then Palestine). He reported that judaicum in several regions in Israel, namely, the Upper Jordan Valley, Mt. Gilboa, and Mt. Hermon, in Syria, Jordan and even in the Cilician Taurus, Turkey, always occurs close to cultivated wheat fields. He also described some wild emmer and ssp. durum hybrids that had been collected in the Upper Jordan Valley. These observations suggest introgression.
Jakubziner’s subdivision of wild emmer was supported by morphological studies of Israeli accessions (Poyarkova 1988), which, following Jakubziner, classified the slender type as horanum and the robust type as judaicum. Poyarkova et al. (1991) drew attention to the morphological, phenological, and geographical differences between the narrow-spiked and the wide-spiked types of Israeli wild emmer accessions. A tendency for increased grain number to three in a spikelet was observed in the both variants, but was more strongly expressed in the wide-spiked accession (Poyarkova et al. 1991). The narrow-spiked form, horanum, is widely distributed in Israel, whereas the wide-spiked form, judaicum, is restricted to the vicinity of the Sea of Galilee and to Mt. Gilboa (Poyarkova et al. 1991). Intermediate morphological forms are abundant in natural habitats where the two variants are sympatric (Poyarkova et al. 1991). Therefore, it was concluded by Anikster et al. (1988) that the two forms of wild emmer are extremes of a continuum.
Genetic variation in several Israeli (the southern race) and Turkish (the northern race) populations of wild emmer was assessed by RFLP analysis (Ozbek et al. 2007b). Frequencies of polymorphic loci and gene diversity were significantly higher in the southern than in the northern populations. The southern populations contained more unique alleles than northern populations. Genetic distance was larger between Israeli and Turkish populations than between populations within each country, indicating that the Israeli and Turkish populations are considerably diverged. Similarly, AFLP analysis showed that the southern race is clearly separated from the northern one (Ozkan et al. 2002, 2005). However, genetic studies (Tanaka and Sakamoto 1979; Saito and Ishida 1979; Nakai 1978a, b; Nishikawa et al. 1979) revealed that the northern race of wild emmer also showed wide variation and that it is differentiated into several populations (Luo et al. 2007). Luo et al. (2007), who performed RFLP analysis at 131 loci of accessions of wild emmer, showed that this taxon consists of a southern population (in Israel, Jordan, southwestern Syria, and southeastern Lebanon) and northern population (southeastern Turkey, northern Iraq, and western Iran), each which can be further subdivided. The southern race consists of two distinct groups, the robust judaicum group located north and northwest of the Sea of Galilee, and the slender group, grown in other Israeli regions (Luo et al. 2007).
Luo et al. (2007) found that gene flow between wild and domesticated tetraploid wheat occurred across the entire area of wild emmer distribution, but failed to show that the judaicum group originated from hybridization between wild emmer and ssp. durum. Feldman and Millet (Feldman M, Millet E, unpublished data) found robust plants of wild emmer on the edges of wheat fields in several northwestern sites of the Sea of Galilee and assumed that they resulted from introgression with domesticated wheats, either tetraploid ssp. durum or hexaploid T. aestivum ssp. aestivum. Similarly, Blumler (1998) studying the judaicum type in the upper Jordan Valley, concluded that it originated relatively recently through hybridization of wild emmer with durum wheat. The occurrence of spontaneous hybrids between wild emmer and ssp. dicoccon, durum or common wheat, was already reported by Cook (1913), Percival (1921), Jakubziner (1932a), Zohary and Brick (1962). Indeed, in a number of wild emmer accessions sown in experimental fields in southern Russia, natural crossing with ssp. durum were frequently observed (Jakubziner 1932a). These spontaneous hybridizations indicate that hybridization between wild emmer and domesticated wheats are not an isolated phenomenon. Such hybridization is doubtlessly due to the numerous intermediate and extraordinarily diverse morphological forms found in its native habitats (Percival 1921). Percival (1921) held the opinion that most of the “large-seeded” forms are of hybrid origin, and contain a trace of ssp. durum. Some of these forms are likely hybrids of ssp. dicoccoides with the domesticated wheats T. turgidum ssp. durum and T. aestivum ssp. aestivum, and with the wild T. monococcum ssp. aegilopoides, which is often found growing sympatrically with wild emmer (Percival 1921).
While typical wild emmer (horanum) is not at all similar to durum wheat, plants from the Israeli upper Jordan Valley occasionally contain several traits of durum wheat (Blumler 1994, 1998) such as plant robustness, grain shape and size, glume shape, first glume tooth, glume pubescence, spikelet width and glutenin A1-1 allele, and early maturing. In general, wild emmer from the upper Jordan valley is highly variable, containing intermediates between durum wheat and horanum wild emmer, as one would expect of products of hybridization (Blumler 1994). Indeed, electrophoretic studies of Nevo et al. (1982), Nishikawa et al. (1994) showed that the wild emmer populations in the upper Jordan Valley are genetically differentiated from all other investigated Israeli populations. As one travels west or east from this site, this race of emmer is replaced by populations of typical wild emmer (Golenberg 1988; Blumler 1994). Domesticated individuals should have had opportunities to come in contact with wild plants especially along rocky, untillable field margins and hybridize with them.
Likewise, the glutenin data of Levy and Feldman (1988) are particularly informative. Glutenin A1-1 is present in domesticated emmer, ssp. dicoccon, but absent in ssp. durum. It is almost always present in wild emmer, but is generally absent in accessions from the upper Jordan Valley, which suggests potentially massive introgression from ssp. durum. Of the 19 wild populations that Levy and Feldman (1988) examined, glutenin A1-1 was present in all but two: a population just south of the upper Jordan Valley, and in Majdal-es-Shams on Mt. Hermon. Jakubziner (1932a) reported on judaicum from Majdal es–Shams. Both populations are in agricultural areas. Interestingly, the glutenin A1-2 locus presented a different pattern, as it is absent in most wild emmer populations, in domesticated emmer and ssp. durum, but present in bread wheat and in some wild emmer plants from the upper Jordan Valley.
10.3.2.2.6 Time and Place of Origin of Wild Emmer
The time of origin of wild emmer was estimated in several studies (Table 10.7; see also Chap. 12). Dvorak and Akhunov (2005), using locus duplications as a clock for estimation of the age of this allotetraploid, suggested that it was formed about 0.360 million years ago (MYA), while Huang et al. (2002), analyzing Acc-1 (plastid acetyl-CoA carboxylase) and Pgk-1 (plastid 3-phosphoglycerate kinase) genes, found that the A subgenome of wild emmer diverged from the genome of T. urartu less than half a MYA, indicating an origin 0.500 MYA. On the other hand, studies of nucleotide sequences of hundreds of nuclear genes showed that wild emmer formed about 0.800 MYA (Marcussen et al. 2014). Gornicki et al. (2014), Middleton et al. (2014), based on sequencing of the entire genomic chloroplast DNA, found that the cytoplasm of the emmer lineage diverged from that of Ae. speltoides 0.700–0.900 MYA, respectively, meaning that the allotetraploidization event that formed wild emmer occurred within the last 0.700–0.900 MYA. This date is slightly above earlier estimates of Huang et al. (2002), Dvorak and Akhunov (2005).
Wild emmer presumably originated in the southwestern part of the Fertile Crescent, i.e., in the vicinity of Mt. Hermon and the catchment area of the Jordan River. This is inferred from the wider morphological, phenological, biochemical, and molecular variation of wild emmer in Israel, Jordan, southern Syria, and southern Lebanon, as opposed to its more limited variation in southeastern Turkey, northern Iraq, and southwestern Iran (Nevo and Beiles 1989; Ozbek et al. 2007b). AFLP analyses showed that the pattern of T. urartu from Mt. Hermon is the closest to that of the A subgenome of wild emmer, suggesting that this allotetraploid formed in the vicinity of Mt. Hermon (Dvorak and Luo 2007). In accordance, the geographic distribution of chloroplast haplotypes of wild emmer and of Ae. speltoides (the assumed cytoplasm donor to allotetraploid wheat) illustrates the possible geographic origin of the emmer lineage in the southern Levant (Gornicki et al. 2014).
From this region, wild emmer spread southward and northward. Wild emmer could presumably have spread into the northern and northeastern parts of the Fertile Crescent during the last part of the Pleistocene (10,000–400,000 years ago), which was characterized by climatic fluctuations that might have facilitated its northward spread. Alternatively, wild emmer may have moved northward much later, in the beginning of the Holocene (somewhat around 10,000 years ago), with the expansion of the cultivation of wild emmer from the Jordan Rift Valley to southeastern Turkey, in the Pre-Pottery Neolithic A (PPNA) 10,300–9500 years ago. Its escape from cultivation in the northern region of the Fertile Crescent could have laid the foundation for “feral” populations there. In addition, the morphological resemblance of wild emmer from the north-eastern region of the Fertile Crescent to wild T. timopheevii and the somewhat better chromosomal pairing in hybrids between wild emmer and wild T. timopheevii (see above) also suggests that introgressive hybridization from the local wild tetraploid wheat, T. timopheevii ssp. armeniacum, might have helped in the establishment of wild emmer in the northeastern region of the Fertile Crescent. The lack of archaeological remains of wild emmer in southeastern Turkey prior to 9500 BP (all dates are uncalibrated) (Nesbitt 2002) supports this second possibility.
This idea is shared by Civáň et al. (2013), who used super-networks with datasets of nuclear gene sequences and novel markers detecting retrotransposon insertions in ribosomal DNA loci, to reassess the evolutionary relationships among tetraploid wheats. The observed diversity and reticulation patterns indicate that wild emmer evolved in the southern Levant, and that the wild emmer populations in south-eastern Turkey and the Zagros Mountains are relatively recent reticulate descendants of a subset of the wild southern Levantine populations.
10.3.2.2.7 Economically Important Genes in Wild Emmer
Already Aaronsohn (1910), who discovered in 1906 wild emmer in nature, was impressed by the adaptation of this taxon to a wide range of climatic and edaphic conditions, by its large grain size, its high resistance to rust, and its ability to grow in relatively dry habitats. Consequently, he recommended to transfer its desirable traits to domesticated wheats, particularly, to improve their resistance to biotic stresses, and tolerance to extreme climatic and soil conditions. Aaronsohn believed that “the cultivation of wheat might be revolutionized by the utilization of wild wheat. Such utilization might facilitate the formation of many new varieties, some of which will be hardy and able to grow in dry and warm habitats or in areas with poor soil and can thus expand the wheat growing area” (Aaronsohn, 1910, p. 52).
Aaronsohn’s belief that wild emmer can be utilized in the improvement of domesticated wheats was shared by Schweinfurth (1908), von Tschermak (1914), Percival (1921), Vavilov (1932), and others. The fertile F1 hybrids between ssp. durum and wild emmer, produced by von Tschermak (1914), showed that gene transfer from wild into domesticated forms is possible. Consequently, selected specimens of subsp. dicoccoides were introduced to various research stations in Europe and the United States for observation and crosses with domesticated wheats. Yet, these early attempts to utilize wild emmer in breeding programs were met with very little success, and Aaronsohn’s vision of using this wild gene resource for the improvement of domesticated wheats was soon neglected. This mainly resulted from lack of genetic and cytogenetic knowledge of the wheats, coupled with a poor understanding of relationships between wild and domesticated wheats. Moreover, wheat breeders were discouraged from utilizing wild wheat in breeding programs because of difficulties to select against undesirable characters derived from wild emmer.
This situation has changed radically in the second half of the twentieth century, leading to a renewed interest in the germplasm of wild emmer as a source of agronomically important traits. The renewed interest in the germ plasm of wild wheat has been stimulated by the large genetic erosion that occurred in domesticated wheat, mainly to common wheat, because of the replacement in parts of the world of a huge number of land races by high-yielding varieties without preserving the land races, resulting in a drastic narrowing of the genetic basis of common wheat. During this period, much information has been accumulated on the genetic relationships between wild emmer and domesticated wheats. The availability of aneuploidy lines of T. aestivum (Sears 1954) and substitution lines in which wild emmer chromosomes or chromosome arms are substituted for their durum wheat homologues (Joppa 1993) or bread wheat homologous arms (Millet et al. 2013, 2014), enabled the genetic analysis of individual wild emmer chromosomes or chromosome arms on the genetic background of domesticated wheat, and thus, facilitated the transfer of selected wild chromosomal segments to domesticated wheat. In particular, the recent sequencing of the wild emmer genome (Avni et al. 2017) opens the possibility of identifying and utilizing beneficial wild genes.
Wild emmer contains an invaluable rich gene resource for wheat improvement that, at present, has been hardly exploited (Feldman and Millet 1995; Feldman et al. 1994, 1996). The gene pool of wild emmer, which is larger and richer than that of the domesticated wheats, contains many agronomically-important genes (for review see Feldman and Millet 1995; Huang et al. 2016). This taxon is genetically very close to durum and common wheat and the F1 hybrids between them are fertile. Since the chromosomes of wild emmer are homologous to those of durum wheat and to those of the A and B subgenomes of common wheat, it is possible to transfer desirable traits from wild emmer into domesticated wheat by simple, conventional plant breeding procedures.
The screening of wild emmer for economically valuable characteristics is only in its initial stages. Recent surveys of samples of wild emmer collected throughout its distribution area have shown that this wild wheat contains many agronomically important genes, such as those conferring resistance to pests and diseases (e.g., Anikster et al. 2005), greater tolerance to drought and heat (Peleg et al. 2005, 2009), higher grain protein content and quality (Avivi 1979; Avivi et al. 1983), higher zinc and iron in the grains (Cakmac et al. 2004), and larger grains (Cook 1913). Moreover, this wild gene pool contains many alleles that do not exist in the domesticated gene pool such as those coding for different subunits of storage proteins (glutenin and gliadins) (Levy and Feldman 1987). Despite its breeding potential, this gene pool has been utilized relatively minimally in wheat improvement (Gerechter-Amitai and Grama 1974; Grama and Gerechter-Amitai 1974; Feldman 1977; Feldman and Sears 1981; Levy and Feldman 1987; Feldman et al. 1994; Feldman and Millet 1995). Simply inherited traits have been transferred from wild emmer into domesticated wheats and the value of these traits has been widely documented. Yet, gene transfer of complexly inherited traits, for which the controlling genes may be located on several different chromosomes of wild emmer, is more difficult, and the presence of undesirable wild alleles may musk the effect of the desirable ones.
Wild emmer contains many genes conferring adaptation populations to biotic and abiotic stresses. (Huang et al. 2016). It comprises resistance to fungal and pest diseases, such as resistance to powdery mildew (Moseman et al. 1984; Gerechter-Amitai and van Silfhout 1984; Dinoor et al. 1991; Rong et al. 2000; Yahiaoui et al. 2009; Li et al. 2020), leaf rust (Moseman et al. 1985; Dinoor et al. 1991; The et al. 1993; Anikster et al. 2005), stem rust (Nevo et al. 1991; Dinoor et al. 1991; The et al. 1993; Moseman et al. 1985; Anikster et al. 2005), stripe rust (yellow rust) (Gerechter-Amitai and Stubbs 1970; Gerechter-Amitai and Grama 1974; Gerechter-Amitai, 1980; Reinhold et al. 1983; Valkoun 2001; Klymiuk et al. 2018), Septoria nodorym (Dinoor et al. 1991), tan spot (Faris et al. 2020), and take-all (Dinoor et al. 1991). It has a variety of glutenins and gliadins subunits (Galili and Feldman 1983; Levy and Feldman 1988; Felsenburg et al. 1991), a high percentage of grain protein Avivi et al. 1983; Mansur-Vergara et al. 1984; Nevo et al. 1986; Levy and Feldman 1987, 1989; Millet et al.1992; Peleg et al. 2008; Chatzav et al. 2010), a high concentration of micronutrients such as zinc (Zn), iron (Fe) and manganese (Mn) (Cakmac et al. 2004; Uauy et al. 2006; Distelfeld et al. 2006; Peleg et al. 2008; Chatzav et al. 2010), and tolerance to abiotic stresses, such as drought (Peleg et al. 2005, 2009), heat (Ullah 2016), and salinity (Nevo and Chen 2010). Several accessions of wild emmer have large grains (Avivi, 1979), and the potential to increase grain yield and grain protein yield (Feldman and Millet, 1995; Millet et al. 2013, 2014), and improve photosynthetic efficiency (Nevo et al. 1991). In a T. durum x T. dicoccoides mapping population, Peng et al. (2003a, b) identified quantitative trait loci (QTLs) contributing to early flowering time, higher spike number and weight, higher kernel number and higher yield.
Chromosome 6B of wild emmer wheat was previously reported to be associated with high grain protein content (Joppa and Cantrell 1990), zinc, iron, and manganese (Distelfeld et al. (2006). This chromosome also carries the wild type allele of Gpc‐B1, causing earlier senescence of flag leaves (Uauy et al. 2006). To explain the pleiotropic effect of the Gpc-B1 gene on the high concentration of protein, zinc, iron, and manganese in the grain, Distelfeld et al. (2006) suggested that this locus is involved in more efficient remobilization of nutrients from the leaves to the grains, in addition to its effect on earlier senescence of the green tissues. Yet, Uauy et al. (2006) claimed that the Gpc-B1 gene confers a short duration of grain fill time due to an earlier flag leaf senescence, thus ceasing synthesis of carbohydrates and their translocation to the grains. This results in a relatively smaller amount of grain carbohydrates and consequently, in a higher concentration of grain protein and several micronutrients.
10.3.2.3 Ssp. dicoccon (Schrank) Thell. (Domesticated Emmer)
10.3.2.3.1 Description of the Subspecies
T. turgidum ssp. dicoccon (Schrank) Thell., known as domesticated emmer or two-grained domesticated wheat [Syn.: T. spelta Host; T. spelta (L.) var. dicoccon Schrank; T. dicoccum (Schrank) Schübl.; T. vulgare dicoccum Alef.; T. vulgare ssp. dicoccum Körn.; T. sativum dicoccum Hack.; T. sativum Lam. ssp. dicoccum Ascher.et Graebn.; T. aestivum L. var. dicoccon (Schrank) Fiori; T. farrum Bayle-Barelle; T. amyleum Seringe; T. zea Wagini; T. dicoccum Körn.; Gigachilon polonicum (L.) Seidl ssp. dicoccon (Schrank) Á. Löve] is an annual, predominantly autogamous, 55–125-cm-tall (excluding spikes) plant. Culms are usually erect, and hollow in some varieties, while solid at the upper internode in others. The spike, whose color is white, red, or black, is bilaterally compressed, dense, determinate, two-rowed, 5–10-cm-long (excluding awns), with 15–30 spikelets, and awned. The rachis is short, flat and smooth, more or less hairy along the margins, with a tuft of hair in its base, and usually non-brittle, but breaks into spikelets upon threshing. Spikelets are oval or lanceolate, 10–16-mm-long, solitary at nodes, with the top spikelet being fertile, and at right angles to the plane of the lateral spikelets. There are 3–4 florets, the lower two being fertile, while the upper ones are sterile. The glumes are rigid, oval and boat-shaped, similar in size, shorter than the spikelet, 10–13-mm-long, with a strong keel ending in a straight or curved teeth that varies in length and form in different varieties, and with 7 veins; the strongest vein converges towards the base of the apical tooth, where it ends in a secondary tooth, which, in some specimens, is 5-mm-long, while in others, is very short. Some varieties have pubescent glumes. The lemma is boat shaped, with 9–11 veins, but without a keel, its central vein is prolonged as a strong and long, 5–14-cm–long awn. The awn is flattened, straight, and with a small basal tooth. Awns are always present on the two lemmas of the fertile spikelets and are often of nearly equal in dimensions. The palea is equal to, or slightly longer than the lemma, ovate-lanceolate, with a narrow apex and two ciliate keels. The palea is membranous and splits at the tip at maturity, and has two veins and two keels. There are 2, rarely 3, caryopses in each spikelet, firmly enclosed by the palea and lemma. The color of the grain is white, yellowish, or red, rarely purple. The grains are comparatively narrow and pointed at both ends and more or less laterally compressed. Each grain has a brush of hairs on the apex. Well-developed grains measure 7–9 mm in length, and 2.85–3.4 mm in width (Fig. 10.3a).
A plant and spikes of domesticated subspecies of T. turgidum L.; a Domesticated emmer, ssp. dicoccon (Schrank ex Schübl.) Thell. b ssp. durum (Desf.) Husn. cv. Inbar; c ssp. polonicum (L.) Thell.; d ssp. carthlicum (Nevski) Löve and Löve
Domesticated emmer closely matches wild emmer in almost all its morphological characteristics (Percival 1921). In both taxa, the hairs on the surface of the leaf blades are similar in form, length and arrangement; the spikes are flat, with narrow spikelets containing two grains in each, and the glumes alike in shape and texture. The conspicuous fringe of silky hairs on the margins of the rachis is missing or much reduced in the domesticated emmer and the grains of wild emmer are longer than those of domesticated emmer. The main difference between wild and domesticated emmer is rachis brittleness; in wild emmer, the rachis is brittle, and the spike disarticulates at maturity into individual spikelets, whereas, in domesticated emmer, the rachis is tough (or semi tough) and non-brittle, and the spike remains intact at maturity. Like wild emmer, domesticated emmer is also hulled wheat, i.e., it has rigid glumes that firmly enclose the grains. This requires pounding to release the grains from the glumes. On threshing, a hulled wheat spike breaks up into spikelets.
Being an ancient crop adapted to diverse climatic and edaphic conditions that exist in many parts of the world as well as to different agricultural practices, domesticated emmer is characterized by numerous landraces and varieties. Percival recognized two groups in domesticated emmer: (1) Indo-Abyssinian emmers—all are early forms, with four-to six–nerved coleoptiles, yellowish-green leaves, short straw (55–65-cm-tall), paler yellowish-green culm leaves, which have fewer and shorter hairs on the ridges, frequently rather glabrous auricles, and ears with a brittle or tough rachis; (2) European emmers—later in growth, with two nerved coleoptiles, glaucous leaves, taller straw (100–125-cm-tall), leaf-blades covered with soft hairs and bluish-green in color, large auricles and a somewhat fragile rachis.
Dorofeev et al. (1980), following Vavilov, distinguished four taxa in domesticated emmer on morphological and geographical bases: abyssinicum Vav. (Abyssinian emmer), asiaticum Vav. (Eastern emmer), dicoccum (European emmer) and maroccanum Flaksb. (Moroccan emmer). These categories were further subdivided by Dorofeev et al. (1980), who distinguished between 8, 13, 40 and 3 botanical varieties within the abyssinicum, asiaticum, dicoccum, and maroccanum taxa, respectively. A detailed description of these botanical varieties is provided by Dorofeev et al. (1980).
Domesticated emmer is the primitive domesticated form of T. turgidum and one of the most ancient cultivated cereals. It was one of the principle wheats in summer-dry, relatively warm south-west Asia, central Asia, the Mediterranean basin, temperate Europe, and Egypt, from the Neolithic time to the second half of the third millennium BP, when it was replaced by the more advanced, free-threshing tetraploid form, T. turgidum ssp. durum (Schrank) Thell (macaroni or hard wheat) (Nesbitt and Samuel 1996; Zohary et al. 2012). In the eighth millennium BP, it was taken from the hilly and mountainous areas of the Fertile Crescent to the lowlands of Mesopotamia, and during the seventh and sixth millennia, to Egypt, the Mediterranean basin, Europe, and central Asia. It was taken to Ethiopia some 5000 years ago. Since its replacement by ssp. durum and by bread wheat, domesticated emmer has been grown as a relic crop in Ethiopia, India, Iran, Transcaucasia, the Volga Basin, eastern Turkey, the Balkans, Italy, Spain and central Europe (Nesbitt and Samuel 1996; Perrino et al. 1996).
Today, domesticated emmer covers only 1% of the total world wheat area (Zaharieva et al. 2010). It has also been introduced to the USA, and presently, limited amounts of spring varieties of domesticated emmer are grown in scattered areas throughout Montana and North Dakota (Stallknecht et al. 1996).
10.3.2.3.2 Genetic Diversity
Domesticated emmer contains very early and late accessions (Zaharieva et al. 2010). Percival (1921), Dorofeev et al. (1980) noted that most emmer wheat landraces are spring types, with the exception of some from western Europe, which are winter type. Damania et al. (1990) found a wide variation in tillering traits, grain protein content, and resistance to common bunt and yellow rust among accessions from Ethiopia, Jordan and Turkey. Wang et al. (2007) reported a wide range of diversity in eight agronomic characteristics among 91 accessions of this subspecies.
Domesticated emmer wheat is characterized by high protein and mineral concentrations; its grain protein concentration can reach 18–23% (Blanco et al. 1990; Dhaliwal 1977a; Perrino et al. 1993; Damania et al.1992). A high variation was found for gluten strength (Blanco et al. 1990; Perrino et al. 1993), and Grausgruber et al. (2004) reported a large variation in rheological properties of this wheat.
10.3.2.3.3 Current Uses of Domesticated Emmer
Domesticated emmer is currently primarily used as a human food, and also for animal and chicken feed (Zaharieva et al. 2010). Ancient Egyptians mainly used domesticated emmer for making a variety of breads (Samuel 1994) and beer (Kemp 1989). In Roman Italy, emmer wheat was used for making bread, as well as porridge and groats (Braun 1995), and is still used in Tuscany as whole grains (farricello) in traditional soups. Its use in the pasta industry is a recent response to the health food market.
10.3.2.3.4 Domesticated Emmer as Health Food
The advantages of domesticated emmer as a health food was recently reviewed by Zaharieva et al. (2010). This subspecies contains an amino acid composition similar to that of bread wheat (Cubadda and Marconi 1996), with some varieties having a higher lysine content (up to 3.65%) (Stehno 2007). Crude fiber content is higher in domesticated emmer than in durum wheat. Mineral and ash content were found in different varieties to be lower, similar, or higher than in durum (Hanchinal et al. 2005; Cubadda and Marconi 1996; Piergiovanni et al. 2009). Domesticated emmer also has a higher concentration of selenium, an important antioxidant factor. Genc and MacDonald (2008) identified domesticated emmer wheat accessions with greater grain zinc concentration than modern durum and bread wheat genotypes.
The nutritional value of domesticated emmer is mainly due to its high fiber and antioxidant concentrations (Piergiovanni et al. 1996), high protein digestibility (Hanchinal et al. 2005) and high resistant-starch content, as well as its slower in vitro carbohydrate digestibility (Mohan and Malleshi 2006). The low glycemic index value and high satiating value (the degree at which food gives a human the sense of food gratification) of this wheat make it particularly suitable for diabetes patients (Buvaneshwari et al. 2003). Most of these qualities are related to a higher total dietary fiber (Yenagi et al. 1999; Annapurna 2000; Hanchinal et al. 2005), which is associated with a reduced rate of starch digestion (Jenkins et al. 1984). Substitution of bread wheat by emmer wheat in the diet for 6 weeks led to a significant reduction in total lipids, triglycerides and LDL (low-density lipoprotein) cholesterol (Zaharieva et al. 2010).
Because of its high value as a health food, nutritional value, and the unique taste of its products, current interest in domesticated emmer is increasing (Zaharieva et al. 2010). Such a renewed interest has its origin mainly in countries with well-developed intensive agriculture (Hammer and Perrino 1995; Nielsen and Mortensen 1998; Olsen 1998).
10.3.2.3.5 Economically Important Genes in Domesticated Emmer
Accessions of domesticated emmer are suited to warm, dry climates, can grow on poor soils, tolerate drought and heat stress, and are resistant to several fungal diseases. As such, they constitute a valuable genetic resource for improving durum and bread wheats. Several accessions of domesticated emmer from Italy were found resistant to stem rust, leaf rust and yellow rust (Corazza et al. 1986). Stem rust resistance was found in the Indian variety Khapli (Jakubziner 1969), in an Israeli accession (Rondon et al. 1966) and in a landrace from Ethiopia (Lebsock et al. 1967). Resistance to yellow rust has also been reported in 18 accessions of emmer wheat belonging to the ICARDA gene bank collection (Damania and Srivastrava 1990). Jakubziner (1969) identified accessions resistance to powdery mildew. A dominant gene for resistance to powdery mildew, designated as Pm4, was transferred by Briggle (1966) from Khapli into the Chancellor variety of bread wheat. Domesticated emmer resistance to loose smut was reported by Michalikova (1970). Similarly, there have been reports of resistance to fusarium head blight (Oliver et al. 2008), tan spot and Septoria blotch (Chu et al. 2008), Russian Wheat Aphid (Robinson and Skovmand 1992) and Hessian Fly (Zhukovsky 1964). Some accessions showed tolerance to drought (Zhukovsky 1964; Damania et al. 1992; Al Hakimi and Monneveux 1997) and heat (Hanchinal et al. 2005).
Domesticated emmer crosses easily with durum wheat and desirable genes can be transferred from the former to the latter. But hybrid necrosis and hybrid chlorosis are frequently met within crosses between domesticated emmer and durum (and also bread wheat), creating significant gene transfer barriers. Hybrid necrosis is governed by two complementary genes, Ne1 and Ne2, located on chromosomes 5B and 2B, respectively (Tsunewaki 1960), and hybrid chlorosis is controlled by two complementary genes, Ch1 located on 2A (Hermsen and Waninge 1972) and Ch2 on 3D (Tsunewaki and Kihara 1961).
Several synthetic hexaploid wheats that were produced at CIMMYT using domesticated emmer as a female parent and Ae. tauschii as a male, were backcrossed to elite cultivars of bread wheat. Several backcross-derived lines were found to have a high level of resistance to green bug (Lage et al. 2003) and Russian wheat aphid (Lage et al. 2004), as well as good grain quality (Lage et al. 2006). Emmer-based synthetic backcross-derived lines also showed higher yield under drought-prone conditions in Mexico, Pakistan and eastern India compared to those using durum wheat (Trethowan and Mujeeb-Kazi 2008).
10.3.2.4 Ssp. paleocolchicum (Men.) A. Löve and D. Löve (Georgian Wheat)
T. turgidum ssp. paleocolchicum (Menabde) A. Löve and D. Löve, known as Kolkhuri Asli, Colchian emmer, or Colchis emmer, kolchis wheat, [Syn.: ssp. georgicum (Dek. et Men.) MK; T. paleocolchicum Men.; T. georgicum (Dek. et Men.) MK: T. dicoccum Schrank grex georgicum Dek. et Men.; T. dicoccum ssp. georgicum (Dek. et Men.) Flaksb.; Triticum dicoccon (Schrank) Schübl.; T. karamyschevii Nevski; T. paleocolchicum Men.; T. turgidum grex paleocolchicum (Men.) Bowden; Gigachilon polonicum (L.) Seidi ssp. paleocolchicum (Men.) Löve; T. macha Dek et Men. ssp. paleocolchicum (Men.) Cai; T. turgidum L. em. Thell. ssp. georgicum (Dek. et Men.) Hanelt]. Van Slageren (1994) maintained that at the species level, the older name T. karamyschevii Nevski should be adopted over the apparently T. paleocolchicum, but Löve and Löve’s combination at the subspecies level is valid.
ssp. paleocolchicum is the second domesticated hulled form of T. turgidum (Table 10.5). This subspecies differs from ssp. dicoccon by its broad, compact, flat spike. The spike has a relatively large number of spikelets (34–36), and 4–5 florets per spikelet. It flowers relatively late, from June to July, and the seeds ripen from August to September. The taxonomic classification and rank have been a matter of much dispute. In light of its distinct morphological traits, it was first included in T. dicoccum as a variety, var. chvamlicum Supat (Supatashvili 1929). Later, Dekaprelevich and Menabde (1932) classified it as a subspecies, namely, T. dicoccum ssp. georgicum, and later, Menabde (1948) (in Jorjadze et al. 2014) ranked it as the species T. paleocolchicum Men. Mac Key (1988) classified it as T. Turgidum ssp. georgicum (Dekapr. & Menabde) Mac Key, whereas van Slageren (1994) considered it as T. turgidum subsp. paleocolchicum (Menabde) A. Love and D. Love. This subspecies contains four varieties (Mosulishvili et al. 2017).
Wang et al. (2019) sequenced and assembled the complete chloroplast (cp) genome sequence of ssp. paleocolchicum, using Illumina sequencing. The assembled cp genome is 136,445 bp in size, and consists of four parts, namely LSC (79,993 bp), SSC (12,832 bp) and two IRs (21,815 bp). Gene annotation found that it encodes 109 non-redundant genes, including 76 protein-coding genes, 29 tRNA genes and 4 rRNA genes, 19 of which are located in the IR region with two copies. An evolutionary tree constructed based on the whole chloroplast genome sequence showed that ssp. paleocolchicum and other species with the BBAA genome were clustered together, while separated from T. timopheevii wheat (GGAA). This study enriched the sequence resources of ssp. paleocolchicum and also provided important data for its molecular identification, marker development and phylogenetic studies.
ssp. paleocolchicum is a small endemic, relic taxon of observed in Georgia (Jorjadze et al. 2014). Currently, it is cultivated on a limited scale in western Georgia (Colchis), often in a mixture with hexaploid wheat T. aestivum ssp. macha. But in the past, it was grown more widely, in eastern Georgia as well. The reason for its maintenance in west Georgia stems from its well performance under the humid conditions prevailing in this part of Georgia. Under these conditions, it has successfully replaced ssp. dicoccon that did not thrive in humid environments. It grows well on sandy, loamy, and clay soils, but prefers well-drained beds. While this subspecies adapts well to the humid climate of west Georgia, it also performs well under the dry, hot climate conditions of east Georgia. It is usually ground into a flour and used for making bread, biscuits, etc. Its grain protein content reaches 18.8%, lysine content is 2.9%, and its high-quality gluten enables the production of a good bread and offers desirable baking properties (Jorjadze et al. 2014). ssp. paleocolchicum is resistant to several fungal disease and can serve as a good source for desirable traits. This subspecies is thought to have been generated by inter-ploidy hybridization between wild emmer wheat, ssp. dicoccoides, and a form of bread wheat (Dvorak and Luo 2001).
10.3.2.5 Ssp. parvicoccum Kislev (Currently Extinct)
T. turgidum L. ssp. parvicoccum (Kislev) Kislev, known as a small-grain wheat (Syn.: T. parvicoccum Kislev sp. nov.), is an archaeobotanical, free-threshing, tetraploid wheat taxon (Kislev 1979,1980, 2009). It seemed justifiable (Kislev 1979/1980) to combine the grains and rachis fragments found in several Near Eastern sites into one taxon since (a) they were located (e.g., in Tel Aphek) within close proximity, at distances of a few millimeters or centimeters; (b) they both belonged to a new taxon; and (c) their morphology was complementary, viz. small grains and compact rachis.
In the description of the species, efforts were made by Kislev (1979/1980, 2009) to reconstruct ssp. parvicoccum as fully as possible. Some features were highly correlated with the habitat or with other plant qualities which survived in the same archaeological sites. The validity of such a description is, of course, not completely satisfactory and the reader may judge each characteristic for himself.
ssp. parvicoccum has a tough rachis with very short and narrow internodes. The grain is very short (about 5-mm-long), oval to elliptic, widest in the middle, thickest in the lower third, with a wide, rounded or truncate apex, and wide, short-haired, and sometimes collared brush, especially in small grains. The embryo is small and oval, the radicle is prominent or slightly so, the plumule is slightly prominent or not at all, the ventral side is flat, ascending at the base, sometimes also at the apex, the crease is narrow or moderately wide and cheeks are rounded.
The following additional characteristics were deduced from circumstantial evidence or correlation with other characteristics: the plant has a domesticated annual, spring habit, and short, dense, compressed and oblong or oval ears. Spikelets are two-grained, and the third floret is reduced. Glumes are very short, diagonally oriented, grains are free, and loosely invested by chaff (Fig. 10.4a–c).
a A coin coined by Agripas 1, king of Judea in the first century AD, showing three wheat spikes, presumably of T. turgidum ssp. parvicoccum, that was cultivated in Israel at least until 130 AD (Kislev 1979/1980), and b grains; and c rachis of T. turgidum L. ssp. parvicoccum Kislev (From Kislev 1979/1980); d A spike and grains of an extracted tetraploid [extracted by Kerber (1964) from the hexaploid cultivar Canthath], that resemble ssp. parvicoccum; e A spike and grains of T. turgidum L ssp. durum (Desf.) Husn. cv. Hourani that according to Kislev (1979/1980) may have derived from ssp. parvicoccum
Kislev (2009) investigated well preserved archaeological remains of ssp. parvicoccum wheat from Late Bronze Timnah (Tel Batash), Israel, and added the following to its morphological description: (1) the culm upper internode is solid, with striate and a slightly rough surface; (2) the ear is bearded, laterally compressed, and of medium to high density; (3) the rachis is fringed, with long hairs along the margins, and bears a frontal tuft of long hairs at the base of each spikelet; (4) the internodes are relatively thick; (5) the spikelets are two-flowered; (6) the outer face of the hairy glumes is somewhat flat, with a prominent keel that runs from the base to the tip; (7) a pair of prominent lumps is present on the rachis node, beneath its glume bases; and (8) after threshing, the basal part of the glume is usually retained on the rachis node.
The archaeological samples of free-threshing (naked), small, and somewhat spherical grains (< 5 mm) and of short internodes found in Near Eastern sites from 8900 to 7000 BP, were considered by Helbaek (1959) to be club wheat, the hexaploid T. aestivum ssp. compactum (= T. compactum antiquorum). However, it is difficult to accept that these Near Eastern wheat remnants from such an early period (9000–7000 years BP) are hexaploids, as explained by Kislev (1979): (1) Modern native strains of hexaploid wheats are more adapted to the northern latitudes (Vavilov 1926) than to the Near East, where Helbaek found his remnants, the latter area being dominated by tetraploid taxa. In the western flank of the Fertile Crescent, however, hexaploid wheat was grown, but only as a crop of little importance (Jakubziner 1932a). (2) Bread wheat (T. aestivum L.) which is sometimes short-grained (c. 5 mm) is lax-eared, while the dense-eared club wheat, T. aestivum ssp. compactum, has grains longer than 5.7 mm (Percival 1921). (3) If Helbaek’s remnants are indeed hexaploid, this implies that hexaploid naked wheat, found in the earliest periods in the Near East, preceded cultivation of tetraploid naked wheats. However, on an evolutionary basis, one would expect that the tetraploids developed first. (4) The earliest samples are probably from too early a period for hexaploid wheats to have come into existence; the spread of agriculture had not yet made geographic contact between the domesticated tetraploid and Ae. tauschii, the wild diploid progenitors of hexaploid wheat.
Based on the morphological characteristics of this archaeological material and the difficulty in defining ancient Near Eastern naked wheat as hexaploid, Kislev (1979/1980) concluded that these wheat remnants belong to an extinct tetraploid species, T. parvicoccum Kislev. According to current classification, this taxon should be referred to as T. turgidum ssp. parvicoccum (Table 10.5).
The first records of the naked tetraploid wheat ssp. parvicoccum were found in the early PPNB. Naked grains were unearthed in phase II of Tell Aswad, near Damascus, dated 8900–8600 BP (Hillman 1996), in Ramad, southwestern Syria, dated 8300 BP (van Zeist and Bakker-Heeres 1982); and in Can Hassan III, south Anatolia, dated 8400 BP (Hillman 1972, 1978). Remnants of naked, small-grain wheat were also reported in Atlit Yam, Israel, the late PPNB (8000–7500 BP) (Kislev et al. 2004) and in various sites in the Pottery Neolithic period (7500–6200 BP), including western Iran, Anatolia, Iraq, Syria, Israel, Georgia, and the Balkans (Kislev 1979/1980, 1981; Schultze-Motel 2019). Archaeological excavations in Israel dated it to as late as 1870 years BP (Kislev 1979/1980, 1981). Schulz–Motel (2019) found ssp. parvicoccum that was presumably grown in Georgia about 800 years BP. It was abundantly grown from the 8th millennium BP onwards in south-east Asia, Transcaucasia and the Balkans (see list of sites in Kislev 1979/1980, 2009). Schultze-Motel (2019) detected it recently in two places in Georgia, broadening the area of this species to the north.
The great advantage of ssp. parvicoccum was its comparatively delicate glumes and tough rachis nodes, which facilitated easy threshing of its grains. The fact that both hulled and naked wheat were found contemporaneously in the Near East for such a long period may indicate that the overall advantage of the latter (free-threshing, but with small grains) must not have been sufficiently great to replace the former (bearing large but hulled grains) as a major crop. In biblical times, they were grown in separate fields and treated as two different, albeit closely related, crops (Kislev 1979/1980, 1981). ssp. parvicoccum was replaced by the related taxon, ssp. durum, that became more abundant, since it combines the free-threshing feature of parvicoccum and the large grains of dicoccon.
The origin of ssp. parvicoccum is obscure. Three major morphological characters distinguish it from domesticated emmer, namely, nakedness (free-threshability), ear compactness, and small grain size. The free-threshing trait could have been derived from a mutation that reduces the toughness of the glumes and increase the rigidity of the rachis (McFadden and Sears 1946; Morris and Sears 1967). The hulled, non-free-threshing emmer contains the q gene, which determines both a semi-fragile rachis and tough, thick glumes. All the extant free-threshing tetraploids contain the Q factor, dictating the free-threshing trait (Muramatsu 1986; Simons et al. 2006). This gene was recently isolated and characterized (Faris et al. 2003; Jantasuriyarat et al. 2004; Simons et al. 2006). Consequently, it is assumed that the ancient free-threshing ssp. parvicoccum also contained this gene. The Q factor, located on chromosome arm 5AL of common wheat (Sears 1954), has a pleiotropic expression pattern, affecting free-threshing as well as several other characteristics that are related to spike and spikelet structure, such as tough rachis and loose glumes. The mutation from q to Q occurred at the tetraploid level, from where it was presumably transferred to hexaploid wheat (Simons et al. 2006). The two alleles differ in a single amino acid, and Q is more abundantly transcribed than q (Simons et al. 2006). The higher expression of Q is in accord with the finding of Muramatsu (1963), who noted that extra doses (five or six) of q mimic the effect of Q in bread wheat. There is a wide variation in the phenotype of QQ lines, which is presumably due to different genetic backgrounds.
In addition to q, there is also an extra dose of group-2 chromosomes in bread wheat, which increases glume toughness (Sears 1954). In accord with this, Kerber and Rowland (1974) found the Tg (tenacious glumes) gene, conferring tough glumes, on chromosome arm 2DS of Ae. tauschii. Likewise, addition of the short arm of chromosome 2Sl (2SlS) of Ae. longissima to common wheat resulted in a similar effect (Feldman unpublished). Chromosome arm 2BS of emmer also contains the Tg gene which determines tough glumes, whereas chromosome arm 2AS does not contain such a gene (Simonetti et al. 1999). Thus, this character is determined in tetraploid wheat by, at least, two complementary genes, Q and tg. Thus, at least two mutations were required to produce the free-threshing character in ssp. parvicoccum (Jantasuriyarat et al. 2004).
Wild and domesticated emmer have long grains, and almost no transitional forms between types with long and short grains are known in the archaeological literature. Yet, in PPNB of Çayönü, southeastern Turkey, a few mid-long grains of domesticated emmer were unearthed (van Zeist 1972), suggesting that the missing link between long and short grains may have been a compact, short-grained domesticated emmer. Outside the Near East, two early Neolithic findings of mid-long grains of naked wheat from Azmak, south Bulgaria, dated to the beginning of the 7th millennium BP, were found (Hopf 1973). Their mean dimensions are 5.6 × 3.3 × 2.9 mm and 5.8 × 3.2 × 2.7 mm. The formation of small-grained wheat presumably occurred as a result of a series of mutations, such as an s-like mutation, which shortened the grain and made the ear dense, as found in other tetraploids (Schmidt and Johnson 1963).
ssp. parvicoccum has been found hitherto in the Near East and the Balkans (Kislev 1979/1980). Recently, Schultze-Motel (2019) found grains of ssp. parvicoccum in several sites in Georgia, dated to about 2300 and 800 BP. According to Kislev (1979/1980), ssp. parvicoccum was grown side by side with domesticated emmer, ssp. dicoccon, in the East Mediterranean and Near Eastern regions over several millennia. The last evidence for cultivation of this subspecies in the Levant is from up 1900 years ago (Kislev 1979/1980, 1981). ssp. parvicoccum was grown in Georgia up to 800 years ago (Schultze-Motel 2019).
Changes in spike compactness and grain size probably occurred as a result of a series of mutations, including an s-like (sphaerococcum-like) mutation that shortened the grain and increased ear density. Such a mutation creating a sphaerococcum-like tetraploid wheat, was indeed described by Schmidt and Johnson (1963). The finding of a few medium-sized grains of wild and/or domesticated emmer In PPNB Çayönü, led Kislev (1979/1980) to suggests that the missing link may have been a compact, short-grained emmer. Alternatively, these traits developed in the free-threshing wheat. In addition, one cannot rule out the introgression of genes conferring compact spikes and short grains from tetraploid Aegilops species, such as Ae. peregrina (= Ae. variabilis) or Ae. geniculata (= Ae. ovata).
10.3.2.6 Ssp. durum (Desf.) Husn. (Macaroni or Hard Wheat)
10.3.2.6.1 Description of Subspecies
T. turgidum ssp. durum (Desf.) Husn., known as macaroni wheat, hard wheat or simply durum wheat, [Syn.: T. durum Desf.; T. alatum Peterm.; T. vulgare var. grex durum Alef.; T. sativum durum Hack.; T. sativum ssp. durum (Desf.) K. Richt.; T. aestivum ssp. durum (Desf.) Thell.; T. turgidum ssp. sementivum Rasse durum (Desf.) Thell.; T. turgidum grex durum (Desf.) Bowden; T. turgidum ssp. durum Löve and Löve; T. turgidum ssp. turgidum convr. durum (Desf.) MK; Gigachilon polonicum (L.) Seidl ssp. durum (Desf.) Á. Löve] is a predominantly autogamous, plant. Its culms, usually 3–4 per plant, are erect, 60–160-cm-high, with 5 or 6 internodes above ground, and generally solid throughout or in the upper internodes, while hollow with thick walls in some varieties. The leaves are linear, flat, 16–25-cm-long, yellowish-green or bluish-green, glabrous in most varieties, and with a transparent ligule and ciliate auricle. The spikes are 4–11-cm-long (excluding awns), two-rowed, determinate, almost always awned, laterally compressed, oblong, or square in cross-section, depending upon the laxness of the spike, and the number and size of the grains in each spikelet, and bear an average of 20 spikelets per spike, at a density varying from about 20 in lax spikes to 47 in compact ones per 10 cm length of rachis. The rachis is usually tough and non-brittle, although in some varieties, it disarticulates more or less easily, especially near the base of the spike; it is fringed with hairs along the margins and bears a frontal tuft at the base of each spikelet, and its internodes are 2.5–5-mm-long, flattened, narrow and wedge-shaped. The spikelets are 10–15-mm-long, with 5–7 florets, the upper 2 or 3 being sterile, and those of square spikes containing three or four grains, while those of compressed spikes usually contain only two. The glumes are yellow, red, or blue-black in color, loosely appressed to the lower florets, glabrous in some varieties and pubescent in others, with considerable variation in hair length and amount, glumes of the lateral spikelets being 8–12-mm-long, asymmetrical, with one prominent keel running from the base to the tip, and 5–7 nerves running from the base to a point close to the apical tooth, with the latter being acute or blunt, and of variable length, and the lateral secondary tooth usually being short or missing. The glumes of the terminal spikelet are ovate and more or less symmetrical. The lemmas are thin and pale, rounded on the back, 10–12-mm-long, with 9–15 nerves which converge at the tip into a terminal, firm awn. As a rule, only the two lower lemmas of each spikelet bear long awns, measuring, in some cases in the lower spikelets, as long as 20–23 cm, longer than those of any other wheats. The awns of the flowers of the upper spikelet are usually 5–4 cm long, i.e., all awns of a spike usually terminate at the same height. Some varieties are awnless or have short (6.0 cm) or medium (6.1–9.0 cm) length awns. The awns are white, red, or black, almost smooth near the base, thus differing from those of ssp. turgidum which are usually rough throughout their entire length, generally straight and more or less parallel to the sides of the spike. The palea is membranous and shorter than the corresponding lemma, and does not split at maturity. The caryopsis is larger (45–60 mg) than those of other wheats, glabrous, free of lemma and palea, white, amber, yellow, or red in color, generally somewhat narrow, tapering towards both ends, more or less laterally compressed, with a narrow dorsal ridge, and wanting in plumpness, and with a shallow furrow usually exhibiting flattish sloping sides; the cross-section is more or less triangular. The embryo is large, with an elongated oval scutellum. Measurements of grains taken from the middle of the spike of flinty forms were of an average length of 8.30 (7.0–9.7) mm, average breadth of 3.48 (2.8–4.1) mm, and an average thickness of 3.61 (3.2–4.25) mm. However, some cultivars, e.g., Hurani, have smaller (about 5 mm long) grains. Most varieties grow in the spring, while several grow in the winter (Fig. 10.3b).
Durum in Latin means “hard” and reflects the hard-flinty nature of the plant grain, the hardest of all other wheat grains. Yet, the name Hard Wheat is confusing, as it is applied to forms of North American bread wheat. It is advisable therefore, to use the common name durum wheat or macaroni wheat for this subspecies.
Because of the similarity between plant remains of tetraploid and hexaploid free-threshing wheats, it was very difficult, if not impossible, to identify the species of the Pre-Pottery Neolithic B (PPNB; 9500–7500 BP) wheat remnants, and consequently, they were referred to as T. turgidum-T. aestivum or as ‘aestivo- compactum’ wheats (Zohary et al. 2012). In fact, almost all naked (free-threshing) wheat remnants described so far have been compared to a free-threshing hexaploid wheat that was grown by the Neolithic Lake dwellers of Switzerland during the Bronze Age, described by Heer (1886) as T. vulgare antiquorum. This wheat, now believed to be extinct, was very similar to T. aestivum ssp. compactum (club wheat); it was a dwarf plant, with extremely small, stubby grains and compact, awnless spikes. Because of its resemblance to T. aestivum ssp. compactum, it has generally been assumed to have been a hexaploid. In fact, palaeoethnobotanists have already described very early naked wheat remnants as belonging to hexaploid species. For example, Helbaek (1959) identified archaeological samples of small grains (less than 5 mm in length) and short internodes, found in very early Near Eastern sites, as hexaploid T. compactum.
Yet, Kislev (1979/1980) found it difficult to explain these remnants as hexaploids for the following reasons: (i) Modern genotypes of hexaploid wheats are more adapted to the northern latitudes than to the Near East, the latter area being dominated by tetraploid forms. In the western flank of the Fertile Crescent, however, hexaploid wheats are grown, but only as a crop of little importance (Jakubziner 1932a) (ii) The most ancient samples are probably from too early a period for hexaploid wheats to have come into existence (van Zeist 1976), i.e., the beginning of the 8th millennium BP; the spread of agriculture had not yet made geographic contact between domesticated tetraploid wheats and Aegilops tauschii, the wild diploid donor of the third subgenome (subgenome D) to hexaploid wheat. Since hexaploid wheat originated toward the middle or even the end of the 8th millennium BP (Kislev 1984), in northwestern Iran, south of the Caspian Sea (Dvorak et al. 1998a, b), outside the Fertile Crescent region, it has to be assumed that most of the PPNB remnants of naked wheat in the Fertile Crescent are of tetraploid forms rather than of hexaploid wheats.
The idea that wheat grown in the ancient Near East was tetraploid rather than hexaploid, has been recently suggested by several researchers (Kislev 1973; van Zeist and Bakker-Heeres 1973; Zohary 1973). Yet, because of the small grains (less than 5 mm in length) and short internodes characterizing these wheat remnants, Kislev (1979/1980) suggested that these wheats belong to an extinct tetraploid taxon, named T. parvicoccum Kislev (currently T. turgidum L. ssp. parvicoccum Kislev). Practically, all prehistoric naked wheat grains in the Fertile Crescent and East Mediterranean regions are less than 5 mm on average (Kislev 1979/1980).
Ssp. durum evolved only later, presumably from hybridization of domesticated emmer and ssp. parvicoccum. Renfrew (1973) indicated that archeological studies suggest that durum wheat may have originated later than hexaploid wheat. Material ascribed to ssp. durum has been found, at first sporadically, among prehistoric plant remnants, already from the 8th millennia BP in Syria. It was unearthed by Hillman (1978) in layers of Pottery Neolithic Can Hassan III (7500–6200 BP). During later Neolithic periods, this wheat gradually gained prominence, until it became the main wheat in the Mediterranean countries, first in its western part, and only in the Helenistic time, in the east Mediterranean and Egypt. It was suggested that ssp. durum was derived from domesticated emmer by a series of mutations that reduced the toughness of the glumes until a free-threshing form was attained (McFadden and Sears 1946; Morris and Sears 1967; Sears 1969). Alternatively, it could have derived from the free-threshing ssp. parvicoccum, or more likely, from crosses between parvicoccum and dicoccon. Hybridization between parvicoccum and dicoccon may lead to the formation of progeny with the free-threshing trait from parvicoccum and the large grains from dicoccon.
Studies of chloroplast markers (cpSSRs) indicated that wild and domesticated emmer and ssp. durum share a common maternal ancestral gene pool (Oliveira et al. 2012). Zohary et al. (2012) proposed that the early naked forms of tetraploid wheats evolved from domesticated emmer in the Fertile Crescent. The data of Oliveira et al. (2012) support this hypothesis. If this event occurred only once or several limited number of times, it is reasonable to assume that only a small number of cp-haplotypes, from a broader gene pool present in domesticated emmer, would appear in the early naked tetraploid forms, and later in ssp. durum, as a consequence of a bottleneck effect. This is apparent from the strong difference between the hulled wild and domesticated emmer and the naked tetraploid wheat, ssp. durum, suggests that the latter subspecies evolved from only a small number of hulled tetraploid genotypes, and have been in relative reproductive isolation since their spread into Europe and North Africa during the Neolithic Age. Oliviera et al. (2012) also detected cp-haplotypes in accessions of both wild emmer and ssp. durum. This suggested an alternate scenario in which free-threshing tetraploid wheats were domesticated de novo from lines of wild emmer, independently acquiring, by mutation, the tough-rachis trait of domesticated emmer, plus the free-threshing trait.
The fact that ssp. durum, for which evidence dates back to 6500–7500 BP, became established as a prominent crop in the east Mediterranean only 2000–2300 years ago, requires an explanation. More specifically, it is perplexing that in spite of its relatively early origin, ssp. durum, featuring both large grains like those of ssp. dicoccon, and a free-threshing trait like that of ssp. parvicoccum, was only established as a major crop in the Mediterranean basin and the Near East during the Late Bronze Age and Hellenistic period (Nesbitt, 2002; Feldman and Kislev 2007). Perhaps the early durum types were not actively cultivated because small-grained wheat and domesticated emmer were better adapted to the semi-arid conditions of the region. Adapted genotypes evolved only later, through a series of mutations, or through introgression of genes from the other two tetraploid subspecies. Kislev (2009) suggested that small grains may have been more competitive than large grains because they could not be attacked by Sitophilus granarius, the most destructive pest beetle of stored cereals. Because the size of its larva would take up half of the parvicoccum grain, it would fail to provide sufficient food for the pest’s normal development. Only upon construction of air-sealed granaries in the classical period, did larger grains become more resistant to pest beetle. Taken together, development of sealable granaries may explain the establishment of ssp. durum in the Near East and the impoverishment of ssp. parvicoccum (Kislev 2009).
The large grain of ssp. durum was probably preferred over the small grains of parvicoccum, and likely lead to the prominence of durum as a tetraploid wheat and to the extinction of parvicoccum. Most other subspecies of T. turgidum with a naked grain are probably of a relatively more recent origin; they deviate from ssp. durum in only a few characteristics (Mac Key 1966; Morris and Sears 1967) and share the genetic system for the free-threshing habit. The cultivation of ssp. parvicoccum alongside ssp. durum in the Near East may explain the morphology of some peculiar taxa of naked tetraploid wheats, such as the compact cv. pyramidale Perc. in Egypt and Horan wheat, cv. horanicum (Jakubz.) Flaksb. in the Levant, with compact ears and small-plump grains (Fig. 10.4e). Also, the extracted tetraploids, derived from T. aestivum ssp. aestivum by Kerber (1964), resemble very much ssp. parvicoccum (Fig. 10.4d). Crosses between durum and parvicoccum might have resulted in such intermediate forms. These new taxa, some of which are adapted to semi-arid conditions, took the place of the old small-grained wheat.
In southwest Asia and in the Mediterranean basin, hulled and parvicoccum wheats were replaced by more modern free-threshing types. Up to the present time, the hulled wheats, emmer and einkorn, continued to occur as minor components. In south-eastern Turkey emmer was replaced by more modern free-threshing wheats at the beginning of the Early Bronze Age (ca. 5000 BP) and have been nearly absent from the archaeobotanical record thereafter (van Zeist and Bakker-Heeres 1975; Nesbitt 1995). In central Turkey, einkorn and emmer appear to be minor crops in Middle Bronze Age samples (3900–3700 BP) (Nesbitt 1993). In the Levant, emmer became a minor component in the 5th millennium BP and almost disappeared in the 4th millennium BP (Miller 1991), whereas in Egypt, emmer was grown until the Hellenistic time (ca. 2300 BP), when it was replaced by the free-threshing ssp. durum (Crawford 1979; Bowman 1990). For further details, see Nesbitt and Samuel (1996). Towards the Late Bronze Age, southwest Asia and the Mediterranean basin both showed a high prevalence of naked wheats. The large quantities of naked wheat unearthed in the Levantine Bronze Age villages in the Levant are impressive (Zohary et al. 2012).
10.3.2.6.2 Current Cultivation of Durum Wheat
The earliest historical reference to durum wheat was made by Dodoens in his Historia frumentorum, published in 1566. Only near the end of the eighteenth century was ssp. durum distinguished from the Mediterranean forms of ssp. turgidum and ssp. aestivum by Desfontaines, who described it in his Flora Atlantica, mentioning solid straw, pubescent glumes, and long flinty grain as its specific characteristics. Today, ssp. durum is the principal tetraploid wheat and next to bread wheat, T. aestivum ssp. aestivum, the various varieties of ssp. durum are the most widely cultivated tetraploid wheats, constituting about 5–9% of global wheat production. The area planted annually is approximately 20 million hectares, averaging about 38 million metric tons annually (FAOSTAT 2018), and current trends are upwards. ssp. durum developed in the hot and dry climate of the Near East and Mediterranean basin. Currently, it grows as a major crop in the Mediterranean basin (Portugal, Spain, Italy, Morocco, Algeria, Tunisia, Egypt, Greece, Turkey, Syria, Lebanon, Israel, and Jordan), the Near East (Iraq and Iran), trans- and cis-Caucasia, Afghanistan, Pakistan, Turkestan, Kazakhstan, the southern portion of East Siberia, Bulgaria, Ukraine, southern Russia, Ethiopia, India, China, and in low rainfall areas of the great plains of the United States and Canada, Mexico, Chili, Argentina, South Africa and Australia (Feldman 2001). The European Union (mainly Italy, Spain, and Greece) is the largest durum wheat producer, Canada is the second largest producer, followed by Turkey and the USA.
10.3.2.6.3 Genetic Analysis of Durum Wheat
A recent major achievement in the study of genome structure of durum wheat is the assembly of 10.45 gigabase (Gb) of the genome of cultivar Svevo by Maccaferri et al. (2019) (see Sect. 3.3.2.2. in Chap. 3). This assembly facilitated the comparison between the genome of ssp. durum and that of its wild ancestor, ssp. dicoccoides, that was sequenced earlier (Avni et al. 2017) (see Sect. 3.3.2.1. in Chap. 3). The comparison revealed, and will continue to do so, changes imposed by the domestication process, by thousands of years of unconscious and conscious selection under cultivation, and by modern, scientific based, breeding. Regions exhibiting strong signatures of genetic divergence associated with domestication and breeding were widespread in the durum genome with several major diversity losses in the pericentromeric regions that occurred during domestication of wild emmer. The reduction of diversity continued more moderately, but spread over the genome, during the evolution of domesticated emmer wheat and that of durum landraces, and, more recently, in modern cultivars as a consequence of the breeding activity.
The study of the assembled genome of the modern Italian durum cultivar Svevo by Maccaferri et al. (2019) showed little evidence of a polyphyletic origin of this subspecies. Principal component analysis showed a close relationship between Svevo and a specific group of durum landrace populations. The observations indicated that two domesticated emmer populations from the southern Levant showed the closest relationship to all durum wheat landrace populations, while the modern durum cultivars were mostly related to two durum wheat landrace populations from North Africa and Transcaucasia. Landraces of ssp. durum from Ethiopia, were genetically isolated.
Assembly of the genomes of durum and dicoccoides may provide a better understanding of how the two durum subgenomes, A and B, interact and coordinate their activities. It may clarify the nature and mode of action of the genetic mechanism(s) governing cytological and genetic diploidization in allopolyploid wheats. These are fundamental biological questions that may elucidate the reasons for the evolutionary success of this allotetraploid as well as of other Triticum and Aegilops allopolyploids.
Assembly of the durum genome will facilitate the investigation of the genetic control of many agricultural and nutritional properties in this important crop, via analysis of genes, their structure, order, control of expression, and communication with one another. It may lead to the identification of genes that are responsible for useful traits such as yield, disease resistance, and nutritional properties, allowing for their selected for breeding programs. For instance, Maccaferri et al. (2019) has already identified the gene most likely responsible for high cadmium (Cd) accumulation in the grains of modern cultivars, an undesirable gene located on chromosome 5B, and the recovery of an allele for a low Cd build up.
During the last several millennia, durum wheat has spread all over the world, which has been accompanied by increased diversity driven by unintentional and conscious selection of adaptive genotypes for different climatic and edaphic conditions as well as different human tastes. The main centers of variation of ssp. durum are in southwest Asia, the Mediterranean basin and Ethiopia. Genetic improvement of durum wheat began very late and has proceeded more slowly than that of common wheat. Breeding of durum wheat is currently concentrating on the simultaneous improvement of grain yield, disease and insect resistance, tolerance to abiotic stresses (cold, heat, drought and salt), grain quality traits, and processing quality traits, including protein concentration, yellow pigment concentration (high carotenoids and flavonoids content), gluten strength, semolina milling properties, and pasta cooking quality.
The increase in genetic diversity of ssp. durum is manifested by the large number of varieties and land races. Percival (1921) described more than 60 varieties, based on spike characteristics, such as awn presence or absence, glume color (white, red or black), pubescence or glabrousness, awn color, and grain color and texture. In the monograph by Dorofeev et al. (1980), durum wheat (as T. durum) is subdivided into the ssp. durum and ssp. horanicum Vav., and about 140 botanical varieties were described, mainly on the basis of spike and grain characteristics.
A consensus genetic map presented by Maccaferri et al. (2014), providing nearly complete genome coverage, as well as marker density, was used as a reference for genetic diversity and mapping analyses of ssp. durum. The consensus map provides the basis for high-density single nucleotide polymorphic (SNP) marker implementation in durum wheat. Markers previously mapped in hexaploid wheat constitute a strong link between the two species. But, differences in marker order and local recombination rate were observed between the durum and hexaploid wheat consensus maps.
Seventy SSRs and 234 AFLPs were used to profile a collection of 58 durum wheat accessions representing the most important extant breeding programs (Maccaferri et al. 2007). In addition, 42 phenotypic traits, including the morphological characteristics recommended for the distinctness, uniformity, and stability tests, were recorded. The correlation between the genetic similarities obtained with the two marker classes was high (r = 0.81), whereas lower correlations were observed between molecular and phenotypic data (r = 0.46 and 0.56 for AFLPs and SSRs, respectively). Morphological data, even if sampled in high numbers, largely failed to describe the pattern of genetic similarity, according to known pedigree data and the indications provided by molecular markers.
Levels of genetic diversity and population genetic structure of a collection of 230 accessions of seven subspecies of T. turgidum were investigated by Laidò et al. (2013), using six morphological, nine seed storage protein loci, 26 SSRs and 970 DArTs. As expected, genetic diversity of the morphological traits and seed storage proteins was always lower in durum wheat compared to those of wild and domesticated emmers. The two sets of molecular markers distinguished durum cultivars from the other free-threshing subspecies of T. turgidum. The genetic diversity of morphological traits and seed storage proteins was always lower in the improved versus older durum cultivars. This marked effect on diversity was not observed for molecular markers, where there was only a weak reduction. The SSR markers identified a greater number of groups within each subspecies as compared to DArT.
Kabbaj et al. (2017) investigated population structure and genetic diversity among elites and landraces of durum wheat collected from 32 countries. A total of 10 sub-populations were identified, with six bearing modern germplasm and four constituting landraces of different geographical origins. Interestingly, genomic comparison between groups indicated that the Middle East and Ethiopia had the lowest level of allelic diversity, while breeding programs and landraces collected outside these regions were the richest in rare alleles. Further, phylogenetic analysis of landraces indicated that Ethiopia represents a second center of durum wheat diversity. Overall, the analyses performed by Kabbaj et al. (2017) provided a global picture of the current genetic diversity for this crop and shall guide its targeted use by breeders.
10.3.2.6.4 Durum Products
The large, hard-textured grains of ssp. durum yield low-gluten flour that creates plastic doughs, contrasting with the strong elastic doughs obtained from flour of bread wheat. As a result, durum wheat is less commonly used in bread making and is especially suitable for making pasta and other semolina products (Hanelt 2001). Durum breads do exist, but, in most instances, the doughs contain only a portion of durum flour and are substantially supplemented with white bread wheat flours; often, bread wheat flour is high in gluten, and is necessary to offset the poor contribution of durum flour to the gluten network. Pure durum breads are often dense, containing few air bubbles, with relatively little elastic structure. Most of the durum grown today is amber durum, the grains of which are amber-colored and larger than those of other types of wheat. Durum has a yellow endosperm that gives pasta its color. When milled, the endosperm is ground into a granular product called semolina, which is used for premium pastas. In southern Europe, it is mainly used for pasta, whereas in North Africa, is used for couscous and in the Levant, for dishes such as tabbouleh, kubbeh, frikeh and bulgur for pilafs. The Israeli variant of couscous involves larger pearls of durum called ptitim in Hebrew. In many Mediterranean countries, it forms the basis of many soups, gruels, stuffings, puddings and pastries. When ground as fine as flour, it is used for making bread; in the Middle East, it is used for flat round breads (pita), and in Europe and elsewhere, it is used for pizza.
Sayaslan et al. (2012) found that several durum landraces have the potential to improve high-quality pasta processing of modern durum cultivars. The seed protein composition may affect the pasta and semolina quality. SDS-PAGE analyses were performed to characterize the four seed protein fractions (albumins, globulins, gliadins, and glutenin subunits), as well as several proteins from each of the four subunits of gliadin (α, β, γ, and ω) in the grains of five bread wheat and five durum wheat genotypes (Žilić et al. 2011). In addition, content of tryptophan and wet gluten were analyzed. It was found that gliadin and glutenin subunits comprised from 58.17% to 65.27% and 56.25% to 64.48%, respectively, of total proteins and, as such, account for both quantity and quality of the bread and durum wheat grain proteins. The analysis demonstrated that bread wheat genotypes had a higher concentration of α + β + γ-subunits of gliadin (on average, 61.54% of extractable proteins) as compared to durum wheat (above 55% of extractable proteins). Low concentrations of the ω-subunit were found in both bread (0.50–2.53% of extractable proteins) and durum (3.65–6.99% of extractable proteins) wheat genotypes. On average, durum wheat contained significantly higher amounts of tryptophan and wet gluten (0.163% dry weight (dw) and 26.96% dw, respectively) than bread wheat (0.147% dw and 24.18% dw, respectively).
High polymorphism of gliadin alleles was described by Dukic et al. (2008) in 21 durum wheat cultivars, each exhibiting different gliadin allelic composition. Gliadin alleles at the Gli-B1 locus showed the highest positive connection with gluten contents associating with good gluten quality and water absorption of flour. A great variation in high molecular weight (HMW) and low molecular weight (LMW) glutenin subunit was found in landraces compared to very low one in modern cultivars (Nazco et al. 2014a, b). The large variation found in landraces proved their potential value in breeding for gluten quality improvement.
The carotenoid concentration in grains of durum wheat is a criterion for the assessment of semolina quality, and it is of particular importance in determining the color of pasta (Beleggia et al. 2011). Among carotenoids controlling yellow color, the presence of β-carotene is also important as precursors of vitamin A. Blanco et al. (2011) detected the amount of individual carotenoid compounds (lutein, zeaxanthin, β-kryptoxanthin, α-carotene and β-carotene) in different durum lines and in segregating populations from inter-lines crosses. Total yellow pigment concentration among the durum genotypes was variable in all environments, but the genotype x environment interaction was not significant. Carotenoid concentration amounted to 37% of the yellow pigments, indicating the existence of unknown color-producing compounds in the durum extracts. Lutein was the most abundant carotenoid, followed by zeaxanthin, α-carotene and β-carotene, while β-Kryptoxanthin was a minor component. The phytoene synthase marker Psy-A1, 150 SSR and EST-SSR markers, and 345 DArT® markers, were used in search for QTLs affecting the various carotenoid compounds. Clusters of QTL for total and/or one or more carotenoid compounds were detected on chromosomes 2A, 3B, 5A and 7A, where major QTLs for yellow pigment concentration and yellow index were identified. The molecular markers associated with major QTLs would be useful in marker-assisted selection programs, to enhance the concentrations of carotenoid compounds with high nutritional value in wheat grain.
Grain characteristics that affect the technological quality of durum wheat, namely, semolina yield and its ability to be processed into pasta, were defined by Porceddu (1995). Semolina yield is influenced by a fusion of grade, intrinsic properties and ash content. Pasta quality can be considered either from the visual or cooking point of view. The visual aspect considers pasta color, which is a combination of yellowness and brownness, the former determined by the carotenoid content and lipoxygenase activity, while the latter is attributed to peroxidase and polyphenoxydase. Cooking quality is associated with gluten properties. Protein content may account for 30–40% of the variability in cooking quality, but the protein ratio, i.e., the of gliadin and glutenin components, has a strong effect on quality.
The very hard texture of durum grains is due to the loss of the puroindoline genes that were eliminated during the allopolyploid formation of ssp. dicoccoides, 0.7–0.9 million years ago (Marcussen et al. 2014). Morris et al. (2011) described transfer of the puroindoline genes from chromosome 5D of T. aestivum cv. Chinese Spring to ssp. durum cv. Langdon, using a Langdon 5D(5B) disomic substitution line, which allowed homoeologous pairing due to the absence of chromosome 5B that carries the Ph1 gene. Puroindoline a and puroindoline b were successfully transferred to durum cv. Svevo, which segregated to soft: heterozygous: very hard in a 1:2:1 ratio. The final backcross (BC3) Svevo line produced uniformly soft grains. The transfer of this fundamental grain property to durum wheat will undoubtedly have an expansive and profound effect on the way that durum grain is milled as well as on the products derived from it (Royo and Abio 2003; Morris et al. 2011).
10.3.2.6.5 Importance of Durum Germplasm
Ssp. durum usually has higher yields than other wheats in areas of low precipitation (250–350 mm per annum). In districts too dry to support the cultivation of bread wheat, ssp. durum will yield 2000–4000 kg per hectare. Its growth is most prosperous, however, in areas with higher annual rainfall. ssp. durum does not tiller much but grows rapidly and succeeds best as a spring crop. In regions with mild winters, it may be sown in autumn, whereas in regions with freezing winters, it is sown in the spring.
Lines of ssp. durum contain genes conferring resistance to biotic stresses and tolerance to abiotic stresses. Several lines show good resistance to powdery mildew (Marone et al. 2013), stem rust (Klindworth et al. 2007; Aghaee-Sarbarzeh et al. 2013; Lemma et al. 2014; Nirmala et al. 2017; Miedaner et al. 2019), leaf rust (Maccaferri et al. 2008; Marone et al. 2009), stripe (yellow) rust (Yahyaoui et al. 2000; Lin et al. 2018), Septoria tritici (van Ginkel and Scharen 1988; Ferjaoui et al. 2015; Berraies et al. 2014; Kidane et al. 2017), Septoria nodorum (Nelson and Gates 1982; Cao et al. 2001), Hessia fly (Amri et al. 1990; El Bouhssini et al. 1999; Ratcliffe et al. 2002; Bassi et al. 2019), and soil-borne cereal mosaic virus (Vallega and Rubies-Autonell 1985; Maccaferri et al. 2012). Lines of durum wheat show tolerance to abiotic stresses such as drought (Saleeem 2003; Golabadi et al. 2006; Diab et al. 2008; Nouri et al. 2011; Kacem et al. 2017), salt (Royo and Abió 2003; Borrelli et al. 2011; Kim et al. 2016; Blumenthal et al. 1995; Sall et al. 2018), and cold (Szűcs et al. 2003; Longin et al. 2013).
Yield loss from sawfly (Cephus cinctus Norton) can be prevented by growing solid-stemmed durum wheat. When crossing solid-stemmed with hollow-stemmed durum lines, Clarke et al. (2002a) found that the F1 were solid-stemmed, and the F2 had three solid-stem to 1 hollow stem plants, showing that the expression of stem solidness fit the expected segregation ratios for a single dominant gene.
Clarke et al. (2002b) assessed the effect of low grain cadmium concentrations on uptake of other elements and on economic traits, such as yield. Grain yield, test weight, kernel weight and protein concentration were determined in five pairs of near-isogenic high/low cadmium durum wheat lines and their parents that were grown in a randomized complete block trial, with three replications. Average grain cadmium concentration differed across years within a given locations, across locations within a given year, and among genotypes. The average grain cadmium concentration of the high-cadmium isolines was approximately double that of the low-cadmium isolines. Grain concentrations of the other tested elements were associated with significant genotypic differences, but the differences were not associated with the high or low cadmium traits. The low-cadmium allele seemed to be specific for cadmium, lowering cadmium without altering concentrations of other elements or affecting economic traits. The low-cadmium trait had no significant effect on average yield, grain protein concentration, test weight, or kernel weight, as indicated by comparison of the high- and low-cadmium isolines.
10.3.2.6.6 Triticum pyramidale Percival
T. pyramidale Percival (Egyptian cone wheat) was considered by Miller (1987) as a special form of T. turgidum senso stricto, but by Mac Key (1966, 1975), as a dense-eared form of ssp. durum. It is a small race, found only in Egypt and Ethiopia, and among the earliest wheats (Percival 1921), with features including short straw, characteristic yellow-green culm leaves, and pointed grains. Egyptian Cone Wheat is a small and distinct race confined to Egypt and Ethiopia. Percival (1921) regarded it as an endemic dense-spiked mutation derived from the Ethiopian form of ssp. dicoccon. It is similar to the latter in the pubescence of its young leaves, yellow-green culm-leaves, short culms, very early habit, and the shape of its grain, and only differs from it in having short, dense spikes, with a tough rachis and free-threshing grain.
10.3.2.7 Ssp. turgidum (Rivet, Cone, or Pollard Wheat)
T. turgidum ssp. turgidum, known as rivet, cone, pollard, or branched wheat (Syn.: T. turgidum L.; T. sativum Hackel.), is a predominantly autogamous plant. It is the tallest of all wheats, with a culm reaching an average height of about 150 cm (120–180 cm) or more. It is slender but strong, having six or seven internodes above ground, the upper internode being curved and, in many forms, solid or filled with pith, while, when hollow, the culm wall is thick. The young shoot is prostrate or semi-erect and the culms are semi-erect or erect. The culm leaves are long and broad, with both sides covered with short, soft, white hairs. The auricles are usually fringed, with a few long hairs. The spikes are simple or branched at base, compact or relatively lax, 7.0–11.5-cm-long (excluding awns), bearing 19–33 spikelets, glabrous or pubescent, large, heavy, bending over at maturity, two-rowed, almost always awned, and square or oblong in section depending upon the laxness of the spike and the number and size of the grains in each spikelet. The rachis is tough, non-brittle, smooth, but fringed along its edges, with white hairs and with white a tuft with 1–2-mm-long hairs at the base of the spikelets. The individual rachis internodes are 2.5–4.7-mm-long, flattened, narrow and wedge-shaped. The spikelets are 10–13-mm-long, with 4–7 florets, with the upper 2 or 3 being sterile. The glumes are broadly lanceolate or oblong-lanceolate, white, yellow, red, or dark-bluish, glabrous in some forms and pubescent in others. The glumes of the lateral spikelets are 8–11-mm-long, shorter or longer than the lemma, inflated unsymmetrical, and with 5–7 nerves running from the base to a point close to the apical tooth. The glumes of the terminal spikelet are ovate and more or less symmetrical. All glumes are keeled from apex to base, with an apical tooth 1–1.5-mm-long. In some forms, the apical tooth is short and blunt, and the lateral nerve in some forms terminates in a short secondary tooth. The lemmas are thin, fragile, pale, oval, inflated, without a keel and with 9–15 fine nerves, which converge at the tip into a terminal, firm, yellowish-white, red, or black, awn, 10–19-cm-long, and triangular in section. Several forms shed their awns when the grain is ripe. As a rule, only the two lower lemmas of the spikelets bear long awns, while those of the third and higher flowers are much shorter or altogether missing. The palea is membranous and shorter than the corresponding lemma. The caryopsis is free from lemma and palea, white, yellow, or red in color, large, broad, plump (6.7–8.37-mm-long, 3.26–4.43-mm-broad, and 3.23–4.1-mm thick), blunt or truncate at the apex, and with a high dorsal arch or hump behind the embryo. The embryo is small and the endosperm is generally opaque and starchy; in few forms it is flinty.
Ssp. turgidum contains many varieties, which mainly differ in glume and awn color, glume hairiness, awn presence or absence, and in spike branching. Genetic diversity of 313 accessions of ssp. turgidum, obtained from different countries in Europe, Asia, USA, and Australia, was assessed by analyzing morphological traits and high-molecular weight glutenin subunits (Carmona et al. 2010a, b). A high level of variability was observed; 20 allelic variants were observed, five in the Glu-A1 loci, two of which were new, and 15 alleles in the Glu-B1 loci, six of these being novel. Genetic diversity among accessions of different countries was considerable, whereas diversity observed within countries was relatively low. The data indicated a clear decrease of morphological variability, along with an asymmetric distribution of the alleles and seed storage protein patterns.
Up until 1950, ssp. turgidum was widely grown in China. However, later its cultivation areas have been gradually reduced and, currently, most turgidum landraces are only preserved in germplasm banks. C-banding analysis revealed more genetic variations in Chinese landraces of ssp. turgidum than in those of common wheat and in other tetraploid wheats (Dou and Chen 2003). Likewise, Li et al. (2006), using SSR markers, investigated the genetic diversity and genetic relationships among 48 accessions of T. turgidum, including 30 ssp. turgidum, 7 ssp. durum, 4 ssp. carthlicum, 3 ssp. paleocolchicum, 2 ssp. turanicum, and 2. ssp. polonicum. A total of 97 alleles were detected at 16 SSR loci. The genetic diversity among the ssp. turgidum accessions from Gansu, China, was higher than among those from Sichuan and Shanxi, China. Similarly, Wei et al. (2008), using EST-SSR markers and analysis of molecular variance (AMOVA), investigated 68 accessions of ssp. turgidum landraces, originating from four geographic areas in China. They noted that 92.5% of the total variations was attributed to genetic variations between accessions from the same area, whereas only 7.5% of the variations were among accessions from different areas.
Oliveira et al. (2012) used nuclear SSRs (nuSSRs), chloroplast SSRs (cpSSRs), insertion site-based polymorphisms (ISBPs) and functional markers in expressed genes to investigate genetic diversity and population structure in landraces of several subspecies of T. turgidum in the Mediterranean basin, including wild and domesticated emmer, ssp. turgidum and durum. Wild emmer was the most diverse of all subspecies (gene diversity of 0.833), followed by domesticated emmer (gene diversity of 0.708) and ssp. turgidum (gene diversity of 0.682), while ssp. durum from northwest African was the least diverse (gene diversity of 0.546).
Most naked tetraploid wheats are likely of relatively recent origin and deviate in only a few characteristics from ssp. durum, its closely-related subspecies (Mac Key 1966; Morris and Sears 1967). It differs from ssp. durum by its softer grain, its somewhat taller stature, and branched spikes, in several forms. Transitional forms between the two subspecies also exist. The time of origin of ssp. turgidum is unclear. Due to the difficulty of distinguishing grains of ssp. turgidum from those of ssp. durum and bread wheat, grains described as those of ssp. turgidum found in deposits of Neolithic and Bronze sites, should be considered with caution.
One of the first accurate descriptions of ssp. turgidum was given by botanists in the first half of the sixteenth century, when this taxon was grown in small areas in southern European countries. Because of its relatively high yield when grown under suitable conditions (Percival 1921), its popularity increased and during the 16th, 17th, and eighteenth centuries, it was also cultivated in England and Central Europe (Germany and northern France). During this period, ssp. turgidum was designated Rivet, Cone, or Pollard wheats. However, in the second half of the nineteenth century, its cultivation area was greatly reduced. Currently, ssp. turgidum is mainly grown in the countries bordering the Mediterranean, namely, Spain, Portugal, and Italy. Several, forms are grown, to a lesser degree, in Bulgaria, Greece, Turkey, northern Iraq, southern Iran, western Georgia, Azerbaijan, and in smaller amounts in Central Asia, and possibly also in Ethiopia and India. It is grown on small scales in Algeria, South Africa, Australia, China, Canada, USA, Chili, and Argentina.
The productive power of most varieties of ssp. turgidum is greater than that of any other subspecies of tetraploid wheat when growing conditions are suitable and climate allows a long growing period for the crop. Their high grain-yielding capacity is correlated with a long vegetative period, leading to an abundance of green-assimilating tissue. Moreover, the number of spikelets on each spike is usually greater among varieties of ssp. turgidum than among the varieties of bread wheat. Their tall straw is strong, the crop rarely lodges, and the stiff awned ears are not readily damaged by birds, deer, and other herbivores. ssp. turgidum contains some varieties that can be cultivated as winter wheat, but the majority of its varieties are cultivated as spring wheats. It grows well on light (sandy), medium (loamy) and heavy (clay) soils and prefers well-drained soil. ssp. turgidum also has the capacity to grow in poor soils, shows a strong weed competitiveness and a good resistance to diseases. Yet, compared to modern cultivars of durum and bread wheat, the varieties of ssp. turgidum occupy the fields during a relatively long period, have a late heading and a modest yield (from 2 to 2.5 tons per hectare).
Ssp. turgidum is less suitable for bread making because of its poor physical quality (elasticity and extensibility) and reduced gluten content. Loaves of bread made from ssp. turgidum flour are more or less dense and non-porous, and of small volume when compared with loaves made from the same weight of dough prepared from the “strong” flour of certain varieties of T. aestivum. Most ssp. turgidum varieties have a soft, opaque, starchy endosperm, which yields “weak” flour, suited to the requirements of the biscuit, porridge, and pasta industries.
Percival (1921) assumed that ssp. turgidum has the characteristics of a hybrid race. According to him, the long growing period, number of culm leaves, velvety leaf surface, plant height, surface, and pithy interior of its straw, spike density, as well as the frequent occurrence of branched spikes, indicate a close relationship between ssp. turgidum and the tall European forms of ssp. dicoccon. Several forms suggest affinity with ssp. durum, while others appear to be allied with T. aestivum. Its affinity with the European emmer can be traced by the morphological characteristics and habit. The two taxa agree in the characteristic pubescence of their young leaves. Both have tall, solid, or nearly solid, culms, and spikes with spikelets very regularly arranged along the rachis. They tiller very little and have a similar late-ripening period. Moreover, the tendency to produce branched spikes is strongly evident in these two taxa and rare in others. The square spike of ssp. turgidum, its many-flowered spikelets, and plump, blunt-ended grains are characteristics derived from the dense-spiked ssp. compactum or ssp. aestivum parent, while the dorsal hump of the grain is derived from the emmer parent.
Despite this, Oliveira et al. (2012), using several types of molecular markers, found that while wild and domesticated emmer is genetically distinct from ssp. durum and turgidum, the latter two share a common gene pool and are almost genetically indistinguishable. Differences in key genes between turgidum and durum have not been identified or quantified and it is debatable if the differences in phenotype are sufficient to classify them as different taxa. Consequently, Oliveira et al. (2012) classified turgidum and durum as varieties of the same subspecies, each with distinct morphological characteristics. Likewise, Morris and Sears (1967) assumed that the turgidum group differs little from the durum group, and that there exist transitional forms between the two types, as reported by Watkins (1940). However, following van Slageren (1994), who thought that the morphological differences between the two justify their separation, we prefer to maintain ssp. turgidum and ssp. durum as separate subspecies of T. turgidum.
Considering the strong genetic similarity between turgidum and durum, demonstrated in all the marker systems used, Oliveira et al. (2012) suggested that the two subspecies originated from a common domesticated ancestor. Their distinct adaptation to specific conditions as they were introduced into Europe could have yielded landrace varieties with distinct morphological characteristics, such as the distinct head form in turgidum or its higher tolerance to cold and humidity in comparison with ssp. durum. Yet, Oliveira et al. (2012) thought that these selective pressures were apparently not sufficiently strong to create a distinct genetic pool between the two. They proposed, based on the considerable difference between the hulled emmer and the naked turgidum and durum, that naked wheats evolved from a small number of hulled tetraploid genotypes, and have been in relative reproductive isolation since their spread into Europe and North Africa during the Neolithic Age. Nevertheless, the data of Oliveira et al. (2012) do not negate the possibility that ssp. turgidum developed from ssp. durum under different cultivation conditions.
10.3.2.8 Ssp. polonicum (L) Thell. (Polish Wheat)
T. turgidum ssp. polonicum (L) Thell., known as Polish wheat, (Syn.: T. polonicum L.; T. levissimum Haller; T. maximum Vill.; T. glaucum Moench: T, turgidum grex polonicum Bowden; T. turgidum ssp. turgidum convar. polonicum Mk; Gigachilon polonicum Seidl.; Deina polonica Alef.) is a subspecies that was discovered by the scientific world last of all the subspecies of T. turgidum. Evidence of its existence was not obtained before the first half of the seventeenth century (Percival 1921). Its name, T. polonicum, was given to this taxon since it was first described after a specimen obtained from the Botanic Garden at Leyden, Poland, but the origin of the name and the early connection of the wheat with Poland is obscure. There is no evidence that it was grown in Poland before 1870 (Percival 1921). In fact, it would be more appropriate to call it Galician wheat. When giving the name T. polonicum, Linnaeus (1753) confused Galicia (a region of Spain) with Galicia (a region of Poland and Ukraine).
Ssp. polonicum is a predominantly autogamous plant. It is one of the tallest wheats, with culms usually reaching a height of 100–160 cm. The upper internode is generally solid, while the lower ones are hollow. The plants tiller very little (three or four tillers per plant), and the shoots are erect. The culm leaves are glabrous or pubescent, bluish-green in color, and with smooth surfaces, like those of ssp. durum. The upper culm leaves are 2-cm-broad, with small auricles. The spikes are very long, 10–16-cm-long (excluding awns), narrow, very lax, almost square in cross-section, with a tough, non-brittle rachis, two-rowed, and awned. It bears 19–23 spikelets, with three or four of the lower ones being rudimentary. In some forms, the spike is compact, short, 7–9-cm-long, and oblong in cross-section. The rachis is flat, narrow and wedge-shaped, each about 1.5-mm-wide at the base and 3-mm-wide at the top, fringed with hairs on the sides, and with a frontal tuft of hairs 2–2.5-mm-long at the base of each spikelet. The spikelets are large, flat, 3–4-cm-long, and consisting of four or five flowers, of which two (or three) produce grain, while the others are sterile. The glumes are delicate, with a glaucous color, glabrous or pubescent, long, lanceolate and narrow, 2–4-cm-long, extending beyond the rest of the spikelet, keeled from the apex to the base, and with a short apical tooth; the second tooth is very short or absent. The lemmas of the two lowest flowers are 2–3-cm-long, the upper ones being much shorter, boat-shaped, rounded on the back and with 15–17 nerves. Their membranous edges are fringed with short hairs, bear a coarse awn, which is 7–12-cm-long, and white or black. The awns of the upper lemmas are either very short, not more than about 5-mm-long, or absent. The palea are only 1.2–1.5-cm-long, lanceolate, with a slightly divided tip, and possess 4 nerves. The grains, are free-threshing, long and narrow, 11–12-mm-long and 4-mm-broad, i.e., the largest of all wheats, narrow, and yellowish-white or pale red, with a flinty endosperm (Fig. 10.3c).
The typical form of ssp. polonicum is strikingly different from all other subspecies of T. turgidum, in that it possesses large ears with long, narrow, papery, somewhat loose glumes of a glaucous color, which extend beyond the rest of the spikelet. A large number of ssp. polonicum varieties have been described. The majority are not currently cultivated and do not appear to have been grown, except for in Botanic Gardens. Percival (1921) recognized only three varieties that are currently found in cultivated fields, namely, levissimum Körn. (white glumes, glabrous, long awn, quadrate ear, white grain), villosum Körn. (white glumes, pubescent, long awns, quadrate ear), and Martinari Körn. (white glumes, pubescent, long awns, flattened ears, white grain).
According to Percival (1921) ssp. polonicum is a mutation of ssp. durum. He considered the only point of difference, namely the excessively long, thin glumes, as a hereditary teratological variation. Percival reported on several specimens of ssp. durum from India with elongated glumes, suggestive of incipient polonicum. Körnicke (in Percival 1921) claimed that he obtained from Upper Egypt a specimen that looked like a transition type between durum and polonicum.
Ssp. polonicum is a rather minor, primitive, durum-like, spring wheat subspecies. It is sporadically Kwiatek grown, not prolific, and of marginal importance in the contemporary grain market (Kwiatek et al. 2016). ssp. polonicum requires hot climate and well-drained soils for satisfactory growth. It is cultivated on small scales in several countries bordering the Mediterranean (Algeria, Spain, Italy, and Turkey), in eastern and southern Europe (European Russia, and Ukraine), in Transcaucasia (Armenia, Azerbaijan, Georgia), in central Asia (Kazakhstan, Kyrgyzstan, and Turkmenistan) and in Ethiopia. It is also grown to a limited degree in the USA and Argentina. In several countries, it is grown principally for plant breeding, while in others, it is grown for its edible seed, and in the Mediterranean, also for cereals, and macaroni but not for bread. The straw is used for fuel, thatching, and as a mulch in the garden. Wiwart et al. (2013) compared morphometric parameters such as plant height, spike length, spike density, grain weight per spike and single kernel weight, and some chemical properties of the grain, i.e., protein, ash, fat, crude fiber, minerals and mycotoxins content, in nine lines of ssp. polonicum with Kamut wheat (a variety of T. turgidum ssp. turnicum) and two common wheat cultivars. The average height of the polonicum lines was 109.8 cm, considerably greater than that of common wheat (88.8 cm), and Kamut wheat (89.3 cm). The average length and density of polonicum spikes did not differ significantly from those of bread wheat, yet the differences between lines were considerable. The shortest spikes were observed in Kamut (5.98 cm), and the most-dense spikes were reported in the polonicum P-4 line (22.7 spikelets per 10 cm of rachis). The highest grain weight per spike was reported in one cultivar of bread wheat (2.17 g), in Kamut (1.90 g), and in the polonicum lines (1.35–1.78 g) and exceeded those of the high-yielding second cultivar of bread wheat (1.31 g). Like Oliver et al. (2008), Wiwart et al. (2013) also found that lines of ssp. polonicum possess moderate to high levels of resistance against Fusarium head blight.
Concerning the chemical properties of the grain, Wiwart et al. (2013) reported that the grains of ssp. polonicum were characterized by a significantly higher average protein (16.61%) and ash (2.14%) content than the grains of bread wheat (13.87% and 1.73%, respectively). The common wheat cultivars had considerably higher concentrations of fat and dietary fiber than polonicum and Kamut. In comparison with bread wheat, the grains of the examined polonicum lines had significantly more phosphorous, sulfur, magnesium, copper, calcium, zinc, iron and molybdenum and contained significantly less aluminum and strontium. Similarly, Bieńkowska et al. (2019) found that ssp. polonicum grain is characterized by a significantly high content of phosphorus (4.55 g/kg), sulfur (1.82 g/kg), magnesium (1.42 g/kg), zinc (49.5 mg/kg), iron (39.1 mg/kg) and boron (0.56 mg/kg). Hence, the nutrient profile of most ssp. polonicum lines differs completely from that of bread and durum wheat. More specifically, seven lines of ssp. polonicum had the highest content of copper, iron and zinc, and the lowest concentrations of strontium, aluminum and barium, which are undesirable in food products, providing a particularly beneficial micronutrient profile (Bieńkowska et al. 2019). These data show that ssp. polonicum may constitute an important genetic resource for improving the nutritive value and resistance to Fusarium head blight of durum and bread wheat (Wiwart et al. 2013; Bieńkowska et al. 2019).
Biffen (1905) was the first to study the genetic control of glume length by making reciprocal crosses between ssp. polonicum (long glumes) and ssp. turgidum (short glumes). In F2, he observed a long:intermediate:short glumes ratio of 1:2:1, showing that only one gene determines this trait and that the long-glume allele is not dominant over the short glume allele. These observations were corroborated by data collected by Engledow (1920), crossing ssp. polonicum x ssp. durum var. Kubanka, and also showed that glume length bears some definite relationship with grain length, and thus, is of economic significance.
In accord with the above, Matsumura (1950) observed in F2 of crosses involving ssp. polonicum, dicoccoides, and carthlicum (formerly T. persicum), that the long glume trait is controlled by one allele (P), which is dominant on the short glume allele (p). He reported that the P locus is linked to the red coleoptile locus (Rc), with a cross-over value of 20.3%. Rc genes are known to be located on the homoeologous group 7 chromosomes (McIntosh et al. 1998). In agreement with these results, Watanabe et al. (1996), Watanabe (1999), used telosomic mapping to locate P, designated by them as P1, on the long arm of chromosome 7A, 9.8 cM from the centromere. Moreover, Watanabe et al. (1996) noted a link between the P1 gene and the chlorina gene CDd6 (cn-A1d; Klindworth et al. 1995, 1997), further suggesting that P1 is located on chromosome 7A. Furthermore, crosses between a near isogenic line of ssp. durum cv. LD222 carrying P1, with the durum cultivar Langdon (LDN) and the LDN D genome substitution lines, LDN 7D(7A) and LDN 7D(7B), corroborated the location of P1 on 7A. Segregation for the long glume trait in the F2 of LDN/P-LD222 and LDN 7D(7B)/P-LD222 was normal (3:1) and indicated that the P1 gene was not on chromosome 7B. The location of P1 on 7AL was confirmed by Koval (1999), Efremova et al. (2001).
The Chinese wheat landrace, Xinjiang rice wheat (T. aestivum ssp. aestivum var. petropavlovskyi (=T. petropavlovskyi Udacz. et Migusch.), was found in 1948, in the agricultural areas of the west part of Talimu basin, Xinjiang, China. This taxon is characterized by long glumes. Watanabe and Imamura (2002) introduced the gene for long glume from var. petropavlovskyi into the LD222 cultivar of ssp. durum and found that it is controlled by a gene located on chromosome 7A. The gene was located approximately 12.45 cM from the centromere on the long arm of 7A. Consequently, Watanabe and Imamura (2002) considered the gene for long glume from var. petropavlovskyi an allele of the P1 locus and designated it P1a. It was suggested that var. petropavlovskyi originated from either a natural hybrid between T. aestivum and ssp. polonicum or a natural point mutation of T. aestivum (Chen et al. 1985; Watanabe and Imamura 2002).
A second gene for elongated glumes (P2) has been identified in var. ispahanicum (Watanabe 1999). The Ispahan emmer wheat, ssp. dicoccon var. ispahanicum, (= T. ispahanicum Heslot), is a hulled taxon that was discovered in Ispahan, Iran, in 1957, by the French expedition of Vinnot-Bourgen, and was considered by Miller (1987) to be a variety of ssp. dicoccon. This wheat has a long glume and a more-slender spike than ssp. polonicum. Watanabe (1999), using a near-isogenic line that carries the P2 gene of var. ispahanicum, located this gene on chromosome arm 7BL, approximately 36.5 cM from the cn-B1 locus, which controls the chlorina trait (Klindworth et al. 1995, 1997) and approximately 40 cM from the centromere. The location of P2 approximately 29.6 cM from the purple color gene (Pc) (McIntosh et al. 1998), provided additional evidence that the order of loci was cn-B1, and that var. ispahanicum originated following a mutation of a gene affecting glume length on chromosome 7B of ssp. dicoccon.
The most pronounced elongated glumes are present in ssp. polonicum, reaching a length of up to 40 mm, compared to 5–8 mm in normal wheats (Dorofeev et al. 1980). Less pronounced glume elongation is present in the tetraploid subspecies of T. turgidum, turanicum and durum convar. falcatum and in the hexaploid taxon T. aestivum ssp. aestivum var, petropavlovskyi. Wang et al. (2002) mapped the respective genes that determine glume length in these taxa, using wheat microsatellite markers. In ssp. polonicum and hexaploid var. petropavlovskyi, loci conferring long glume were mapped near the centromere on the long arm of chromosome 7A. These two loci were designated by Wang et al. (2002), P-Apol1 (currently P1) and P-Apet1 (currently P1a), respectively. It was shown that both are probably homoeoallelic to each other and to the P2 gene of var. ispahanicum on the long arm of chromosome 7B. The loci determining elongated glumes in ssp. turanicum and ssp. durum conv. falcatum are not homoeologous to the P loci in the centromeric region of group 7 chromosomes (Wang et al. 2002).
Pan et al. (2007), using SDS-PAGE, assessed genetic diversity in ssp. polonicum by analyzing gliadins and high molecular weight glutenin subunits in 72 accessions from 23 countries. High genetic variability was observed in both types of storage proteins. Diversity indices (H) at Glu-B1 loci (0.659) were much higher than in Glu-A1 loci (0.271). Variation in these proteins was associated with their geographic origins.
Watanabe (1994) studying near-isogenic lines of ssp. durum cv. LD222 carrying the P1 gene, derived from crosses involving ssp. polonicum, reported that the long glume trait, controlled by the P1 gene, which resulted in a large photosynthetic area, tended to increase the main culm dominance, and plant height, resulting in declined grain yield and harvest index.
Biffen (1905), Engledow (1920), crossing ssp. polonicum x ssp. turgidum and durum, showed that glume length has some definite relation to grain length, and thus, appeared to be of economic significance. In this respect, Millet and Pinthus (1984) assumed that long glumes may allow grain growth by preventing the effect of penetrating light to the flower cavity. They found that removal of organs that exposed the developing wheat grain to increased light intensity, resulted in a reduction in grain size. The restriction in grain growth was already apparent two weeks after anthesis. Covering the treated spikes with opaque bags restored grain growth.
Like all other subspecies of T. turgidum, ssp. polonicum is also a tetraploid taxon, with 2n = 4x = 28 chromosomes and genome BBAA. Nakajima (1955) observed 0–3 bivalents and 15–21 univalents in meiotic first metaphase of F1 hybrids from the cross ssp. polonicum x Secale africanum. He concluded that the bivalents resulted from autosyndesis between the chromosomes of the AB subgenomes of ssp. polonicum and not from pairing between the chromosomes of the two taxa.
10.3.2.9 Ssp. turanicum (Jakubz.) Löve and Löve (Khorassan Wheat)
T. turgidum ssp. turanicum (Jakubz.) Löve & Löve, known as Khorassan wheat or Oriental wheat [Syn.: T. turanicum Jakubz.; T. orientale Percival; T. percivalii Hubb. ex Schiem.; T. percivalanum Parodi; T. turgidum grex turanicum (Jakubz.) Bowden; T. turgidum ssp. turgidum conva. turanicum (Jakubz.) MK; T. georgicum convar. turanicum (Jakubz.) Mandy; T. durum ssp. turanicum L. B. Cai; Gigachilon polonicum ssp. turanicum (Jakubz,) Á. Löve] is a predominantly autogamous, 66–110-cm-tall plant, with an upper internode that is either solid or hollow with thick walls. The young shoots are erect, with very narrow pubescent leaves. The plants tiller very little and the straw is thin. The spikes are very long, narrow, very lax, almost square in cross-section, with a tough non-brittle rachis, 10–11.5-cm-long (excluding awns), two-rowed, and awned. The rachis sides are fringed with white hairs, and there is a conspicuous frontal tuft below each spikelet. The rachis internodes are narrow and wedge-shaped, each about 1.5-mm-wide at the base and 3-mm-wide at the top. The spikelets (15–20 per spike) are 15–17-mm-long, and with 2–3 grains. The glumes are delicate, white, pubescent, large, 12–15 mm-long, keeled from the apex to the base, with a short apical tooth, and prominent lateral nerve. The lemma bears a coarse awn, which scabrid to the base, 14–16-cm-long, and white or black. The grains are free-threshing, very long (10.5–12 mm), narrow, twice the size of modern wheat kernels, with a thousand-kernel weight up to 60 g, white to amber in color and flinty, with a short brush, resembling those of ssp. polonicum. This wheat grown in spring, is early in maturity and resistant to several fungal diseases.
ssp. turanicum, Khorasan wheat (Khorasan refers to a region in northeast of Iran, Afghanistan and central Asia, where this subspecies was cultivated) contains two varieties, differing only in the color of their awns (white or black). It is a small, ancient race of the free-threshing subspecies of T. turgidum. Khorasan wheat was probably continuously cultivated on small scales and for personal use, in Near East, Central Asia, and northern Africa (Vavilov 1951). In these areas, it was grown mostly as an admixture in durum wheat fields, seldom in pure sowing. Currently, Khorasan wheat is grown on a small scale in Europe and the Middle East, mainly for special bread, and in central Asia, mainly as food for livestock (camels). Approximately 6500 ha of Khorasan wheat, mostly cultivar Kamut, were cultivated worldwide in 2006, mainly in north-central Montana, USA, and southern Saskatchewan and southeast Alberta, Canada (Brester et al. 2009).
The origin of the cultivar Kamut is accompanied by a mystical story, namely, a USA airman claimed to have taken a handful of grains from a stone box in a tomb near Dashare, Egypt (Quinn 1999). Wheat grains usually lose their germination ability few years after harvest, and therefore, it is unfeasible that seeds several thousands of years old will germinate. It is more likely that someone put fresh seeds in the tomb or that making of such a story furnishes some mysterious sense to the origin of Kamut. In any case, Kamut (an ancient Egyptian word for wheat) was developed in Montana, USA, and appeared on the market about 35 years ago. In 1990, the US Department of Agriculture recognized the grain as a protected cultivar, which was given the official name ‘QK-77’. Kamut yield is less than that of standard cultivars of spring wheats (Stallknecht et al. 1996).
Cultivar Kamut contains some nutritional, health, and taste advantages over modern wheat varieties, but lacks some of their agronomic advantages (Brester et al. 2009). The average yield of cv. Kamut is very low (1.1–1.3 t/ha), approximately 1/3 that of durum wheat. Its grain is twice the size of that of modern-day wheat and is known for its rich nutty flavor. Grains of Khorasan wheat contain a high protein content (15%), several B vitamins and minerals, such as iron, zinc, magnesium, manganese, phosphorus and potassium, and soluble and insoluble fibers (Brester et al. 2009; Abdel-Haleen et al. 2012). Kamut grains can be either directly consumed or milled into flour, which can be found in breads, bread mixes, breakfast cereals, cookies, waffles, pancakes, bulgur, baked goods, pastas, drinks, beer and snacks (Brester et al. 2009). Sofi et al. (2013) examined the effect of a Kamut diet on cardiovascular risk parameters by conducting a randomized, single-blinded cross-over trial with two intervention phases on 22 healthy subjects (14 females; 8 males). Their results suggested that a diet with Kamut products could be effective in reducing metabolic risk factors, markers of both oxidative stress and inflammatory status.
ssp. turanicum is a tetraploid taxon, a free-threshing subspecies of T. turgidum. It is considered to be an ancient taxon of this species. With respect to ear form and grain length, it closely resembles some of the varieties of ssp. polonicum (Percival 1921). But, although it is long-grained, ssp. turanicum lacks the long glumes of ssp. polonicum. Khlestkina et al. (2006), studying the taxonomic classification of Kamut and ssp. turanicum, presented genetic evidence from DNA fingerprinting that ssp. turanicum is perhaps a natural hybrid between ssp. durum and ssp. polonicum. They investigated the taxonomic placement of Kamut using micro-satellite genotyping. In total, 89 accessions of 13 tetraploid wheat species, including ssp. turanicum and Kamut, were genotyped. Kamut clustered together with three accessions of, ssp. polonicum and three of ssp. durum, indicating the genetic proximity of ssp. turanicum (including Kamut) to ssp. durum and ssp. polonicum.
10.3.2.10 Ssp. carthlicum (Nevski in Kom.) Á. Löve and D. Löve (Persian Wheat)
T. turgidum ssp. carthlicum (Nevski) Á. Löve and D. Löve, known as dika wheat, Persian wheat, Persian black wheat, [Syn.: T. carthlicum Nevski; T. persicum Vavilov ex Zhuk.; T. dicoccum var. persicum Perciv.; T. persicum (Boiss.) Aitch. & Hemsl.; T. ibericum Menabde; T. paradoxum Parodi; T. carthlicum grex carthlicum (Nevski) Bowden; T. turgidum ssp. carthlicum (Nevski) MK; T. turgidum convar. carthlicum (Nevski) Morris & Sears: T. georgicum convar. carthlicum (Nevski) Mandy: Gigachilon polonicum ssp. carthlicum (Nevski) Á. Löve] is an autogamous plant. Its young shoots are erect and young leaves pubescent, its straw is thin, of medium height (104 cm), solid or hollow with thick walls and with hairy nodes. Its rachis is narrow, spike lax, narrow, 9-cm-long, square in cross-section, and with 19–20 spikelets, each with 2–3 red grains. Glumes bear a single awn, 3–4 cm in length. The lemma is white at the bottom and dark brown at the top, with an 8–11-cm-long awn. Grains are flinty and reddish, the apex is blunt, 6.5-mm-long, 3-mm-broad, and 2.9-mm-thick. The plant flowers very late and grows in the spring (Fig. 10.3d).
Ssp. carthlicum was found in Transcaucasia and was first referred to as a separate species, T. persicum Vav, by Vavilov (1918), who believed it originated in Iran. This peculiar species morphologically resembles hexaploid wheat, T. aestivum ssp. aestivum, but is biologically and cytologically related to tetraploid wheats (Jakubziner 1959). Later, it was found that this tetraploid taxon was not exclusive to Iran, as it was discovered by Zhukovsky (1923) in Georgia, and by other in Armenia, Azerbaijan, Dagestan, and Turkey (Jakubziner 1959).
The epithet was renamed by Nevski as Triticum carthlicum Nevski (Nevski 1934), with original publication in Komarov VL (ed.), Fl. URSS 2: 688 (1934), replacing T. persicum Vavilov ex Zhuk., which is illegitimate because the name T. persicum (Boiss.) Aitch. & Hemsl. was awarded to another taxon now included in the genus Aegilops, i.e., Ae. persicum Boiss. (Now recognized as a variety of Ae. triuncialis namely, var. persica (Boiss.) Eig). More recent names given to this taxon such as T. ibericum Men. (1940) and T. paradoxum Parodi (1940), ought to be rejected (Jakubziner 1959).
ssp. carthlicum is an endemic domesticated wheat from the Caucasus-Trans-Caucasus region, grown in pure stands or, more commonly, in mixture with domesticated emmer, durum, or bread wheat, confined to mountainous regions in Georgia, Armenia, Azerbaijan, Dagestan, northern Ossetia, northwestern Iran, northern Iraq and northeastern Turkey (Dorofeev 1968; Hanelt 2001).
The study of Dekaprelevich (1925) showed that this subspecies, which was previously considered more or less ecologically homogenous, is actually divided into two different ecotypes: the mountainous-forest ecotype (forma caucasionis dika) and the mountainous-steppe ecotype (forma dzhavachetica dika). The former is distributed in elevations of 900–1400 m above sea level and is represented by a late-ripening, moisture-loving, black-spiked variety. The latter is adapted to a higher elevation of 1400–2100 m above sea level and is chiefly represented by early-ripening, and white- or red-spiked varieties. Dorofeev (1968) described two varieties of ssp. carthlicum in Armenia, vars. Stramineum and rubiginosum.
Variation in spike color of ssp. carthlicum, namely, black, red and white, was found in Georgia and Daghestan, but, in Armenia, only types with white or red ears occur (Dorofeev 1968). The various forms have a spring habit, and are tolerant to low temperatures (Dorofeev 1968).
A sample of 74 accessions of ssp. carthlicum were scored for 46 characteristics using numerical analysis (Vieira 1985). The study enabled the recognition of three morphological distinguishable groups in this subspecies. The data provide supportive evidence for the recognition of var. rubiginosum Zhuk. and var. fuliginosum Zhuk. as distinct taxa. However, recognition of var. stramineum Zhuk. based on spike color could not be achieved. Variation patterns in ssp. carthlicum suggested that geographical distance and taxonomic distance between populations are associated. SDS-PAGE analysis of the HMW glutenin subunits in the 74 carthlicum accessions provided identical HMW glutenin subunits profile, indicating a monophyletic origin of ssp. carthlicum. The lack of variability also suggests its recent origin. This interpretation seems to favor the hypothesis that ssp. carthlicum is a young form derived from a cross between a free-threshing and a tetraploid wheat.
Interspecific relationship studies involving the subspecies of T. turgidum were conducted using iso-enzymatic characters located in dry mature seeds (Asins and Carbonell 1986b). Studies of peroxidases in the embryo and alkaline phosphatase in the endosperm showed no variation in these two enzymes in ssp. carthlicum which, in turn, showed no new enzymatic pattern for that had not been observed in wild emmer, ssp. dicoccoides. Hence, from all the subspecies of T. turgidum, the closest relationship was found between ssp. carthlicum and ssp. dicoccoides, suggesting the origin of the former from the latter (Asins and Carbonell 1986b).
ssp. carthlicum is very morphologically distinct from the other free-threshing subspecies of T. turgidum, namely, durum, turgidum, turanicum, and polonicum. Watkins (1928, 1940) reported that while ssp. carthlicum is characterized by non-keeled round glumes, and possesses the recessive k allele, all the other tetraploid wheats had keeled glumes, and the dominant K allele. Following Watkins (1928, 1940), many wheat geneticists, e. g., Mac Key (1954a, 1966, 1975; Morris and Sears 1967) assumed that only in this tetraploid subspecies is the free-threshing trait determined by the Q factor, as in hexaploid wheats, while in other tetraploids, this trait is determined by another genetic system. Mac Key (1954a), using irradiation experiments, found that the free-threshing, non-keeled glumes and rachis toughness traits of ssp. carthlicum are, in fact, controlled by one factor, i.e., the same as the square-head gene Q, while all other free-threshing tetraploids possess the q allele (Mac Key 1954a, 1966, 1975). These traits in the other tetraploid wheats were assumed to be controlled by a different gene system than Q, i.e., a polygenic system (Mac Key 1966, 1975). Another striking feature of ssp. carthlicum is its awned glumes, with all the spikelets displaying four awns, one on each of the two glumes and one on each of the lemmas of the two lower flowers. As it looks very much like hexaploid T. aestivum ssp. aestivum, ssp. carthlicum was classified at first as a hexaploid species, T. persicum Vav. (Vavilov 1918). Only later, on account of its chromosome number (2n = 28), and the high sterility of its F1 hybrid with T. aestivum, ssp. carthlicum was recognized to be a tetraploid taxon (Schiemann 1948). The very restricted distribution area of ssp. carthlicum to the mountainous regions of Caucasia and Trans-Caucasia and surroundings countries (Zhukovsky 1923; Vavilov and Jakushkina 1925) align with its recent origin, presumably by hybridization between an unknown tetraploid and a hexaploid of the aestivum group (Mac Key 1954a, 1966, 1975; Morris and Sears 1967). Alternatively, it may be an offspring of a mutation in an emmer–like ancestor (Hanelt 2001). Mac Key (1966) assumed that the Q gene was transferred to hexaploid wheat from carthlicum, with the latter being involved in the formation of hexaploids via hybridization with Ae. tauschii, the donor of the D subgenome. Alternatively, spelt-type hexaploid wheat was first formed and then crossed with carthlicum, producing the free-threshing hexaploids. On the other hand, if Q evolved on the hexaploid level, carthlicum must be considered a much younger type, originating from a cross of Q-hexaploid x q-emmer (Vavilov 1926).
Free-threshing tetraploid types evolved from the dicoccoides-dicoccum group but through two different genic systems (Mac Key 1966 1975). Carthlicum (cf. Jakubziner 1959) is the only free-threshing tetraploid endemic to Transcaucasia. It resembles the 6x ssp. aestivum wheat, with which it consistently grows with and with which it shares Q. This gene, located on chromosome 5A (Sears 1954, 1959), appears to be lethal at the diploid level (Mac Key 1966). If Q arose already at the tetraploid level, carthlicum may have been the key for the development of the naked hexaploid wheats. However, it seems more likely that carthlicum arose through 6x aestivum x 4x dicoccon than formation of 6x aestivum through 4x carthlicum x 2x Ae. tauschii or (4x dicoccum x Ae. tauschii) x carthlicum. All three possibilities have been proven to yield 6x T. aestivum (Mac Key 1966).
Kuckuck (1979) found in the border region of Iran, Turkey and Transcaucasia, accessions of free-threshing hexaploid wheat exhibiting the subsp. carthlicum-like morphology, i.e., four awns on each spikelet; however, the glume awns of ssp. carthlicum are longer than those of the hexaploid taxon. Since chromosome number was 2n = 42, he named these accessions T. aestivum subsp. carthlicoides. This taxon is not mentioned among the subspecies of T. aestivum in recent taxonomical treatments of the genus Triticum, e, g, by Bowden (1959), Löve (1984), Dorofeev et al. (1980), Mac key (1988, 2005), van Slageren 1994. Hence, it will be referred to from here on as var. carthlicoides. Kuckuck (1979) proposed that ssp. carthlicum originated from a spontaneous hybridization between var. carthlicoides and an accession of domesticated emmer. The 6x var. carthlicoides should be considered as the original and older genotype from which genes for the particular morphology of the spike were transferred together with the Q-factor, to ssp. carthlicum. The prolongation of the glume awns in ssp. carthlicum, relative to that of var. carthlicoides, might be due to the lack of the D subgenome (Kuckuck 1979).
Kerber and Bendelow (1977), based on similarity in several milling and baking properties, and Bushuk and Kerber (1978), based on similarity in the gliadin electrophoretic mobility, concluded that ssp. carthlicum cannot be rejected as a possible source of the BBAA component of bread wheat, nor did the evidence exclude the hypothesis that this tetraploid is merely a segregate from a hexaploid wheat x tetraploid wheat hybrid.
Haque et al. (2011) found that the tetra-aristatus recessive allele, t, controlling the glume awns in ssp. carthlicum, is located on chromosome arm 5AL, and is among the b1 genes that determine awn development on the lemma. This conclusion was reached because the semi-dwarf Rht12 gene is linked to the b1 gene and the t locus is approximately 11 cM units from Rht12. Gandilyan (1972) pointed out the significance of the t gene for wheat domestication along with the Q gene, because the four-awned-hexaploid accessions were more easily threshed than other genotypes. Thus, a supposed spontaneous mutation at the T locus in T. aestivum (TTQQ) led to the formation of var. carthlicoides (ttQQ), which then hybridized with the hulled tetraploid ssp. dicoccon (TTqq); subsequent recombination and fixation produced ssp. carthlicum (ttQQ). The phenotype ‘‘tetra-aristatus’’ has not been found in tetraploid wheat species other than ssp. carthlicum.
Takumi and Morimoto (2015) supported Kuckuck’s (1979) idea that ssp. carthlicum evolved through inter-ploidy hybridization between a tetraploid form and hexaploid var. carthlicoides. They provided evidence for the origin of ssp. carthlicum based on the discovery of a new allele for the 5th-to-6th exon region of the Wknox1b KNOTTED1-type homeobox gene in the common wheat var. carthlicoides. In this Wknox1b region, var. carthlicoides contains an inverted duplication mutation in the 3′ flanking region of a 157-bp MITE insertion site. This structural mutation resulted in the suppression of Wknox1b expression in var. carthlicoides, but no structural mutation was observed in the same region of ssp. carthlicum. In addition, the ssp. carthlicum Wknox1b 5th-to-6th exon region exhibited the same sequence as that of the wild emmer wheat subsp. dicoccoides. These observations support the suggestion that ssp. carthlicum originated from inter-ploidy hybridization between wild emmer and var. carthlicoides.
However, Muramatsu (1978, 1979, 1985, 1986) found out that all the free-threshing subspecies of T. turgidum possess the Q factor. By substituting chromosome 5A of the tetraploids for 5A of hexaploid ssp. aestivum cv. Chinese Spring (that carries the Q factor), he found out that not only does ssp. carthlicum have the Q factor, but also all other free-threshing tetraploids. Even ssp. dicoccon var. liguliforme, a hulled subspecies with a compact spike, with a brittle rachis and keeled glumes, has the Q factor, while other hulled cultivars of ssp. dicoccon, farrum, Large White, and Vernal, possess the q allele. Muramatsu (1986) concluded that there is wide phenotypic variation of characteristics in different QQ lines, and suggested that the range of variation of these characteristics is very narrow in the absence of Q, but when Q is present, they express an obvious phenotype. The discovery that all free-threshing tetraploids carry the Q factor may indicate that ssp. carthlicum could originate from an hybridization between free-threshing tetraploid with wild or domesticated emmer.
Nevertheless, crucial questions concerning this conclusion have been raised, and stand in the way of a full understanding of the tetraploid wheat phenotype. That the expression of the Q factor may be modified by the genetic background, seemed to decisively clear up the difficulty in explaining the relation between spike morphology and wheat evolution. So, if the effect is only due to the genetic background, and if the genes making up this background are minor in effect, then why are there not many transitional types between brittle and tough rachis in qq KK tetraploids? Or, is there a major gene with such a strong effect that it is equivalent to Q? Such a gene would have been highly important, but it has not been discovered. Besides, there are some varieties of tetraploid wheat that have square-headed spikes. Because squareheadedness is one of the pleiotropic effects of Q, it is unlikely in a plant with genotype qq. Analysis of one such typical variety of ssp. polonicum, namely, var. vestitum, showed that, despite having keeled glumes, it has the aestivum gene Q (Muramatsu 1978). A preliminary result similar to this was obtained even with ssp. dicoccon var. liguliforme (Muramatsu 1979).
Because the rest of ssp. dicoccon differs from var. liguliforme and ssp. carthlicum in being speltoid, its chromosome 5A is presumed to carry the spelta gene q, and, therefore, this 5A should affect speltoidy in ssp. aestivum cv. Chinese Spring background (Mac Key 1954a; Muramatsu 1963). This has been confirmed with two series of aneuploid progeny involving ssp. dicoccon cv. Large White emmer, and cv. Vernal-squarrosa amphiploid (Muramatsu 1985).
The round glume of ssp. carthlicum is ascribed to lack of the proper genotype to develop strong keels. However, it is also assumed that carthlicum does not completely lack such genes because its phenotype resembles that of the hexaploid cultivars with round glumes, in which removal of Q led to keeled glumes (Muramatsu 1979, 1985, 1986).
McFadden and Sears (1946) mentioned that addition of the D subgenome to a tetraploid wheat from Ae. tauschii tends to increase the size of the grains. This is especially noticeable when the small-grained ssp. carthlicum is the tetraploid involved. It has also been observed that free-threshing hexaploid segregates from crosses between ssp. carthlicum and 6x ssp. spelta invariably have larger seeds than the free-threshing tetraploid parent.
The grains of ssp. carthlicum have a high protein content, but a low baking quality (Hanelt 2001). ssp. carthlicum is mainly used as a cereal. The seed is low in gluten, therefore bread made from it will not rise very well. The straw has many uses, as a biomass for fuel, for thatching, and as a mulch in the garden. The fibers obtained from the stems are used for paper-making. The stems are harvested in the late summer, after the seed has been harvested, they are cut into usable pieces and soaked in clear water for 24 h. They are then cooked for 2 h in lye or soda ash and then beaten in a ball mill for 1.5 h. The fibers make a green-tan paper. The starch from the seed is used for laundering.
Ssp. carthlicum is marked by a high resistance to fungal diseases. As such, they are considered to be of high value for wheat improvement (Dorofeev 1968). Already Vavilov (1914, 1926) found it resistant to downy mildew. Oliver et al. (2008) evaluated reactions to Fusarium head blight (FHB) in 376 accessions of five cultivated subspecies of T. turgidum, including carthlicum, dicoccon, polonicum, turanicum, and turgidum. Preliminary data showed that 16 carthlicum and 4 dicoccon accessions consistently exhibited full resistance or moderate resistance to FHB. These accessions likely carry genetic resistance to FHB and can be used directly in breeding programs to enhance FHB resistance in durum wheat.
10.3.2.11 Diversity of Domesticated T. turgidum
Given that only a relatively small number of wild emmer genotypes were taken into cultivation, the genetic basis of the cultivated wild emmer was relatively narrow, representing only a fraction of the large variation that exists in the wild form. This narrow genetic basis was further reduced during the formation of domesticated emmer, as mutations from fragile to non-fragile rachis presumably occurred only in a small number of wild emmer genotypes. These two phenomena, referred to as a “genetic bottleneck”, is characteristic of many domesticated crops (Stebbins 1950). Moreover, a large fraction of the ancient gene pool of domesticated tetraploid wheat was lost in the Near East about 2500 years ago, or even earlier, when ssp. durum replaced domesticated emmer and the small-grained, free-threshing tetraploid wheat, ssp. parvicoccum (Nesbitt 2002). In addition, modern plant breeding practices have further eroded the genetic basis of domesticated tetraploid wheat due to the replacement, in many countries, of lots of traditional varieties (landraces) by a small number of high-yielding cultivars. The current, relatively narrow genetic basis of the domesticated tetraploid wheats decreases their adaptability to abiotic stresses, increases their susceptibility to biotic pressures, and considerably limits the ability to further improve their performance. This has further boosted the interest of wheat geneticists and breeders in the wild relatives of wheat, mainly in wild emmer, in an attempt to exploit their broad gene pool for the improvement of domesticated tetraploid wheat.
Several studies have estimated changes in diversity between wild emmer and its domesticated descendants. Most studies used isozymes, SSRs, or RFLPs, but recently, studies based on nucleotide diversity, that are being more comparable between laboratories and experimental systems, have been performed (Buckler et al. 2001).
Thus, Haudry et al. (2007) analyzed nucleotide diversity at 21 loci in a sample of 28 wild emmer accessions, collected from all the distribution areas of this taxon, in 12 ssp. dicoccon lines, 20 ssp. durum lines, and 41 T. aestivum ssp. aestivum lines. As expected, their results showed that the diversity of the domesticated subspecies of T. turgidum, dicoccon and durum, and of T. aestivum was a subset of that observed in wild emmer, namely, nucleotide diversity levels were found to be much lower in the domesticated forms than in the wild progenitor. Assuming that the sample of wild emmer studied by Haudry et al. (2007) accurately reflected the diversity of wild emmer 10,000 years ago, initial diversity was reduced by 84% in ssp. durum and 69% in ssp. aestivum. The loss of nucleotide diversity during domestication of the wheats is one of the largest reported thus far for a crop species (Haudry et al. 2007). Most crops have nucleotide diversities about 30% lower than those of their wild progenitor, but wheat and barley lost significant and similar amounts of diversity (Kilian et al. 2006).
Akhunov et al. (2010) assessed the distribution of diversity in 2114 genes among and within the bread wheat subgenomes of T. aestivum ssp. aestivum and wild emmer. Of the analyzed loci, 305 (52%) and 296 (51%) were polymorphic in the A and B subgenomes of ssp. aestivum, respectively, and 316 (54%) and 338 (59%) were polymorphic in the A and B subgenomes of wild emmer, respectively. The estimates of nucleotide diversity were similar between the A and B subgenomes of bread wheat and between the A and B subgenomes of wild emmer, which showed higher diversity than the corresponding genomes in ssp. aestivum (Akhunov et al. 2010). Chromosome 5A of ssp. aestivum and chromosomes 2A and 7A of wild emmer had higher diversity than the genome-wide average. With the sole exception of ssp. aestivum chromosome 2A, diversity was low in genes in proximal chromosomal regions and high in genes in distal chromosomal regions. In the B subgenome of ssp. aestivum, chromosome 2B had higher diversity and chromosome 4B had lower diversity than the rest of the chromosomes (Akhunov et al. 2010).
Thuillet et al. (2005) reported a series of bottleneck effects in the population history of ssp. durum landraces, detected as decreases in the effective population size, one of these being in the transition from emmer to free-threshing wheat. In accordance with these findings, maternal lineages in emmer and wild emmer also seem to be more diversified (Oliveira et al. 2012). The number of unique chloroplast (cp) haplotypes detected in wild emmer (7) was higher than in domesticated emmer (3), ssp. durum (3) or ssp. turgidum (2). Out of the 14 cp haplotypes found in durum and turgidum, 4 were also present in domesticated emmer accessions and 3 were present in wild emmer. Of the 7 cp haplotypes found in domesticated emmer, 2 were also found in wild emmer. This suggests a scenario in which all three subspecies share a common maternal ancestral gene pool that later became distinct between them, due to different population histories.
The recent assembly of the genome of cultivar Svevo of ssp. durum by Maccaferri et al. (2019), facilitated the comparison between the genome of ssp. durum and that of its wild ancestor, ssp. dicoccoides (Avni et al. 2017), revealing changes imposed by the domestication process during thousands of years of unconscious and conscious selection under cultivation, and by modern, scientific-based, breeding programs. Regions exhibiting strong signatures of genetic divergence associated with domestication and breeding were widespread in the durum genome, with several major diversity losses in the pericentromeric regions, which occurred during the domestication of wild emmer. The reduction of diversity continued more moderately, but spread over the genome, during the evolution of domesticated emmer wheat and that of durum landraces, and, more recently, in modern cultivars as a consequence of breeding activity.
In accordance, Avni et al. (2017) examined DNA variation in regions of the emmer genome that were under domestication selection. To identify these regions, they characterized the genomic diversity of 31 domesticated accessions and 34 wild emmer accessions, using a whole exome capture assay. Depending on the method used, between 32 and 154 genomic regions, spanning 0.6% (68 Mb)–3.1% (373 Mb) of the domesticated emmer genome, emerged as regions potentially affected by selection. These regions in the domesticated emmer genome were significantly enriched (> 95th percentile) with nonsynonymous SNPs. In these regions, Avni et al. (2017) found only a minor loss of genetic diversity among domesticated emmer genotypes (mean nucleotide diversity in domesticated emmer was πD = 1.1 × 10−3) as compared to wild emmer (mean nucleotide diversity πD = 1.3 × 10−3). This minor loss of genetic diversity indicating that selection under domestication preferentially enriched variants with possible functional effects in coding regions. The enrichment under domestication included genes involved in response to auxin stimulus.
It is likely that, the long-mixed cultivation of wild and domestic forms of emmer in many sites in the Levantine Corridor (Kislev 1984) has provided ample opportunities for some gene flow from wild to domesticated emmer. Consequently, domesticated emmer evolved in many sites as a polymorphic population, rather than as single genotypes (Feldman and Levy 2015). The increase in the genetic basis of the young crop, reduced its vulnerability to biotic and abiotic stresses. Moreover, the spread of wheat culture to different countries with different climatic and edaphic conditions, created different kinds of abiotic stresses. These stresses might have triggered activities of retrotransposons and MITEs as well as of transcription factors that, in turn, turned on many silent genes or suppressed the activity of others, and also caused new genetic variation via mutations. Selection under domestication by different farmers for different useful traits in different climatic and edaphic regions, further increased the diversity of the domesticated forms. Moreover, the tendency of traditional farmers in many parts of the world to grow in a single field (polymorphic fields), a mixture of genotypes that hybridized and recombined, enabled the selection of genotypes that were more desirable to the farmers. Selection pressure was thus, exerted consistently, but in different directions, by different farmers. These efforts resulted in many landraces that had a better adaptation to a wider range of climatic and edaphic conditions and to diverse farming regimes.
Furthermore, even after the complete replacement of wild emmer by domesticated emmer, the latter could continue to absorb genes from wild genotypes that grew on the edges of many cultivated fields or among the stones and rocks within fields, which further broadened its genetic basis (Percival 1921; Huang et al. 1999; Dvorak et al. 2006; Luo et al. 2007). This is in agreement with the comparatively high level of RFLP recently found in a sample of lines of domesticated tetraploid wheat, i.e., in T. turgidum ssp. dicoccon and ssp. durum (Huang et al. 1999; Luo et al. 2007). Genetic diversity of domesticated tetraploid wheat was only somewhat smaller than that of wild emmer (Huang et al. 1999), indicating that the domesticated types absorbed a significant portion of the genetic variation that exists in the wild forms.
Thus, the study of He et al. (2019) revealed that the genome-wide single-nucleotide polymorphism (SNP) diversity in hexaploid wheat was strongly influenced by gene flow from its tetraploid wild ancestor. Regions of introgression in the wheat A and B subgenomes showed increased levels of genetic diversity and reduced genetic differentiation from wild emmer. Both patterns were consistent with wild-relative introgression into domesticated wheat, which offset the effects of allopolyploidization and domestication bottlenecks on diversity in these genomes (Akhunov et al. 2010).
10.3.2.12 Cytology, Cytogenetics and Evolution
The discovery of wild diploid wheat T. monococcum ssp. aegilopoides and wild tetraploid wheat T. turgidum ssp. dicoccoides, made it possible for Schulz (1913b) to assemble, on the basis of plant morphology, the first natural classification of the wheats (Table 10.1). He divided the genus Triticum into three major groups: einkorn, emmer, and dinkel. Each group was subdivided into wild and domesticated species; the domesticated species were separated further into hulled and naked (free-threshing) types. Schulz (1913b) assumed correctly that the domesticated naked types were derived from the domesticated hulled forms, which, in turn, were derived from the wild progenitors. Schulz’s classification was supported by further studies of taxonomic classifications (von Tschermak 1914; Percival 1921), by serological relationships, as determined by Zade (1914), by Vavilov’s (1914) classification in respect to reaction to the pathogens rust and mildew, and by Sax’s (1921) studies of sterility in interspecific wheat hybrids. Table 10.6 presents the modern classification of the wild and domesticated subspecies of the emmer series, i.e., Triticum turgidum.
At the same time, a comparatively large number of investigators performed cytological studies of the chromosome number in the wheats. Several cytologists reported 8 haploid chromosomes in T. monococcum, while others reported 40 in T. vulgare (currently T. aestivum ssp. aestivum) (reviewed in Sax 1922). However, the pioneering cytological studies of Sakamura (1918), Sax (1918) revealed the correct chromosome number of the wheats. Sakamura (1918), analyzing root-tip cells, obtained the following results: T. monococcum had 14 chromosomes, T. dicoccon, T. durum, T. turgidum and T. polonicum (currently all are subspecies of T. turgidum) had 28, and T. vulgare, T. compactum and T. spelta (currently all are subspecies of T. aestivum) had 42. Sax (1918) determined in meiotic cells the correct chromosome number of tetraploid wheat, T. turgidum ssp. durum. It then became obvious that Schultz’s three groups of wheats also differ in their chromosome number and represent a polyploid series in which the einkorn are diploids (2n = 14), the emmer are tetraploids (2n = 28), and the dinkel are hexaploids (2n = 42).
But, since Sakamura (1918) did not present any illustrations to support his counts, his results were questioned by Percival (1921). Yet, the studies of Kihara (1919, 1924) and Sax (1921, 1922) regarding the cytogenetic relationships between the three wheat groups, diploid, tetraploid and hexaploid, showed that Sakamura’s results were definitely correct and the wheats comprise a polyploid series, based on sets of seven chromosome pairs.
In 1930, Kihara upgraded the definition of “genome”, that was termed earlier by Winkler (1920), as a haploid chromosome set, to a chromosome set that acts as a fundamental genetic and physiological system whose complete gene content is indispensable for the normal development and activity of an organism. One pair of homologous genomes must be present in a fully viable fertile diploid organism, and at least one in polyploid. Two genomes are strictly homologous, if the chromosomes forming bivalents at first meiotic metaphase are identical, similar in length, gene position, and centromere location, whereas two genomes are semi-homologous (= homoeologous; Huskins 1931) if they are phylogenetically similar but not strictly homologous and all or a part of their pairing chromosomes have only similar segments in common (Kihara 1930).
Since the discovery that the polyploid species of Triticum comprise an allopolyploid (having two or three different subgenomes) series, attempts have been made to identify the diploid donors of the two subgenomes to allotetraploid wheat. In this endeavor, studies were extended to the wild relatives of wheat, particularly to the closely related genus Aegilops that also comprises an allopolyploid series with diploid, tetraploid and hexaploid species (Lilienfeld 1951, and reference therein). The species of these two genera have been subjected to extensive taxonomic, cytogenetic, genetic, biochemical, molecular, and evolutionary studies by numerous scientists (see review s of Kihara 1954; Mac Key 1966; Morris and Sears 1967; Kimber and Sears 1987; Feldman et al. 1995; Feldman 2001; Gupta et al. 2005; Dvorak 2009).
Based on the concept of genome stability, and on the assumption that the genomes of the allopolyploid species remain similar to those of their parental forerunners, Kihara (1930) developed the “genome analysis” method for the identification of the genomic constitution of the wheat allopolyploid species. This method has been one of the most extensively used in attempts to identify the diploid ancestors of the allotetraploid wheats. This method is based on the use of diploid species as analyzers in crosses with allopolyploid species whose genome constitution had to be ascertained. The first step in this method involves the analysis of the chromosomal-pairing relations between the genomes of all available diploid species of the group in question. Kihara broadened his investigation to include species of the closely related genera Aegilops and Ambliopyrum (Kihara 1929, 1930, 1937, 1940, 1947, 1949, 1954). In these studies, Kihara and colleagues studied chromosomal pairing at first meiotic metaphase and fertility of all the possible combinations of interspecific diploid hybrids. These studies has provided the most consistent recognition of genomic similarities in the wheat group (Lilienfeld 1951). Genome analysis of wheat and its relatives also provided insight into the evolutionary past of these species. With this method. Kihara used the diploid species of Aegilops and Amblyopyrum as analyzers of the genomes in the allopolyploids of the genera Aegilops and Triticum (Lilienfeld 1951). Nine diploid analyzers were established: one from Amblyopyrum (A. muticum), and eight from Aegilops (caudata, umbellulata, comosa, uniaristata, squarrosa (currently tauschii), bicornis, longissima (including sharonensis) and speltoides). All allopolyploid Aegilops and Triticum species are comprised of contributions of the genomes of these diploid analyzers, except for A. muticum, Ae. bicornis, Ae. sharonensis, and T. monococcum (Kihara 1954). [Ae. searsii was discovered later on, in 1976 (Feldman and Kislev 1977), and was not included in Kihara’s genome analysis]. The lack of participation of these diploids in the formation of allopolyploid species of Triticum and Aegilops requires an explanation.
The working hypothesis of Kihara (1930), Sax (1935) was that cytogenetics of interspecific hybrids, especially between species of different ploidy levels, might have great theoretical and applied aspects; they may shed light on the origin and mode of evolution of the relevant allopolyploid species and offer the possibility to synthesize them from different lines (genotypes) of the parental species and thus, to augment the genetic basis of the pertinent allopolyploid species (Lilienfeld 1951). The cytological analysis of interspecific hybrids has been of value in determining the relationships and origin of many species of plants (Sax 1935). Species which produce hybrids with regular meiotic pairing and normal fertility appear to be distinguished primarily by differentiation of genetic factors. Such species retain their identity only solely by geographic or physiological isolation. Hybrids showing irregular meiotic pairing and reduced fertility indicate that the genomes of their parental species have diverged.
Kihara (1919, 1924), Sax (1922) provided the first evidence indicating that the polyploid wheats were allopolyploids. This conclusion was based on the mode of meiotic chromosome behavior observed in F1 hybrids between diploid and tetraploid wheat species and between tetraploid and hexaploid wheat species. Seven bivalents and seven univalents were observed in the majority of the meiocytes in triploid hybrids derived from crosses between T. turgidum (2n = 28) and T. monococcum (2n − 14). Thus, Kihara (1919, 1924), Sax (1922) concluded that the chromosomes in one of the two subgenomes in T. turgidum were homologous with the chromosomes of the genome in T. monococcum. The pollen mother cells in the pentaploid hybrids derived from crosses between T. aestivum (2n = 42) and T. turgidum contained 14 bivalents and 7 univalents. This indicated that the chromosomes in two of the three subgenomes of T. aestivum were homologous with those of the two subgenomes of T. turgidum. These studies indicated that T. turgidum evolved as a result of hybridization between two different diploid species, a diploid wheat and another yet unknown diploid species, followed by chromosome doubling, and that T. aestivum is an allohexaploid that resulted from hybridization of T. turgidum with a yet unknown diploid species (Kihara 1924, 1925, 1932, 1938; Percival 1921; Sax 1921, 1927). Consequently, Kihara (1924) designated the genome of diploid wheat AA, that of allotetraploid wheat AABB, and the genome of hexaploid wheat AABBDD. However, since the International Code for Botanical Nomenclature dictates indication of the genome of the female parent in hybrids and allopolyploids first, then, as the donor of the B subgenome was the female parent, the correct designation of the genome of T. turgidum should be BBAA and that of T. aestivum BBAADD.
Following van Slageren (1994), modern classification for the genus Triticum recognizes two diploid species, T. monococcum L. and T. urartu Tum. ex Gand., two tetraploid species, T. turgidum L. and T. timopheevii (Zhuk.) Zhuk., and two hexaploid species, T. aestivum L. and T. zhukovskyi Men. & Er. (Table 10.5). The evolution of the wheats is illustrated in Fig. 10.5 (for details see Levy and Feldman 2022). The economically important wheats are T. aestivum ssp. aestivum (bread or common wheat, comprising 95% of the global wheat production) and T. turgidum ssp. durum (macaroni wheat).
Phylogenetic representation of wheat evolution. Wheat evolution is shown starting ~ 7 MYA from a progenitor that gave rise to the A, B and D lineages that merged to form bread wheat. The relative timing of the major speciation events is shown in the horizontal axis and described in the boxes above. The tree is adapted from Glémin et al. 2019; Avni et al. 2022; Li et al. 2022. [Fig. 1 from Levy and Feldman (2022)]
The polyploid species of wheat are a classic example of evolution through allopolyploidy (Kihara 1924; Sax 1921, 1927; Sears 1948, 1969; Kihara et al. 1959; Morris and Sears 1967). They behave like typical genomic allopolyploids; that is, their chromosomes pair in a diploid-like fashion and the mode of inheritance is disomic. Many attempts were made to identify the diploid donors of the B subgenomes to T. turgidum, and the third subgenome of T. aestivum. Most of these attempts used the cytogenetic approach of genome analysis, developed by Kihara (1919, 1924, 1930). However, the accumulating cytogenetic and molecular evidence has indicated that, while one subgenome remained relatively unchanged, the second subgenomes of allopolyploid wheat and Aegilops, changed considerably from those of their parental diploids. These genomes were termed modified genomes by Kihara (1954) and other wheat cytogeneticists. Thus, almost every allotetraploid species of Aegilops and Triticum contains an unchanged genome alongside a modified one whose diploid origin has been difficult to trace (Zohary and Feldman 1962). It is therefore more difficult to identify the diploid donor of the B subgenome of the allopolyploid wheats than the donor of the A subgenome.
10.3.2.13 Origin of the A Subgenome
From the time when only one diploid wheat species, T. monococcum, was known, and although the correspondence of the A subgenome of the tetraploid subspecies of T. turgidum with the A genome of the wild and domesticated T. monococcum is not perfect (Kihara and Lilienfeld 1932), it was generally accepted by wheat cytogeneticists that this diploid wheat specie is the donor of the A subgenome to allotetraploid wheat (Sax 1922; Kihara 1924; Lilienfeld and Kihara 1934; Sears 1948). The discovery in 1937 in Armenia (Tumanian 1937) of a second wild diploid wheat species, T. urartu, suggested the presence of another potential donor of the A subgenome. T. urartu differs from wild T. monococcum, ssp. aegilopoides, by several morphological features (Gandilian 1972; Dorofeev et al. 1980; Johnson 1975). Johnson (1975) also found T. urartu growing abundantly in Lebanon, southeastern Turkey, southwestern Iran and Transcaucasia. Although Giorgi and Bozzini (1969b) showed that the karyotypes of T. urartu and T. monococcum are identical, the nuclear DNA content is significantly different in the two species (Furuta et al. 1986; Eilam et al. 2007; Table 2.4). Moreover, T. urartu and T. monococcum differ in biochemical and molecular features, namely, isozymes (Jaaska 1974, 1980, 1982), HMW glutenin subunits (Waines and Payne 1987; Ciaffi et al. 1998; Castagna et al. 1994), Gliadin genes (Ciaffi et al. 1997), AFLP (Sasanuma et al. 2002; Heun et al. 2008), RFLP (Takumi et al. 1993; Le Corre and Bernard 1995), SSRs (Hammer et al. 2000), and AFLP and simple sequence length polymorphism (SSLP) (Sasanuma et al. 2002). A similar conclusion that the two diploid species differ from each other was also reached following chloroplast SSLP analysis (Mizumoto et al. 2002). Furthermore, Baum and Baily (2004) found that T. urartu differs from T. monococcum in the short and long units of the 5S DNA, and Dvorak et al. (1988, 1993) found extensive differences between these two species in the restriction profiles of repeated nucleotide sequences and the promoter region of the 18S-5.8S-26S rRNA genes. The divergence between T. urartu and T. monococcum is also apparent from the cytogenetic data; chromosome pairing in the F1 hybrids between the two species was somewhat reduced (Johnson and Dhaliwal 1978; Shang et al. 1989) and the F1 hybrid was completely sterile when T. urartu served as the female parent (Johnson and Dhaliwal 1976). Although they grow sympatrically in many parts of their distribution area, the two species are partly genetically isolated and have diverged to some extent from each other on the morphological, cytogenetic and molecular levels. Yet, in spite of these differences, it is generally accepted that the two-diploid Triticum species are closely related and presumably, of monophyletic origin (Dvorak and Zhang 1992). Hence, Dvorak (1998) designated the nuclear genome of T. urartu A and that of T. monococcum Am.
As it became apparent that diploid wheat comprises two different species, it was important to reexamine the sources of the A subgenome in the allopolyploid wheats. Studies of chromosome pairing in F1 hybrids between ditelosomic lines of T. aestivum and T. urartu or T. monococcum showed somewhat better pairing with T. urartu chromosomes than with T. monococcum, indicating that the A genome of T. urartu is closer to the A subgenome of polyploid wheat than to that of T. monococcum (Chapman et al. 1976; Dvorak 1976). To determine whether the T. urartu genome is more closely related to the A or B subgenome of the polyploid wheats, Chapman et al. (1976), Dvorak (1976) crossed T. urartu with lines of T. aestivum that were ditelosomic for the A and B subgenome chromosomes. In both studies, only the telocentrics of the A subgenome paired with T. urartu chromosomes, unequivocally showing that the chromosomes of T. urartu are homologous to the chromosomes of the A subgenome.
Similarly, by means of serological storage protein markers, Konarev and his associates (Konarev 1983; Konarev et al. 1976, 1979) were able to distinguish between the genomes of T. urartu and T. monococcum, a discovery that enabled them to show that the genome of T. urartu is more similar to the A subgenome of the wild and domesticated subspecies of T. turgidum than to the genome of T. monococcum. Additional evidence that subgenome A of allopolyploid wheats derived from T. urartu were obtained by polyacrylamide gel electrophoresis (PAGE) and by differential staining of seed albumins and globulins (Caldwell and Kasarda 1978). Likewise, Nishikawa (1983), using isozyme studies, showed that emmer wheat received its A subgenome from T. urartu. Similar results were obtained by Takumi et al. (1993), who used DNA clones, known to hybridize with the DNA of the A subgenome chromosomes of common wheat, in RFLP analyses of nuclear DNAs of diploid and polyploid wheats. They calculated genetic distances between all the pairs of accessions determined using RFLP data and clustered the species using the UPGMA method. All the accessions of T. urartu, T. turgidum ssp. durum and T. aestivum ssp. aestivum were clustered in one group. Those of wild and domesticated T. monococcum were in a different group. So, they concluded that the A subgenomes of tetraploid and hexaploid wheats originated from T. urartu. Dvorak et al. (1988), analyzing polymorphism in repeated nucleotide sequences, confirmed that the A subgenome derived from T. urartu and not from T. monococcum. Similarly, variation in 16 repeated nucleotide sequences showed that the A subgenomes of T. turgidum, T. timopheevii, and T. aestivum were contributed by T. urartu (Dvorak et al. 1993). Still little divergence in the repeated nucleotide sequences of the A subgenomes of these allopolyploid species from the genome of T. urartu was detected (Dvorak et al. 1993). In accordance with the data of Dvorak et al. (1993), recent whole genome sequencing showed that the donor of the A subgenome to allotetraploid wheat diverged from the genome of T. urartu ~ 1.28 MYA (Li et al. 2022).
The donor of the A subgenome to allotetraploid wheat diverged from the genome of T. urartu ~ 1.26 MYA (Li et al. 2022).
10.3.2.14 Origin of the B Subgenome
In contrast to the A subgenome donor, the identity of the B subgenome donor has so far not been conclusively defined. On the basis of chromosome pairing at meiosis in F1 hybrids involving tetraploid and hexaploid wheats with polyploid species of Agropyron, researchers like Wakar (1935), Peto (1936), Matsumura (1951) believed that the B subgenome must have been contributed by an Agropyron species. In accord with this, McFadden and Sears (1946) suggested that the species involved might be the diploid A. triticeum. Yet, it soon became apparent that the diploid donor of the B subgenome to allopolyploid wheats is a more closely related species, possibly from the section Sitopsis of the genus Aegilops. Studies were then extended to the five species of Aegilops section Sitopsis, namely Ae. speltoides, Ae. bicornis, Ae. sharonensis, Ae. longissima and Ae. searsii, since they appear to possess the complementary requisite morphological characteristics of the B subgenome donor (Kerby and Kuspira 1987). Consequently, the five Sitopsis species have been subjected to intense morphological, geographical, cytogenetic, genetic, biochemical, molecular, and evolutionary studies by numerous researchers, who employed various experimental approaches (see reviews of Kihara 1954; Riley et al. 1958; Mac Key 1966; Morris and Sears 1967; Kerby and Kuspira 1987; Kimber and Sears 1987; Feldman et al. 1995; Feldman 2001; Gupta et al. 2005; Dvorak 2009). These studies implicated six different diploid species as putative B subgenome donors: the five species of section Sitopsis and T. urartu. Yet, despite these countless efforts, the presented evidence obtained by the above-mentioned studies still failed to unequivocally identify the B subgenome donor and its identity remains ambiguous and controversial.
10.3.2.14.1 Morphological Evidence
Based on morphological comparison, Sarkar and Stebbins (1956) concluded that wild T. turgidum arose as an allotetraploid between T. monococcum and another species that is morphologically close to Ae. speltoides var. ligustica. Consequently, they suggested that Ae. speltoides, or a closely related species, is the donor of the B subgenome. On the other hand, Sears (1956a, 1956b) observed that the amphiploid Ae. bicornis—T. monococcum more closely morphologically resembles T. turgidum ssp. dicoccon than the amphiploid Ae. speltoides—T. monococcum. Moreover, at meiosis of the F1 hybrid between the amphiploid Ae. bicornis—T. monococcum and ssp. dicoccon, an average of almost 9 bivalents or its equivalent was observed, indicating some pairing affinity between subgenome B and the Ae. bicornis genome. From these morphological and cytological data, Sears (1956a) concluded that Ae. bicornis or a closely related species, is the donor of the B subgenome.
Tanaka (1956) pointed out that both Ae. longissima and Ae. sharonensis possess morphological traits expected of the B subgenome donor. The amphiploid derived from crossing Ae. longissima with T. monococcum resembled T. turgidum with respect to several morphological properties. However, from the low pairing (average of 7 bivalents) in the hybrid between them, he concluded that there is very little chromosomal homology between the chromosomes of Ae. longissima and those of subgenome B and thus, it can not be considered the B subgenome donor. On the other hand, Kushnir and Halloran (1981) observed that the amphiploid derived from the hybrid Ae. sharonensis x T. monococcum had a spike, spikelet, and grain morphology similar to that of wild emmer, T. turgidum ssp. dicoccoides, and can be considered the B subgenome donor. On the basis of its morphology, Ae. searsii was also suggested as a possible B subgenome donor (Feldman 1978). Hence, based on morphological traits, each of the five Aegilops species of section Sitopsis were proposed as the donor of the B subgenome.
10.3.2.14.2 Geographical Evidence
Currently, Ae. speltoides is in contact with T. urartu in Lebanon, Syria, Turkey, Iraq, and Iran. In this region, Ae. speltoides is also in contact with wild T. turgidum and wild T. timopheevii. Ae. searsii, on the other hand, is native to the southern Levant (Feldman and Kislev 1977), where it has a sympatric distribution with wild T. turgidum. In southern Syria and southeastern Lebanon, Ae. searsii has massive contact with T. urartu (Feldman and Kislev 1977; Feldman 1978). Dvorak and Luo (2007), based on RFLP studies, found that T. urartu from the vicinity of Mount Hermon is the closest to the A subgenome of wild T. turgidum and assumed that this allotetraploid formed in this region. Assuming that the present-day distribution of the Sitopsis species reflects their distribution 700,000–900,000 years ago, when wild T. turgidum formed (Gornicki et al. 2014; Marcussen et al. 2014; Middleton et al. 2014), then, Ae. searsii can be considered the donor of the B subgenome to allotetraploid T. turgidum.
10.3.2.14.3 Evidence from Karyotypic Studies
T. turgidum and T. aestivum contain two pairs of satellited (SAT) chromosomes (Pathak 1940; Riley et al. 1958). Using monosomic lines, Okamoto (1957b) determined that these satellited chromosomes belong to the B subgenome; one satellite is located on the short arm of chromosome 1B and the second on the short arm of chromosome 6B. Riley et al. (1958) found that two similar pairs of SAT chromosomes are found in Ae. speltoides and not in Ae. bicornis, Ae. longissima, and Ae. sharonensis, thus showing that Ae. speltoides is the only Sitopsis species that can be considered the B subgenome donor. Kushnir and Halloran (1981) reported that the SAT chromosomes in Ae. sharonensis are similar to those observed in T. turgidum and concluded that this Aegilops species could be the B subgenome donor. Feldman (1978), upon observing that the chromosomes of Ae. searsii with large and medium sized satellites resembled chromosomes 1B and 6B of T. aestivum, respectively, suggested that Ae. searsii could be the B subgenome donor to the allopolyploid wheats.
Giorgi and Bozzini (1969a, b, c) described the karyotypes of T. turgidum, T. monococcum, T. urartu, Ae. bicornis, Ae. speltoides, and an Ae. speltoides x T. monococcum amphiploid. They found that the karyotypes of T. urartu, Ae. bicornis, and Ae. speltoides show that these three species could not be donors of the B subgenome to T. turgidum. Kerby and Kuspira (1988) compared the karyotypes of T. turgidum, T. monococcum, and all the putative B subgenome donors. The chromosomes of the A subgenome of T. turgidum were identified via comparison to the karyotype of T. monococcum. Comparisons of the chromosomes of the B subgenome of T. turgidum with the karyotypes of the putative B subgenome donors showed that only the karyotype of Ae. searsii was similar to the one deduced for the donor of the B subgenome, suggesting that Ae. searsii is, therefore, the most likely donor of the B subgenome to the allopolyploid wheats.
Natarajan and Sarma (1974) studied the distribution of large blocks of constitutive heterochromatin and found that Ae. speltoides, of the Sitopsis species, had a pattern of distribution of heterochromatin that most resembled that of the B subgenome chromosomes. Contrarily, Gill and Kimber (1974b) observed that the C-banding pattern of Ae. speltoides chromosomes differs substantially from that of the B subgenome chromosomes of T. aestivum and therefore, casts doubt on the validity of the satellite and heterochromatin distribution evidence.
10.3.2.14.4 Evidence from Meiotic Chromosome Pairing
One of the most extensive searches for the B subgenome donor involved analysis of chromosome pairing at first meiotic metaphase of F1 hybrids between T. turgidum and different diploid species considered to be the B subgenome donor. Many such studies indicated Ae. speltoides as a possible donor of the B subgenome, since hybrids between Ae. speltoides and T. turgidum exhibited a relatively high level of pairing, namely, from a range of 4.66 to 6.22 bivalents per meiocyte (McFadden and Sears 1946; Riley et al. 1958), to 7 bivalents per meiocyte in most pollen mother cells (Jenkins 1929). Since F1 hybrids between Ae. speltoides and T. monococcum showed little or no pairing (Kihara 1940), it was concluded that Ae. speltoides and T. monococcum possessed different genomes, and that most of the pairing in T. turgidum x Ae. speltoides hybrids was between the B subgenome and speltoides chromosomes (Riley et al. 1958).
But allopolyploid wheats contain mechanisms restricting homoeologous pairing, including the Ph1 gene on chromosome arm 5BL of T. aestivum (Okamoto 1957a; Riley and Chapman 1958; Sears and Okamoto 1958), and, therefore, pairing in hybrids between allopolyploid wheats and the four Sitopsis species (excluding Ae. speltoides), namely, Ae. bicornis, Ae. sharonensis, Ae. longissima, and Ae. searsii, is very low. On the other hand, Ae. speltoides contains genes that suppress the Ph1 effect and thus, brings about homoeologous pairing (Riley et al. 1961; Dvorak 1972). Indeed, in 1961, Riley et al. crossed T. aestivum monosomic for chromosome 5B, the chromosome that carries the Ph1 gene, with Ae. speltoides. Regardless of whether chromosome 5B (Ph1) was present, the F1 hybrids showed a high incidence of chromosome pairing, which included the formation of bivalents, trivalents, and quadrivalents. These observations indicated that all or most of the pairing was between and among homoeologous chromosomes. From this result, it was concluded that the genotypes of Ae. speltoides used in this and previous experiments suppressed the action of Ph1, allowing homoeologous as well as homologous chromosomes to pair. Thus, it was impossible from the original cytological data to determine the extent of homology between the chromosomes of Ae. speltoides and those in the B subgenome of the allopolyploid wheats.
Dvorak (1972), in studying chromosome pairing of different accessions of Ae. speltoides in hybrids with bread wheat, recognized three speltoides types of genotypes: those showing high pairing, intermediate pairing and low pairing. On the basis of heteromorphic bivalents observed in hybrids derived from crosses between ditelosomic lines of T. aestivum and low-, intermediate-, and high-pairing genotypes of Ae. speltoides, Kimber and Athwal (1972) concluded that the pairing in these hybrids was between homoeologous chromosomes. Chromosomal pairing in the F1 hybrid with the low-pairing genotype of Ae. speltoides was very low, with average 0.7 rod bivalents per cell. The conclusion that Ae. speltoides contains only homoeologous chromosomes rather than homologous ones to the chromosomes of T. aestivum was further supported by the observation that only homologous chromosomes paired in the amphiploids T. aestivum—low-pairing type of Ae. speltoides (Kimber and Athwal 1972). These cytological data preclude Ae. speltoides as the source of the B subgenome (Kimber and Athwal 1972).
Ae. longissima, Ae. sharonensis, and Ae. bicornis have been ruled out as the potential donors of the B subgenome, mainly on the grounds of the low meiotic pairing in F1 hybrids between them and allopolyploid wheats (Riley et al. 1958; Riley 1965). Recent studies, however, attributed the low pairing to a Ph-like gene, existing in these three Aegilops species, that, together with the Ph1 of allopolyploid wheats, suppresses homoeologous pairing in the hybrids between allopolyploid wheat and these species (Feldman 1978). Mello-Sampayo (1971) discovered one genotype of Ae. longissima that induced an intermediate level of pairing (IP) (five to six bivalents) in hybrids with T. aestivum. It was assumed that this IP genotype lacks the Ph-like gene (Avivi 1976; Feldman 1978). The existence of ph-like genes in diploid species of Aegilops has already been suggested by several researchers (Okamoto and Inomata 1974; Waines 1976; Maan 1977). Feldman (1978) crossed this IP genotype of Ae. longissima with ditelosomic lines of the A and B subgenomes of T. aestivum and found that most of the pairing involved chromosomes of the B subgenome and those of Ae. longissima, while the chromosomes of the A and D subgenomes paired relatively little. The chromosomes of the B subgenome paired at a much higher frequency in hybrids with Ae. longissima as compared to hybrids with Ae. speltoides. Based on these observations, Feldman (1978) concluded that the genome of Ae. longissima and probably of other Sitopsis species (e.g., Ae. searsii) is closer to the B subgenome than that of Ae. speltoides.
The meiotic behavior of Triticum aestivum x Aegilops speltoides, T. aestivum x Ae. sharonensis and T. aestivum x Ae. longissima (hybrid genome constitution ABDS, ABDSsh, and ABDSl, respectively) has been analyzed by Fernandez–Calvin and Orellana (1994), using the C-banding technique. In all of the hybrids analyzed, the mean number of bound arms per cell for associations between the A and D subgenomes chromosomes was significantly higher than the mean number of associations between the B and S, the B and Ssh and the B and Sl genomes. These results indicated that the genomes of Ae. speltoides, Ae. sharonensis and Ae. longissima show a similar affinity with the genomes of hexaploid wheat; therefore, none of these species can be considered to be a distinct donor of the B subgenome of wheats (Fernandez–Calvin and Orellana 1994).
A different conclusion was reached by Maestra and Naranjo (1998), who analyzed homoeologous pairing at first meiotic metaphase of F1 hybrids between T. aestivum, bearing the Ph1 and the Ph2 genes, or its mutants ph1b or ph2b, with a high-pairing genotype of Ae. speltoides. They applied the C-banding technique to identify the chromosome arms of both species. All chromosome arms of Ae. speltoides showed normal homoeologous pairing, implying that no apparent chromosome rearrangements occurred in the evolution of Ae. speltoides relative to wheat. A pattern of preferential pairing of A-D and B-S, confirmed that the S genome is closely related to the B subgenome of allopolyploid wheat. Consequently, they concluded that their results sustain the hypothesis that the B subgenome of the allopolyploid wheats was derived from Ae. speltoides.
Rodriguez et al. (2000a) also set out to assess the relationships between the genome of Ae. speltoides and those of the allopolyploid wheats. To this end, they used C-banding to analyze chromosome pairing at first meiotic metaphase of F1 hybrids involving Ae. speltoides (genome SS), T. timopheevii (genome GGAA), T. turgidum (genome BBAA), and T. aestivum (genome BBAADD). Pairing between chromosomes of the G and S genomes in T. timopheevii x Ae. speltoides (GAS) hybrids reached a frequency much higher than pairing between chromosomes of the B and S in T. turgidum x Ae. speltoides (BAS) hybrids and T. aestivum x Ae. speltoides (BADS) hybrids and pairing between B and G genome chromosomes in T. turgidum x T. timopheevii (BGAA) hybrids or T. aestivum x T. timopheevii (BGAAD) hybrids. These results support a higher degree of closeness of the G and S genomes to each other than to the B subgenome. Such relationships are consistent with independent origins of tetraploid wheats T. turgidum and T. timopheevii and with a more recent formation of the timopheevii lineage.
10.3.2.14.5 Evidence from Seed-Storage Proteins
The electrophoretic pattern of the water-soluble endosperm proteins was determined for T. monococcum, T. aestivum and T. turgidum, (Johnson and Hall 1965; Johnson 1972), T. timopheevii (Johnson et al. 1967), Ae. tauschii (Johnson et al. 1967), and Ae. speltoides, Ae. longissima, and Ae. sharonensis (Johnson 1972). The three Aegilops species of section Sitopsis were found to have electrophoretic band patterns that were inconsistent with those expected of a B subgenome donor, thereby ruling them out as potential donors (Johnson 1975). Johnson then mixed equimolar amounts of proteins from selected lines of T. monococcum and T. urartu and found that the electrophoretic pattern of the mixture included all the bands found in T. turgidum. This led him (Johnson 1975) to suggest that T. urartu could be the B subgenome donor to polyploid wheats. However, the pairing data of Chapman et al. (1976), Dvorak (1976) showed unequivocally that T. urartu is very close to the A subgenome and cannot be the B subgenome donor.
One component of water-soluble endosperm proteins is amylase inhibitors. Vittozzi and Silano (1976) compared the molecular weight and activity of the α-amylase inhibitors from the polyploid wheats with those from all the putative B subgenome donors, excluding Ae. searsii and Ae. sharonensis. Ae. bicornis, Ae. speltoides and T. urartu were rejected as possible B subgenome donors on the basis of differences in α-amylase inhibitor content. Ae. longissima was the only species found to possess all the α-amylase inhibitors contained in T. turgidum, but the specific activities of these proteins were not identical, implying that Ae. longissima might play a role in the speciation of T. turgidum.
Konarev et al. (1976, 1979), Peneva and Konarev (1982), Konarev (1983) compared albumins and gliadins, that are species- and genus-specific, from all the putative B subgenome donors with those from allopolyploid wheats. They found that both Ae. longissima and Ae. searsii possess proteins that are identical to one another as well as to those specified by the B subgenome in the allopolyploid wheats. Many of the proteins of the other potential donors were different from those coded for by the B subgenome. On the basis of this information, Konarev and colleagues concluded that both Ae. longissima and Ae. searsii are equally probable B subgenome donors.
Purothionins are small, basic, highly conserved endosperm proteins (Jones et al. 1982). Jones and Mak (1977) established that there were two forms of the α-purothionin fraction in T. turgidum and T. aestivum isolates, which they designated α and α1, the latter form being specific to the B subgenome. Kerby (1986) determined the amino acid sequence of purothionins from all the putative B subgenome donors and compared these sequences with those of αl-purothionin of T. turgidum and T. aestivum. None of the purothionins isolated from these species had an amino acid sequence identical to that of αl-purothionin. Each of the proteins from Ae. searsii and Ae. bicornis differed from α1 purothionins by a single amino acid substitution, whereas the purothionins from the remaining putative B subgenome donors differed from the α1 sequence by two to five amino acid substitutions. On the basis of these protein comparisons, Kerby (1986) concluded that either Ae. bicornis or Ae. searsii is the most likely donor of the B subgenome. Similarly, Dass (1972) compared the chromatographic profiles of the phenolic compounds from T. turgidum, T. monococcum, Ae. bicornis, and Ae. speltoides. His comparisons revealed Ae. bicornis to possess a profile that most closely resembled the B subgenome profile of T. turgidum, and therefore, he concluded that Ae. bicornis is the more likely B subgenome donor.
10.3.2.14.6 Evidence from Isozymes
Jaaska (1974, 1976, 1980), surveying variation in several enzymes in wheat and diploid Aegilops species, found that, among the contemporary species of section Sitopsis, only Ae. speltoides proved suitable to be the B-subgenome donor to allopolyploid wheats. Diploids of the Emarginata subsection of section Sitopsis, namely, Ae. longissima, Ae. sharonensis, Ae. searsii and Ae. bicornis, are unsuitable for the role of the wheat B genome donors. Nakai (1979), analyzing esterase isozymes, concluded that wild T. turgidum originated from the hybrid of wild einkorn and a member of the Sitopsis section of Aegilops. Likewise, Nishikawa (1983), studying variation in α- and- ß- amylase isozymes in allopolyploid wheats and in their putative diploid ancestors, revealed that the B subgenome of T. turgidum is a recombinant subgenome comprising, at least, chromosome 6Sl from Ae. longissima and 7S from Ae. speltoides. Nishikawa et al. (1992) further sustained the conclusion that T. urartu, the A subgenome donor, first gave rise to a hybrid with Ae. speltoides as the donor of the second subgenome, B, and cytoplasm, and later, a species of subsection Emarginata, most likely Ae. longissima, was involved in repatterning the second subgenome, which resulted in subgenome B of allotetraploid wheat.
10.3.2.14.7 Evidence from Studies on Nuclear DNA
10.3.2.14.7.1 Nuclear DNA Content
Based on nuclear DNA content of T. monococcum, T. turgidum, T. aestivum, Ae. tauschii, Ae. speltoides, Ae. longissima, and Ae. bicornis, Rees (1963), Rees and Walters (1965), Pegington and Rees (1970) supported the notion that Ae. speltoides is the donor of B subgenome to allopolyploid wheats. In contrast, Nishikawa and Furuta (1978) found that the DNA content of T. turgidum is very close to the sum of the content of the diploid species T. monococcum and Ae. longissima, or Ae. bicornis, while the sum DNA of T. monococcum and Ae. speltoides is considerably less than that of T. turgidum. They suggested that Ae. longissima or Ae. bicornis, rather than Ae. speltoides, contributed the B subgenome. Furuta et al. (1984) determined the DNA content of the B subgenome of hexaploid wheat by summing up the DNA contents of the individual B subgenome chromosomes. They found that the nuclear DNA content of Ae. speltoides, is only about 87% that of the B subgenome of hexaploid wheat, whereas the DNA contents of Ae. bicornis, Ae. searsii, Ae. longissima, and Ae. sharonensis are comparable to that of the B subgenome (Furuta et al. 1984). This was consistent with the results they obtained from the synthetic tetraploids T. monococcum–Ae. longissima, T. monococcum–Ae. sharonensis, and T. monococcum–Ae. bicornis, which had DNA content very similar to that of natural T. turgidum. From this, Furuta et al. (1984) concluded that Ae. speltoides was not the donor of the B subgenome.
The results of Eilam et al. (2008) also showed that tetraploid wheat, T. turgidum, contains much more DNA than the sum of DNA content of T. urartu and Ae. speltoides. Consequently, the B subgenome either derived from a species containing more DNA or, if it derived from Ae. speltoides, its DNA content was increased at the polyploid level. If so, the B subgenome is unique in that it underwent DNA content upsizing, as all other genomes of Aegilops and Triticum allopolyploids underwent downsizing, including the synthetic allopolyploids containing the S genome of Ae. speltoides (Eilam et al. 2008), as also shown by Salina et al. (2004), Han et al. (2005), who described elimination of repetitive sequences from genome S of Ae. speltoides in newly formed allopolyploids.
10.3.2.14.7.2 In Vitro DNA:DNA Hybridizations
To identify the donor of the B subgenome of the allopolyploid wheats, Nath et al. (1983, 1984) hybridized 3H-Triticum aestivum DNA to the unlabeled DNAs of the six putative donors of the B subgenome, namely, T. urartu, Ae. speltoides, Ae. sharonensis, Ae. bicornis, Ae. longissima, and Ae. searsii, and found that while the genome of T. urartu was more closely related to the A subgenome than to the B subgenome, that of Ae. searsii was most closely related to the B subgenome of T. aestivum. Consequently, they concluded that Ae. searsii was the B-subgenome donor to the allopolyploid wheats or a major chromosome donor, if the B subgenome is, in fact, polyphyletic in origin. Similarly, Thompson and Nath (1986) performed DNA:DNA hybridization between unique and repeated-sequence fractions of labeled T. turgidum ssp. durum DNA and the corresponding fractions of unlabeled DNAs of Ae. searsii, Ae. speltoides, Ae. longissima, Ae. sharonensis, and Ae. bicornis, and found Ae. searsii fractions to be the most closely related to the B subgenome of T. turgidum ssp. durum.
10.3.2.14.7.3 Evidence from RFLP Patterns of Genes Coding for rRNAs
Hybridization of total DNA from the tetraploid and hexaploid wheats, treated with the BamHl restriction enzyme, to a labelled 5S rRNA probe, showed that the repeating unit of the 5S rRNA genes comprise two fragments, 420- and 500-base pairs-long (Peacock et al. 1981). They found that the 420-base pair repeat unit was located on chromosome 1B. While neither T. monococcum nor Ae. speltoides contained the 420-base pair repeat unit, whereas Ae. longissima, Ae. sharonensis and Ae. searsii did. On this basis, they concluded that the 5S gene pattern excludes Ae. speltoides but is consistent with the other species of Sitopsis section, being closely related to the B subgenome.
A different conclusion was reached by Ruban and Badaeva (2018) who, using Giemsa C-banding and fluorescence in situ hybridization (FISH) with DNA probes representing 5S (pTa794) and 18S-5.8S-26S (pTa71) rDNAs, as well as the following nine tandem repeats: pSc119.2, pAesp_SAT86, Spelt-1, Spelt-52, pAs1, pTa-535, and pTa-s53, found that the B and G subgenomes of polyploid wheat are most closely related to the S genome of Ae. speltoides. Likewise, Zhang et al. (2002) cloned, sequenced and compared the internal transcribed spacer (ITS) sequences of nuclear rDNA of T. turgidum, T. timopheevii, and of the following diploid species, T. monococcum, T. urartu, the five Sitopsis species, and Ae. tauschii. Phylogenetic analysis demonstrated that the ITS sequences of Ae. speltoides, that were distinct from those of other Sitopsis species, were similar to the B and G subgenomes of the allotetraploid wheats.
Sallares and Brown (2004) amplified the entire 5′ external transcribed spacer (ETS) region of the 18S rRNA gene of all the diploid species of Aegilops and polyploid wheat. The phylogenetic analysis performed on the complete set of ETS sequences showed that the B and G subgenomes of tetraploid wheats form a clade with Ae. speltoides, in which the B subgenome diverged first and the G subgenome more recently.
10.3.2.14.7.4 Evidence from Hybridization with Single Copy Nuclear Genes
Petersen et al. (2006), using a sophisticated extension of the PCR technique, successfully isolated two single-copy nuclear genes, DMC1 and EF–G, from each of the three subgenomes of T. aestivum and from the two subgenomes of the tetraploid progenitor T. turgidum. Phylogenetic analysis of these sequences showed that the B subgenome derived from Ae. speltoides. The B subgenome donor was associated with a higher diversification rate of the B subgenome as compared to the diversification rate seen in A subgenome in the polyploid wheats. Petersen et al. (2006) extended the phylogenetic hypothesis suggesting that neither Triticum and Aegilops are monophyletic.
Daud and Gustafson (1996) cloned a genome-specific DNA sequence pSP89.XI from Ae. speltoides which was barely detected in any of the other Sitopsis genomes, while Southern blot analyses established that this sequence was present in the B subgenome of allotetraploid and allohexaploid wheat, though its relative abundance seemed to decrease at the allopolyploid levels. Hence, Daud and Gustafson (1996) concluded that the B subgenome derived from Ae. speltoides but that it was somewhat modified compared with that of modern Ae. speltoides.
Salse et al. (2008) compared sequences of the storage protein activator (SPA) locus region of the S genome of Ae. speltoides to those of the A, B and D subgenomes of hexaploid wheat. They concluded that the S genome of Ae. speltoides is more evolutionary related to the B subgenome of T. aestivum and had diverged very early from the progenitor of the B subgenome which remains to be identified.
10.3.2.14.7.5 Evidence from Hybridization with Repeated DNA Sequences
Flavell et al. (1979) found that the B subgenome of hexaploid wheat is highly enriched with repeated sequences homologous to those of Ae. speltoides, thus supporting the notion that the B subgenome of hexaploid wheat is closely related to an Ae. speltoides-like genome.
Dennis et al. (1980) isolated and hybridized a single highly repeated satellite DNA with chromosomes of various Triticum and Aegilops species and found that this satellite DNA hybridized to specific major sites in all B subgenome chromosomes, as well as to chromosomes 4A and 7A of T. aestivum. Observations of such in situ hybridization patterns in chromosomes of all putative B subgenome donors (except Ae. searsii) showed that none had a satellite distribution identical to that of the chromosomes of the B subgenome of hexaploid wheats. However, three chromosomes of Ae. longissima had a satellite distribution pattern similar to chromosomes those of 2B, 3B, and 5B in T. aestivum. Thus, Ae. longissima was selected as the most likely source of the B subgenome (Dennis et al. 1980). Peacock et al. (1981) extended these studies and found that Ae. tauschii, T. monococcum, and T. urartu had no major sites of hybridization, eliminating them as possible contributors to the B subgenome. They also showed that the diploid species with greatest similarity to the B subgenome of the allopolyploid wheats was Ae. longissima. On the other hand, whereas every chromosome in the complement of Ae. searsii possessed a specific pattern of major hybridization sites, the patterns did not resemble those of the B set of chromosomes of T. aestivum (Peacock et al. (1981). Dvorak and Zhang (1990) developed a general method, based on variation in repeated nucleotide sequences, for the identification of the diploid species most closely related to the B and G subgenomes of the allopolyploid wheats. Using this method, they demonstrated that Ae. speltoides is the most closely related species to both the B and G subgenomes of allotetraploid wheats.
10.3.2.14.7.6 Evidence from Cytoplasmic Analyses
Maan and Lucken (1967, 1968b, 1970) observed that hybrids derived from crosses between T. monococcum as female parent and T. turgidum and T. aestivum as male parents, were sterile males and lacked vigor. This led them to conclude that only the B subgenome donor could have contributed the cytoplasm to the allopolyploid wheats. Suemoto (1968), studying F1 hybrids and backcross derivatives of T. monococcum x T. turgidum and Ae. speltoides x T. turgidum, found that both pollen and seed fertility were significantly greater among the progeny of the latter cross, and consequently suggested that Ae. speltoides or a close relative in the Sitopsis section, was the female parent of T. turgidum. Fertile offspring were obtained after replacing the cytoplasms of T. turgidum and T. aestivum with cytoplasms of any of the Aegilops species from the Sitopsis section (Hirai and Tsunewaki 1981; Tsunewaki and Ogihara 1983). These studies confirmed Suemoto’s findings that the cytoplasm of the polyploid wheats was derived from a diploid Aegilops species of section Sitopsis.
Based on this conclusion, comparisons have been made between the cytoplasmic components of the allopolyploid wheats with those of T. monococcum, Ae. tauschii, and all the putative B subgenome donors from the Sitopsis section. Chen et al. (1975) determined the isoelectric points of the polypeptides comprising the large and small subunits of ribulose-1–5, biphosphate carboxylase-oxygenase (RuBisCO or fraction I protein). The small subunit was composed of one polypeptide chain and was coded for in the nuclear genome, whereas the large subunit was composed of three polypeptide chains encoded in the chloroplast genome. Isoelectric focusing of the polypeptides that comprise the large subunit revealed two patterns: T. aestivum, T. turgidum, and Ae. speltoides had an identical and higher isoelectric pattern, while T. monococcum, T. urartu, and Ae. tauschii had identical and lower isoelectric points. Thus, they concluded that T. turgidum is the female parent of T. aestivum and not Ae. tauschii. Moreover, the data indicated that neither T. monococcum nor T. urartu provided the genetic information for the large subunits in T. turgidum, thereby precluding both as the B subgenome donor and female parent of T. turgidum. On the other hand, the data unequivocally show that Ae. speltoides, or another species containing an identical large subunit pattern, was the B subgenome donor to T. turgidum. Hirai and Tsunewaki (1981) extended this study by using different alloplasmic lines, each of which contained the nuclear chromosome complement of T. aestivum and the cytoplasm from a specific Aegilops species in the Sitopsis section. Their results, supporting those of Chen et al. (1975), showed that the large subunit polypeptides of fraction 1 protein in alloplasmic lines containing Ae. speltoides or Ae. longissima cytoplasms had the same migration patterns (H type) as those of allopolyploid wheats. On the other hand, the large subunit polypeptides in the alloplasmic lines containing Ae. bicornis or Ae. sharonensis cytoplasms were of the L type found in T. monococcum, T. urartu, and Ae. tauschii. The authors concluded that either Ae. speltoides or Ae. longissima provided the cytoplasm to the allopolyploid wheats and, therefore, could have been the B subgenome donor to these species. Of note, Ae. searsii was not included in this study.
Comparison of the effect of various cytoplasms on several traits in euplasmic and alloplasmic lines (bearing the wheat nucleus in alien cytoplasm) made by Hori and Tsunewaki (1967), Suemoto (1968), Maan and Lucken (1971), and Tsunewaki et al. (1976, 1978), showed that the cytoplasm of several Sitopsis species can be considered the cytoplasm donor to the allopolyploid wheats. These results were supported by the results of Hirai and Tsunewaki (1981) regarding the Fraction I protein, as Ae. speltoides and Ae. longissima had a plasma gene encoding the H-type large subunit in all the polyploid wheats. Ae. bicornis and Ae. sharonensis could not have been the cytoplasm donor because they bear a plasma gene for the L-type large subunit.
Assuming that little divergence of potential B subgenome donors and the polyploid wheats has occurred since the origin of T. turgidum, several studies have compared the restriction fragment pattern of chloroplast DNA from the polyploid wheats with those of a number of Triticum and Aegilops species (Vedel et al. 1976; Ogihara and Tsunewaki 1982; Tsunewaki and Ogihara 1983). The most complete study reported to date has been that of Tsunewaki and Ogihara (1983), who used seven restriction enzymes. When compared to the chloroplast restriction fragment patterns of T. aestivum and T. turgidum, T. monococcum differed by 11 fragments, Ae. bicornis, Ae. searsii, and Ae. speltoides by 10 fragments and T. urartu by 8 fragments. Yet, the fragment pattern of chloroplast DNA from Ae. longissima was identical to those of T. turgidum and T. aestivum, prompting the authors to conclude that it is the most likely B subgenome donor.
Ogihara and Tsunewaki (1988), assessing variation in the chloroplast (cp) DNAs of 35 Triticum and Aegilops species, by analyzing restriction fragments that were obtained by applying 13 different restriction enzymes, classified the chloroplast genomes of these species into 16 types. This classification of cpDNAs was principally in agreement with that of the plasma types assigned according to phenotypes arising from nucleus-cytoplasm interactions. The chloroplast genome of the Aegilops diploid species of section Sitopsis separated into two distinct groups, one consisting of Ae. speltoides and the other comprising Ae. bicornis, Ae. sharonensis and Ae. searsii (Ae. longissima was not included in this study). The speltoides cpDNA was closely related to the that of T. timopheevii and T. aestivum, but somewhat more distant from the latter. Similar results were obtained by Miyashita et al. (1994), who, using a battery of four-cutter restriction enzymes, investigated restriction map variation in two 5–6-kb chloroplast DNA regions of the five Sitopsis species and of two wild allotetraploid wheats, T. turgidum ssp. dicoccoides and T. timopheevii ssp. armeniacum, as well as a single accession each of T. turgidum ssp. durum, T. timopheevii ssp. timopheevii and T. aestivum ssp. aestivum. Whereas low polymorphism was found in Ae. speltoides, no restriction site polymorphisms were detected in any of the other diploid and allopolyploid species. One accession of Ae. speltoides had a plastotype identical to those of wild and domesticated T. timopheevii. On the other hand, no diploid species had the plastotype of T. turgidum. Three of the plastotypes found in the Sitopsis species were very similar, but not identical, to those of T. turgidum and T. aestivum. It was concluded that T. timopheevii and T. turgidum have a diphyletic origin, evolving at different times and originating from two different, but closely related, maternal parents.
Provan et al. (2004) utilized polymorphic chloroplast microsatellites to analyze cytoplasmic relationships between Triticum and Aegilops species. Phylogenetic analyses revealed three distinct groups of accessions; one group contained all the non-Ae. speltoides S-type cytoplasm species, another comprised almost exclusively A, C, D, M, N, T and U cytoplasm-type accessions, and the third contained the allopolyploid Triticum species and all the Ae. speltoides accessions. These results further confirm that Ae. speltoides, or a closely related species, was the original B subgenome donor of allopolyploid wheat. Similarly, Haider (2012) compared the polymorphism of chloroplast DNA between T. aestivum and 8 different Aegilops species, using cleaved amplified polymorphic sequence (CAPS) and sequencing of 28 chloroplast loci and concluded that Ae. speltoides is B subgenome and the cytoplasm donor to T. aestivum.
Studies of mitochondrial (mt) DNA variation in Triticum and Aegilops may provide a sensitive assay for assessing cytoplasmic relationships between the diploid Triticum and Aegilops species and the allopolyploid wheats. Breiman (1987) found that the Sitopsis species exhibited wide intra- and inter-specific variation, with Ae. speltoides showing the most extensive intraspecific diversity, whereas no variation was detected among the cytoplasms of the allopolyploid Triticum species sharing the BBAA genome. In an attempt to identify the donor of the B subgenome to T. turgidum and T. aestivum, the restriction endonuclease profiles of two regions around the mitochondrial cytochrome oxidase subunit I gene were compared with those of Ae. speltoides, Ae. bicornis, Ae. sharonensis, Ae. longissima, Ae. searsii, Ae. tauschii and T. monococcum (Graur et al. 1989). The results indicated that none of these diploid species were likely to have either donated the B subgenome or to be closely related to the donor.
Terachi et al. (1990) examined the mitochondrial genomes of three Sitopsis species (Ae. bicornis, Ae. sharonensis, and Ae. speltoides), three subspecies of T. turgidum (dicoccoides, dicoccon, and durum), three subspecies of T. aestivum (spelta, aestivum, and compactum), two subspecies of the timopheevii group (armeniacum and timopheevii), and the species T. zhukovskyi. mtDNAs from the subspecies dicoccon, durum, aestivum, and compactum yielded identical restriction fragment patterns which differed from those of the subspecies dicoccoides and spelta in only 2.3% of their fragments. The fragment patterns of ssp. timopheevii and T. zhukovskyi were identical, and both differed from the ssp. armeniacum mtDNA pattern by only one fragment. The differences in the mitochondrial genome of T. turgidum and T. aestivum from those of T. timopheevii and T. zhukovskyi suggest a diphyletic origin of the two groups. Whereas the mtDNAs of Ae. bicornis, Ae. sharonensis, and Ae. searsii were relatively similar, that of Ae. speltoides differed greatly from the other three, and was identical, or nearly so, to the mtDNAs of T. timopheevii and T. zhukovskyi. Terachi et al. (1990) could not determine with precision the cytoplasm donor to T. turgidum and T. aestivum, as their results revealed that the ctDNA underwent smaller evolutionary divergence than the mtDNAs from these same accessions.
To investigate phylogenetic relationships among plasmons (the whole cytoplasmic genome) in Triticum and Aegilops, Wang et al. (1997), performed PCR–single-strand conformational polymorphism (PCR-SSCP) analyses on 14.0-kb chloroplast and 13.7-kb mitochondrial DNA regions isolated from 46 alloplasmic wheat lines and one euplasmic line. The phylogenetic trees of plasmons indicated Ae. speltoides as the cytoplasm donor to the allopolyploid wheat, suggesting that this species is the B and G subgenomes donor of all allopolyploid wheats. Mori et al. (1997) studied variation in mitochondrial DNA of Triticum and Aegilops species by PCR-aided RFLP analysis of a 1.3 kb region containing the intron of coxll. All but one accession of Ae. speltoides possessed a haplotype common to T. timopheevii wheat, thus supporting the hypothesis that Ae. speltoides donated the G subgenome to T. timopheevii. However, these findings did not agree with the hypothesis that Ae. speltoides was the B subgenome donor to the allotetraploid and allohexaploid wheats.
Gornicki et al. (2014) sequenced 25 chloroplast genomes and genotyped 1127 accessions of 13 Triticum and Aegilops species. They found that Ae. speltoides diverged before the divergence of T. urartu, Ae. tauschii and the Aegilops species of section Sitopsis. Ae. speltoides had formed a monophyletic clade with the allopolyploids T. turgidum and T. timopheevii, which originated within the last 0.7 and 0.4 million years ago, respectively. The geographic distribution of chloroplast haplotypes of the wild tetraploid wheats and Ae. speltoides illustrates the possible geographic origin of wild T. turgidum in the southern Levant and of wild T. timopheevii in northern Iraq. Chloroplast haplotypes were often shared by species or subspecies within major allopolyploid lineages and between the lineages, indicating the contribution of introgression to the evolution of the allopolyploid wheats.
10.3.2.14.7.7 Concluding Remarks on the Origin of the B Subgenome
As seen from the above data, the identification of the donor of the B subgenome to allopolyploid wheats has so far lacking conclusive results, despite the many attempts that were made during the last century to identify the diploid donor(s) of the B subgenome of the allopolyploid wheats. The morphological, geographical, cytological, genetic, and molecular data reviewed above implied that one of the species of Aegilops section Sitopsis, can be the donor of the B subgenome albeit unequivocally. Indeed, over the years, all five species of section Sitopsis have been proposed, by various authors, as the putative donors of the B subgenome to T. turgidum and T. aestivum.
As was pointed out by Kerby and Kuspira (1987), already Sarkar and Stebbins (1956), Sears (1948) ascribed these failures to the great antiquity of wild T. turgidum and hence, to the many changes that must have occurred in the B subgenome since its incorporation into the allotetraploid. Chromosomal and genetic changes could have also occurred in the diploid donor of the B subgenome since its hybridization with T. urartu.
On the other hand, evidence for a polyphyletic origin of the B subgenome was presented by Giorgi and Bozzini (1969a) on the basis of karyotype analysis, by Vittozzi and Silano (1976) from studies of enzyme systems, and by Dennis et al. (1980) on the basis of satellite distribution patterns. Support for such an origin of the B subgenome was also obtained from isozyme studies by Nishikawa (1983). His results implied that chromosome 6B of allohexaploid wheat derived from Ae. longissima and 7B from Ae. speltoides. Further evidence for a recombinant B subgenome was presented by Nishikawa et al. (1992), suggesting that the B subgenome of T. turgidum and T. aestivum is a recombinant subgenome, comprising segments that derived from various Sitopsis species. Chromosomes 2B and 3B contain segments of Ae. longissima (Gerlach et al. 1979), and chromosome 3B also has segments of Ae. speltoides (Vittozzi and Silano 1976; Jaaska 1980). Chromosome 4B (formerly 4A) derived from Ae. speltoides (Dvorak 1983; Chen and Gill 1983), and contains segments from Ae. sharonensis (Rayburn and Gill 1985). Chromosome 5B contains segments from Ae. longissima (Gerlach et al. 1979), and Ae. speltoides (Jaaska 1978). The long arm of chromosome 6B derived from Ae. longissima (Nishikawa 1983), and contains segments from Ae. sharonensis or Ae. bicornis and Ae. speltoides (Nishikawa et al. 1992). The long arm of chromosome 7B derived from Ae. speltoides (Nishikawa 1983; Nishikawa et al. 1992) and contains segments from Ae. sharonensis or Ae. searsii (Nishikawa et al. 1992). Similarly, Zhang et al. (2017), using an integrative cytogenetic and genomic approach, assessed the homology of the wheat B subgenome with the S genome of Ae. speltoides and revealed noticeable homology between wheat chromosome 1B and Ae. speltoides chromosome 1S, but not between other chromosomes in the B subgenome and S genome. Evidently, Ae. speltoides had been involved in the origin of the wheat B subgenome but should not be considered an exclusive donor of the subgenome. To elucidate the origin of wheat B subgenome, Kong et al. (Kong XY, Dong YS, Jia JZ, personal communication) isolated four B subgenome-specific repetitive sequences from T. turgidum ssp. dicoccon. A Southern hybridization analysis with these clones showed that four species, Ae. speltoides, Ae. longissima, Ae. sharonensis and Ae. searsii, contained different B subgenome-specific repetitive sequences. Hence, their results implied that the B-subgenome of allopolyploid wheat is a recombined subgenome comprising chromosomal segments from several Sitopsis species. Thus, one possibility to explain the above data is to assume that the wheat B subgenome might have a polyphyletic origin with multiple ancestors involved.
Blake et al. (1999) used the B subgenome of allopolyploid wheat as a model system to test hypotheses that bear on the monophyly or polyphyly of the individual constituent subgenomes. By using aneuploid wheat stocks, combined with PCR-based cloning strategies, they cloned and sequenced two single-copy DNA sequences from each of the seven chromosomes of the wheat B subgenome and the homologous sequences from representatives of the five diploid species in section Sitopsis. Phylogenetic comparisons of sequence data suggested that the B subgenome of wheat diverged from a diploid B subgenome donor. The extent of genetic diversity among the Sitopsis diploids and the failure of any of the Sitopsis species to group with the wheat B subgenome, indicated that these species also diverged from the ancestral B subgenome donor. Their results support monophyletic origin of the wheat B subgenome.
Thus, a plausible possibility therefore, is that the B-subgenome donor is a distinct diploid species different from the current Sitopsis species, which is either extinct or extant that still remain to be discovered (Feldman et al. 1995). The genome of this species is closely related to that of Ae. speltoides and other Sitopsis species, and it was estimated, based on whole genome sequencing of Sitopsis species, to have diverged from the S genome of Ae speltoides ~ 4.49 (4.31–4.67) MYA (Li et al. 2022) and to have introgressed with the Sitopsis species of the D-lineage before its hybridization with T. urartu leading to formation of T. turgidum. Hence, hybridization between the B subgenome donor as female and T. urartu as male, 700,000–900,000 years ago (Gornicki et al. 2014; Marcussen et al. 2014; Middleton et al. 2014), led to the formation of wild emmer T. turgidum ssp. dicoccoides. That such allopolyploidization occurred over and over again is conceivable, possibly involving somewhat different genotypes of the concerned diploid parents. The accumulated cytogenetic and molecular evidence has indicated that assumption of genome stability, that is, that the genomes of the allopolyploid species remain similar to those of their diploid parents, is not always correct, and that subgenome(s) may undergo considerable changes at the polyploid level. Indeed, the formation of allotetraploid wheat was followed by revolutionary (occurring during allopolyploid formation) and evolutionary (occurring during the life of the allopolyploid) genetic, and epigenetic changes that brought about cytological and genetic diploidization (Feldman et al. 1997; Liu et al. 1998a, b; Ozkan et al. 2001, 2002; Shaked et al. 2001; Kashkush et al. 2002, 2003; Salina et al. 2004; Han et al. 2003, 2005; Ma and Gustafson 2005, 2006; Baum and Feldman 2010; Guo and Han 2014; Cheng et al. 2019) as well as introgression with other diploid and allopolyploid species (Zohary and Feldman, 1962; Vardi 1973; Rao and Smith 1968; Rawal and Harlan 1975; Gornicki et al. 2014; El-Baidouri et al. 2017: Glemin et al. 2019; Bernhardt et al. 2020).
10.3.2.15 DNA Content of T. turgidum
The subspecies of T. turgidum contained from 12.52 to 12.91 pg 1C DNA (Eilam et al. 2008). Sixteen ssp. dicoccoides accessions (35 plants) had a mean 12.91 ± 0.194 pg 1C DNA; the three ssp. dicoccon cultivars (8 plants) analyzed had mean 1C DNA content of 12.87 ± 0.093 pg, the eleven ssp. durum cultivars (22 plants) analyzed had a mean 1C DNA content of 12.84 ± 0.175 pg, the one ssp. polonicum cultivar (2 plants) analyzed had a mean 1C DNA content of 12.52 pg, the two ssp. turgidum cultivars (4 plants) analyzed had a mean 1C DNA content of 12.75 ± 0.085 pg and the one in ssp. carthlicum cultivar (3 plants) analyzed had a mean 1C DNA content of 12.87 pg. Domestication seemingly had no effect on genome size in this species. The genome of T. turgidum is larger than the genomes of T. timopheevii and of most Aegilops allopolyploids (Eilam et al. 2008). The DNA content reported for T. turgidum by Eilam et al. (2008) is in accord with the findings of Rees (1963) and Rees and Walters (1965), who determined DNA content in tetraploid wheats and found significantly less nuclear DNA in T. timopheevii as compared to T. turgidum ssp. durum. The 1C DNA content of T. turgidum is significantly larger than the additive amount of 1C DNA of Ae. speltoides (5.81 pg), and T. urartu (6.02 pg) (Eilam et al. 2007). On the other hand, the amount of DNA in T. turgidum is about equal to the sum of the amphiploids of any of the other four Sitopsis species together with T. urartu, i.e., Ae. bicornis 6.84 pg, Ae. searsii 6.65 pg, Ae. longissima 7.48 pg, Ae. sharonensis 7.52 pg and T. urartu 6.02 pg (Eilam et al. 2007). It is deduced therefore, that 1C DNA amount of the B-subgenome donor was around 7.50 pg. Estimates of genome size in the Sitopsis from whole genome sequences (Avni et al. 2022) are in same range as those of Eilam et al. (2007; Table 9.3) while those of Li et al. (2022) are a bit lower.
Similar results were obtained by Furuta et al. (1984), who determined the DNA content of the three subgenomes of hexaploid wheat by summing the DNA contents of the seven individual chromosomes of each subgenome. They found that the DNA content of the B subgenome was significantly higher than those of the A and D subgenomes, and that the nuclear DNA content of Ae. speltoides is only about 87% of that of the B subgenome of hexaploid wheat. On the other hand, the DNA contents of Ae. bicornis, Ae. searsii, Ae. longissima, and Ae. sharonensis were comparable to that of the B subgenome (Furuta et al. 1984). This was consistent with the results they obtained for the synthetic allotetraploids T. monococcum—Ae. longissima, T. monococcum—Ae. sharonensis, and T. monococcum—Ae. bicornis. All three synthetic allotetraploids had DNA content very similar to that of natural T. turgidum.
10.3.2.16 Chromosome Morphology
The different subgenomes of T. turgidum are composed of chromosomes with median or submedian centromeres, which lack distinctive morphological features (Riley et al. 1958). For this reason, there are no distinct diagnostic markers in the chromosome complement of this species, except for the satellited (SAT) chromosomes and some differences in total length and, to some extent, in arm length ratios.
Kagawa (1929), one of the first cytologists to study chromosome morphology of domesticated emmer, T. turgidum ssp. dicoccon, observed that its genome in mitotic metaphase consisted of two different chromosomal sets which were designated A and B by Kihara (1924). Kagawa recognized ten chromosome types in this subspecies, seven of which were with secondary constrictions. Bhatia (1938) found that the morphology of all the chromosomes in ssp. dicoccon was quite clear, and that the homologous pairs were easily recognizable. In contrast to Kagawa, Bhatia observed only two chromosome pairs that were satellited, and which differed in their morphology from one another. Of the remaining 24 chromosomes, 22 chromosomes had only one constriction each and the remaining pair had two constrictions each. All the 28 chromosomes fell into fourteen pairs and no two pairs were alike in the position of the centromere. Pathak (1940) observed two pairs of satellited chromosomes in T. turgidum ssp. durum. Similarly, Waines and Kimber (1973) observed in one line of wild emmer, T. turgidum ssp. dicoccoides, two pairs of SAT chromosomes. Morrison (1953) identified the two satellited pairs most commonly observed as chromosomes I and X of Chinese Spring (the old designation system of bread wheat chromosomes; Sears 1954). Okamoto (1957b, 1962) confirmed that both of these chromosomes belong to the B subgenome; chromosome I was identified as 1B and chromosome X as 6B (Okamoto 1957b).
Riley et al. (1958) noted that the short arm of chromosome 1B carried the smallest satellite and was larger than the second SAT chromosome and more hetero-brachial, whereas the short arm of chromosome 6B carried the longer satellite and was shorter than 1B. The satellites of chromosome 1B were less than 1/3 the length of the adjacent arm, whereas, in 6B, the satellites were 1/3 to ½ the length of the adjacent arm. Similarly, Coucoli and Skorda (1966) analyzing the karyotype of T. turgidum ssp. durum var. leucurum, found two pairs of satellited chromosomes. But, in contrast to what was found by Riley et al. (1958), Coucoli and Skorda (1966) reported that the longer SAT pair, on chromosome 6B, also had the longest satellite (2.29 µ), corresponding to approximately 1/5 of the total chromosome length and less than the half of the adjacent short arm. The SAT pair on chromosome 1B possessed the shorter satellite (approximately 1/7 the total length), which is almost equal to one third of the adjacent short arm and was more heterobrachial. Chromosomes length was found to range from 12.97 µ (the longest pair) to 8.80 µ (the shortest). All chromosomes of ssp. durum are metacentric or sub-metacentric, but more hetero-brachial chromosomes are present in the genome of ssp. durum than in T. monococcum.
Giorgi and Bozzini (1969a) performed a detailed analysis of the karyotypes of several subspecies, cultivars and varieties of T. turgidum, including ssp. durum (cvs. Cappelli and Aziziah), ssp. dicoccoides, ssp. dicoccon, ssp. aethiopicum Jakubz. (currently a variety of ssp. durum), ssp. carthlicum, ssp. turgidum (var. plinianum) and ssp. ispahanicum (currently a variety of ssp. dicoccon). Analyzing mitotic metaphase in root-tip cells, they showed that all the studied taxa had a basically similar karyotype. They then classified the chromosomes of T. turgidum as follows: (i) Two satellited (SAT) chromosomes, SAT1, presumably on chromosome 1B, can be distinguished from SAT2, presumably on chromosome 6B, mainly due to its shorter satellite and greater arm ratio. (ii) Two subterminal (ST) chromosomes, one is a little longer and with a slightly more subterminal centromere than the second. (iii) seven submedian (SM) chromosomes (of which some are nearly median, while others are almost subterminal. SM 7 is the shortest submedian chromosome in the complement and has the highest arm ratio in the group, which makes it easily distinguishable. (iv) Three median (M) chromosomes of which one, M1, is the longest, usually slightly submedian and, therefore, sometimes difficult to separate from submedian chromosomes. Chromosome M2 is invariably a true median chromosome, shorter than M1. Chromosome M3 is the shortest in the M group. Chromosomes of this group are fairly easily distinguishable. In summary, at least 6 out of the 14 chromosome pairs present in T. turgidum are distinguishable with sufficient accuracy (SAT1 and SAT2, SM7, and M1, M2 and M3).
The measurement of B and A subgenome chromosome length in the common wheat cultivar Chinese Spring (Sears 1954; see Sect. 10.4.2.8 in Chap. 10) indicated that B subgenome chromosomes are longer than A chromosomes (total subgenome length is 43.65 µ vs. 41.01 µ, respectively, with an average chromosome length of 6.24 µ vs. 5.86 µ, respectively). Chromosome 3B is the longest and 2B is the shortest in the B subgenome, whereas chromosome 2A is the longest and 1A is the shortest in the A subgenome. Chromosome 5B is the most brachial (arm ratio 2.65:1) and 6B is the least brachial, almost metacentric, in the B subgenome (arm ratio 1.05:1), while chromosome 1A is the most brachial (arm ratio 1.91:1) and 6A the least brachial (arm ratio 1.12:1) in the A subgenome. Sasaki et al. (1963) measured chromosome length in the bread wheat cv. Cheyenne, and Gill et al. (1963 in cv. Wichita and their results sustain, for the most part, those of Sears (1954). In all three studies, chromosomes 1B and 6B were found to carry satellites on their short arm.
As most chromosomes of all subspecies of T. turgidum, as well as all other wheat species, lack morphological features, it was necessary to look for other means of identifying individual chromosomes. This necessity has led to the development of chromosome banding techniques, especially Giemsa C-banding and N-banding, that facilitated the identification of individual chromosomes in diploid, allotetraploid and allohexaploid wheats, and thus, has advanced cytogenetic studies in wheat and related species (Gill 1987). In addition to chromosome size, centromere position and arm ratio, the position, size, and intensity of individual C- or N-bands are also important criteria for chromosome identification.
The Giemsa stain interacts specifically with constitutive heterochromatin and thus, the C-bands expose the position of this type of chromatin in the chromosomes. The dark (stained) bands and light (unstained) bands represent heterochromatic and euchromatic regions, respectively (Gill 1987). The C-banding technique stains all classes of constitutive heterochromatin and identifies each of the 21 chromosomes in T. aestivum (Endo and Gill 1984), and each of the 14 chromosomes of T. turgidum (Seal 1982; Bebeli and Kaltsikes 1985; Badaeva et al. 2015).
As in T. aestivum (Endo and Gill 1984), subgenome B in T. turgidum is also more heavily banded than subgenome A; chromosomes 1B, 3B, 5B, 6B and 7B of the B subgenome and chromosome 4A of the A subgenome are most heavily banded in durum wheat (Seal 1982; Bebeli and Kaltsikes 1985; Badaeva et al. 2015). The bands in both A and B subgenomes were concentrated in the centromeric, distal and terminal regions. Yet, there is widespread banding polymorphism among different lines of wild and domesticated T. turgidum (Badaeva et al. 2015). For example, these authors found that karyotypes of wild and domesticated emmer showed an extremely high diversity of C-banding patterns. B subgenome chromosomes were more polymorphic than A subgenome chromosomes. The lowest diversity of C-banding patterns was found for chromosome 3A, while chromosomes 2A and 4A proved to be most variable among the A subgenome chromosomes. On the B subgenome, the lowest polymorphism was observed for chromosome 4B and the highest, for chromosomes 3B and 7B, respectively.
The C-banding method has been used in studies of several aspects of cytogenetics and evolution of T. turgidum. For example, using C-bands, Seal (1982) identified all 14 T. turgidum chromosome pairs in hexaploid triticales (genome BBAARR). Similarly, Bebeli and Kaltsikes (1985) constructed the karyotypes of Capeiti and Mexicali, two durum wheat cultivars, on the basis of C-banding of their chromosomes.
In contrast to C-banding, the N-banding technique specifically reveals heterochromatin containing polypyrimidine DNA sequences (Dennis et al. 1980). Nine of the 21 chromosome pairs of the hexaploid wheat Triticum aestivum cv. Chinese Spring showed distinctive N-banding patterns (Gerlach 1977). These nine chromosomes were 4A, 7A and all of the B subgenome chromosomes. The remaining chromosomes showed either faint bands or no bands at all. Wild tetraploid wheat, T. turgidum ssp. dicoccoides, showed banded chromosomes similar to those observed in the A and B subgenomes of hexaploid wheat. Of the diploid species, only Ae. speltoides had several N-banded chromosomes similar to, but somewhat different than those of the B subgenome. Endo and Gill (1984) identified 16 of the 21 chromosomes of common wheat using an improved N-banding technique.
C-banding has been used quite extensively in the identification of intraspecific chromosomal rearrangements in the different subspecies of T. turgidum (Badaeva et al. 2007, 2015, 2019). During a C-banding survey of a large collection of cultivars of domesticated emmer, ssp. dicoccon, Rodríguez et al. (2000b), Badaeva et al. (2015) identified different types of chromosomal rearrangements, some of which were novel to T. turgidum. Chromosomal rearrangements were represented by single translocations and or multiple translocations, as well as by paracentric and pericentric inversions. The use of C-banding enabled the detection of the position of translocation breakpoints, which was either at or near the centromere, or interstitial. Centromeric translocations significantly prevailed in tetraploid wheat (Badaeva et al. 2015).
Use of the C-banding technique in the identification of individual chromosomes and chromosome arms at first meiotic metaphase of F1 hybrids involving T. turgidum and related species, enabled determination of the type of pairing of each T. turgidum arm, i.e., homologous versus homoeologous pairing. Thus, for example, Naranjo (1990) analyzed meiotic pairing in the hybrid tetraploid triticale (genome BARR x rye) and identified the arm homoeology of A-B chromosomes of T. turgidum using the C-banding technique. Results confirmed that the homoeologous relationships between chromosome arms of the A and B subgenomes in T. turgidum are the same as in T. aestivum, and that a double translocation involving 4AL, 5AL, and 7BS, and a pericentric inversion involving a substantial portion of chromosome 4A, are present in T. turgidum as in T. aestivum.
C-banding was also applied in T. turgidum to determine the approximate location of the Ph gene in the 5BL arm. Dvorak et al. (1984) C-banded the long arm of chromosome 5B of a mutant line of the Italian cultivar Cappelli of T. turgidum ssp. durum deficient for the Ph gene and of another Cappelli line bearing a duplication of part of the long arm of 5B that carries Ph. Compared with arm 5BL of the parental cultivar, the 5B long arm of the Ph mutant was shorter, owing to a deletion of one of two inter-band regions in the middle of the arm. In the line suspected to have a duplication, the 5BL arm was longer than in Cappelli and the interband region that was absent in the Ph mutant was twice as long.
Genetic mapping of polymorphic C-bands also enables direct comparisons between genetic and physical maps (Curtis and Lukaszewski 1991). More specifically, Curtis and Lukaszewski used eleven C-bands and two seed storage protein genes on chromosome 1B, polymorphic between Langdon durum and four accessions of ssp. dicoccoides, to study the distribution of recombination along the entire length of the chromosome. The genetic maps obtained from the four individual T. dicoccoides chromosomes were combined to yield a consensus map of 14 markers (including the centromere) for chromosome 1B.
10.3.2.17 Development and Use of Aneuploid Lines in Durum Wheat
Several series of aneuploid lines were produced in T. turgidum ssp. durum cultivar Langdon by Joppa and colleagues (Joppa 1987, 1993). These aneuploids have been used to identify and locate genes on chromosomes, to map gene-to-centromere distances, to transfer chromosomes from one cultivar or species to another, and to identify chromosome homoeology (Joppa 1987). In contrast to hexaploid aneuploids that were produced in the 50 s of the previous century (Sears 1954), aneuploids in the tetraploid T. turgidum only became available during the late 1970s. Several kinds of aneuploids are not vigorous and fertile in tetraploid wheat, particularly those with reduced chromosomes number, i.e., monosomes, monotelosomes and nullisomes. On the other hand, increases in chromosome numbers in the form of trisomics, is tolerated in tetraploid wheat. Indeed, a complete set of primary trisomics that are vigorous and fertile was developed in the Italian durum cultivar Cappelli by Simeone et al. (1983).
A complete set of double-ditelosomics, dimono-telosomics for the A and B subgenome chromosomes has been developed in cultivar Langdon of durum wheat (Joppa 1987, 1993; Joppa and Williams 1988). These lines are fully fertile and vigorous and resemble Langdon in morphology. The lines have been used to identify chromosome substitutions.
Sears (1966) classified the chromosomes of hexaploid wheat into seven homoeologous groups and showed that the chromosomes of different subgenomes within the same group can compensate for each other in nullisomic-tetrasomic combinations. Thus, for example, four doses of chromosome 1D compensated for the absence of 1A or 1B. Joppa (1987, 1993), Joppa and Williams (1988) developed a more useful material for cytogenetic and genetic analyses in tetraploid wheat, namely, disomic substitutions, in which a pair of chromosomes of another subspecies of tetraploid wheat or of the D subgenome of hexaploid wheat, substituted for a homoeologous durum pair. Such inter-cultivar chromosome substitution lines, D-subgenome disomic substitutions and also homozygous recombinant lines were produced in the durum cultivar Langdon.
Joppa and colleagues produced complete sets of 14 different disomic-substitution lines bearing D subgenome chromosomes of hexaploid wheat or A and B subgenome chromosomes of several subspecies of T. turgidum, which substituted their durum homoeologues or homologues, respectively. These lines enabled the evaluation of the genetic contribution of each of the substituted chromosomes on the genetic background of durum, as well as identification of useful genes and their location on specific chromosomes (Joppa and Williams 1983; Joppa and Cantrell 1990; Cantrell and Joppa 1991; Joppa et al. 1991).
10.3.2.18 Crosses with Other Species of the Wheat Group
Chromosome pairing at first meiotic metaphase of F1 hybrids between wild and several domesticated subspecies of T. turgidum is complete, or practically so, exhibiting 14 bivalents, or close to this value, per pollen mother cell (PMC) (Table 10.8). This pattern of pairing implies that the chromosomes of the wild and domesticated subspecies of T. turgidum are homologous and that domestication did not cause any conspicuous genomic changes. The existence of reciprocal translocations between accessions of wild emmer (Rao and Smith 1968; Rawal and Harlan 1975; Kawahara and Tanaka 1978, 1981, 1983; Kawahara 1984, 1986, 1987; Joppa et al. 1995; Badaeva et al. 2007, 2015) is not sufficient for setting up a genetic barrier(s) and preventing gene flow between them.
Hybrids between T. turgidum and the wild and domesticated subspecies of diploid wheat, T. monococcum, (hybrids genome BAAm), had approximately 4.61–5.70 bivalents per PMC (Table 10.9), indicating that one of the two subgenomes of T. turgidum, i.e., subgenome A, is close but not fully homologous with the Am genome of T. monococcum. The F1 hybrid between T. turgidum ssp. dicoccon and the second diploid wheat, T. urartu (hybrid genome BAA), had somewhat higher pairing (6.10 bivalent per PMC; Table 10.8), but, still, subgenome A of the tetraploid albeit close to but not completely homologous with the A genome of T. urartu.
Hybrids between wild and domesticated T. turgidum and wild and domesticated T. timopheevii (hybrids genome BAGA) exhibited reduced chromosome pairing at first meiotic metaphase (Table 10.8). This pattern of pairing showed that the two allotetraploid wheats share one subgenome and differ in the second subgenome. However, the more than 7 bivalents that existed in these hybrids indicate that sporadic hybridization between these two allotetraploid species and backcross to one of the parents can produce progeny with recombinant B/G subgenomes. Indeed, such recombinant subgenomes were found in natural population where the two species grows sympatrically (Sachs 1953; Rao and Smith 1968; Wagenaar 1966).
Hybrids between domesticated T. turgidum ssp. durum and T. aestivum ssp. aestivum (hybrid genome BABAD) exhibited almost 14 bivalents or 12 bivalents and one translocation (Table 10.8), indicating that the two allopolyploid species share two subgenomes and that the allohexaploid contains an additional non-homologous subgenome.
Hybrids between wild and domesticated subspecies of T. turgidum with three species of Aegilops section Sitopsis, namely, Ae. bicornis, Ae. sharonensis, and Ae. longissima, showed very little pairing at meiotic first metaphase, with between 0.00 and 2.50 bivalents per PMC (Table 9.9). This very low pairing indicates either that there is no homology between the subgenomes of the allotetraploid wheat and the genomes of these three Sitopsis species or, alternatively, that these species contain a gene(s) that, together with ph1 of T. turgidum, suppresses homoeologous pairing (Feldman 1978). On the other hand, there are two types of hybrids between T. turgidum and Ae. speltoides, the first, involving the high-pairing type of Ae. speltoides, had higher pairing than the second hybrid with the low-pairing type of Ae. speltoides (Table 9.9). Evidently, the high-pairing genotype of Ae. speltoides carries a gene(s) that promotes homoeologous pairing, even in the presence of the wheat Ph1. Hybrids between wild T. turgidum and Ae. tauschii (hybrid genome BAD) had very little pairing, 0.0–3.0 bivalents per PMC (Table 9.9) indicating no homology between the subgenomes of T. turgidum and the genome of Ae. tauschii.
10.3.3 T. timopheevii (Zhuk.) Zhuk. (Genome GGAA)
10.3.3.1 Description of the Species
Triticum timopheevii (Zhuk.) Zhuk., commonly known as timopheev’s wheat [Syn.: T. dicoccoides Körn. var. timopheevii Zhuk.; T. dicoccoides Körn. subsp. armeniacum Jakubz.; T. turgidum L. var. timopheevii Zhuk.; T. turgidum L. var. timopheevii (Zhuk.) Bowden; T. turgidum var. tumanianii (Jakubz.) Bowden; T. dicoccoides var. nudiglumis Nabalek; T. araraticum Jakubz.; T. armeniacum (Jakubz.) Magush. & Dorof.; T. chaldicum Menabde; T. miguschovae Zhirov; T. timonovum Heslot & Ferrary; Gigachilon timopheevii (Zhuk.) Á. Löve] is an annual, predominantly autogamous, 70–90(–100)-cm-tall (excluding spikes) plant. Culms are erect. The entire plant is clothed with stiff hairs which can be up to 3-mm-long on the leaf sheaths. Leaf blades are 20–45–cm-long, and hairy on both sides. The spike is indeterminate, strongly bilaterally compressed, two-rowed, 8–12-cm-long (excluding awns), ovoid, tapering to both the base and tip, hairy and awned. In the wild form, the entire spike disarticulates into individual spikelets at maturity, each with its associated rachis segment (wedge-type dispersal unit), while in the domesticated form, the rachis is not fragile and consequently, the spike remains intact on the culm. In both subspecies, wild armeniacum and domesticated timopheevii, the rachis internodes are covered with dense, white hairs and the spikelets are compressed and ovoid, with the top spikelet being fertile and generally in the same plane as those below. There are 8–15 spikelets per spike, and the 2–3 basal spikelets are rudimentary. The fertile spikelet is 10–12-mm-long and has 3 florets, the upper one usually being sterile. The glumes are similar to one another, 7–10-mm-long, very hairy, with 2 keels and 5–9 veins, and with two teeth on the upper margin, one larger and pointed and separated from the other by an acute angle. Lemma is elliptic, hairy, 10–12-mm-long, without keels, and with 9–11 veins, and features a central vein prolonged as a narrow 50–60(–90)-mm-long awn. In addition to awn, the lemma has a lateral tooth. At maturity, the palea is membranous and split along the keel. Usually, there are two grains per spikelet. The plant is caryopsis-free but adhered to the lemma and palea (hulled type). It is laterally compressed, and hairy at the apex (Fig. 10.6).
Plants and spikes of allopolyploid species of Triticum with the G subgenome; a T. timopheevii (Zhuk.) Zhuk. ssp. armeniacum (Jakubz.) van Slageren (wild timopheevii); b T. timopheevii ssp. timopheevii (Zhuk.) Löve and Löve (domesticated timopheevii)
Wild T. timopheevii was discovered several years after the discovery of wild T. turgidum. In 1910, Theodor Strauss, a botanist who served as the British vice-consul in Sultanabad, Iran, found several specimens of two-grained wild wheat in Noa-kuh, near the city of Kerind, in the mountainous region of western Iran. Schulz (1913a) identified the material collected by Strauss as T. dicoccoides (Kcke) form. Straussiana, distinguishing it from the Syrio-Palestinian two-grained wild wheat, which he named T. dicoccoides (Kcke) form. kotschyana. Schulz assumed that dicoccoides had a continuous range from the Hermon region in northern Israel to Iran, via eastern Turkey.
In 1923, Zhukovsky found a unique form of hulled, two-grained, domesticated wheat in western Georgia. He first classified it as T. dicoccon Schr. ssp. timopheevii Zhuk. (Zhukovsky 1923), but in 1928, he raised this taxon to the species rank and termed it T. timopheevii (Zhuk.) Zhuk. (Zhukovsky 1928b). Wild timopheevii was collected by M. G. Tumanyan and A. G. Araratyan in 1928 southeast of Erevan, Armenia, and in 1932 in several other locations in Armenia, Azerbaijan, Iran, Iraq, and Turkey (Jakubziner 1932b, 1959). The understanding of the natural distribution of wild timopheevii got bigger by the botanical expeditions to southwest Asia, namely, by Johnson to Turkey in 1965 and to the Fertile Crescent in 1972–1973, and by The Botanical Expedition of Kyoto University to the Northern Highlands of Mesopotamia in 1970 (Badaeva et al. 2021). Wild timopheevii was found also in north-western Syria (Valkoun et al. 1998).
A specimen of two-grained wild wheat was also collected by J. B. Gillett in Rowanduz, northern Iraq, which Nabalek (1929) classified as T. dicoccoides ssp. nudiglumis. Sachs’ classification (1953) coincided with Nabalek’s, despite the fact that his studies of chromosome pairing in F1 hybrids between this taxon and T. turgidum ssp. dicoccoides clearly showed that this wild wheat actually belongs to T. timopheevii ssp. armeniacum. Indeed, based on chromosome pairing and fertility, Tanaka and Ichikawa (1972) included this taxon in the timopheevii complex. Also, the specimen discovered by Strauss in 1910 in western Iran should be included in T. timopheevii ssp. armeniacum and Theodor Strauss should be credited as the first to have found ssp. armeniacum in nature.
Further studies on the distribution of ssp. armeniacum by Jakubziner and others (see Jakubziner 1959), showed that this wild wheat also grows in Azerbaijan and on the eastern slopes of the Akhsam Mountain in Caucasia. In addition, more recent studies (see Kimber and Feldman 1987) established that ssp. armeniacum also grows in the northeastern region of the Fertile Crescent arc, namely, southeastern Turkey, northern Iraq and western Iran. In the Fertile Crescent part of its distribution area, it is found in mixed populations with types that morphologically and cytologically resemble wild emmer, T. turgidum ssp. dicoccoides (Harlan and Zohary 1966; Rao and Smith 1968; Dagan and Zohary 1970; Rawal and Harlan 1975). Yet, it is quite difficult to distinguish T. timopheevii ssp. armeniacum from ssp. dicoccoides, although both subspecies are genetically isolated even when they grow sympatrically in the same population (Tanaka and Ichikawa 1972).
Wild timopheevii differs from wild T. turgidum, ssp. dicoccoides by its shorter stature, hairy leaves (blades and sheaths), culms and spikes, shorter and ovoid spike, less-developed keel, and delicate awns. Accordingly, Jakubziner (1932b) placed it in a separate sub-species, namely, T. dicoccoides ssp. armeniacum. Further studies by Makushina in 1938 (see Jakubziner, 1959) showed that this taxon is sufficiently distinct from the Syrio-Palestinian ssp. dicoccoides to warrant the rank of a separate species, and consequently, she called it T. armeniacum Mak. However, since this name had been briefly used for another taxon, Jakubziner changed it in 1947 to T. araraticum Jakub. (see Jakubziner 1959). Still, T. araraticum was included as a subspecies in T. timopheevii and therefore, cannot be used as a species name (Mac Key 1975). Tzvelev (1976, 1984), van Slageren (1994) correctly considered Mac Key’s classification of araraticum as a subspecies of T. timopheevii illegitimate, since the older epithet armeniacum should have been used both at the subspecies and varietal levels. Accordingly, the wild form of this species should be referred to as T. timopheevii (Zhuk.) Zhuk. ssp. armeniacum (Jakubz.) van Slageren (van Slageren 1994).
A mutant of domesticated T. timopheevii with naked (free-threshing) seeds, was discovered by Zhukovsky and, in 1969, was given the species status, Triticum militinae Zhuk. & Migush. However, this naked wheat was later referred to by van Slageren (1994), Mac Key (2005) as a variety of ssp. timopheevii, namely, var. militinae (Zhuk. et Migusch.) Zhuk. et Migusch., because it is a free-threshing mutant that was selected from a single specimen of domesticated T. timopheevii (Miller 1987) and not commercially cultivated (Mac Key 2005).
Triticum timopheevii contains two subspecies, the wild ssp. armeniacum (former araraticum) and the domesticated ssp. timopheevi. These subspecies, are morphologically similar, and genetically are closely related. The F1 hybrids between them are either sterile, semi-fertile or fully fertile, while they differ genomically and are reproductively isolated from the second tetraploid wheat, T. turgidum (Tanaka and Ichikawa 1972; Tanaka and Ishii 1975; Tanaka et al. 1978). The most differentiating trait between the wild and the domesticated subspecies is rachis brittleness at maturity; in the wild form, the rachis disarticulates, whereas, in the domesticated one it remains intact. In the wild form, the brittle rachis is an essential trait, leading at maturity, to disarticulation of the spike into individual spikelets. Each spikelet, equipped with two awns above and a sharp rachis segment below, is an arrow-like seed-dispersal unit that is very effective for seed dispersal and self-planting under wild conditions (Zohary et al. 2012). In contrast, in the domesticated subspecies, the mature spike remains intact on the culm and breaks into individual spikelets only when slight mechanical pressure is applied at threshing (Dorofeev and Korovina 1979). This difference was caused by two recessive mutations yielding a tough rachis, that occasionally occur in the wild, preventing the dispersal of seeds. While such a mutation is nuisance in nature, it has a positive adaptive value under cultivation, facilitating harvesting, and has thus been preferred by farmers.
Domesticated T. timopheevii contains the recessive br-A1 allele on the short arm of chromosomes 3A (Li and Gill 2006). It is likely that the domesticated form contains an additional recessive allele in the Br-B1 locus on the short arm of chromosome 3G, since Ae. speltoides, (genome SS), the putative donor of the G subgenome, carries the dominant Br-S1 allele for rachis brittleness on chromosome 3S (Li and Gill 2006).
It is difficult to distinguish wild timopheevii, ssp. armeniacum, from wild emmer, T. turgidum ssp. dicoccoides, by morphology (Tanaka and Sakamoto 1979). But, both wild taxa can easily be differentiated based on biochemical, immunological, cytological and molecular markers (Lilienfeld and Kihara 1934; Kawahara and Tanaka 1977; Konarev et al. 1976; Gill and Chen 1987; Jiang and Gill 1994b; Badaeva et al. 1994). From an archaeobotanical perspective, both species can be reliably identified based on several characteristics of charred spikelets (Jones et al. 2000). In blind tests, it was possible to distinguish modern representatives of the two wild taxa on the basis of the primary keel of the glume, which arises just below the rachis disarticulation scar, and the prominent vein on the secondary keel, observable at the base of the glume, which is the part of spikelet most commonly preserved by charring in archaeological material (Jones et al. 2000).
In order to differentiate between seeds of domesticated T. timopheevii from those of domesticated emmer, that were uncovered in archaeological excavations, Boscato et al. (2008) used ribosomal primers ITS2 and ITS2, both from T. timopheevii, and the nuclear primer acetyl-coenzyme A from timopheevii, to discriminated the related DNA sequences of these two taxa. Moreover, Tanno et al. (2018) developed a multiplex PCR DNA marker for quick and easy identification of the genome of the T. timopheevii lineage, including the wild and the domesticated subspecies, and of the T. turgidum lineage, including the wild and domesticated subspecies. This multiplex PCR system is based on the simultaneous PCR amplification of two chloroplast regions, matK and rbcL. The matK region molecularly distinguishes between the two lineages with complete accuracy, whereas the rbcL region serves as a positive control amplicon.
Morphological variation in T. timopheevii involves mainly spike and spikelet sizes and shapes, glume and awn colors and hairiness, plant heights, and leaf widths. T. timopheevii is normally characterized by a dense and pyramidal spike. Yet, wider intraspecific variation was found on the biochemical and molecular levels. Asins and Carbonell (1986a), using the isoenzymes peroxidase and alkaline phosphatase, observed a wide intraspecific variability of these enzymes in wild and domesticated forms of T. timopheevii, with inter-population variability proving greater than the intra-population variability. Domesticated T. timopheevii showed higher variability than the wild subspecies. The interspecific variability data indicated that T. timopheevii is closer to T. turgidum than to any of the diploid species (Asins and Carbonell 1986b). These close relationships stem from the fact that both species share the A subgenome derived from T. urartu. Thus, the differences between these two species must be due to the second subgenome, G in timopheevii and B in turgidum, which derived from different, but closely related, diploid species.
Protein spectra from several subspecies of T. turgidum and from the two subspecies of T. timopheevii, were obtained by electrophoresis of seed extracts on polyacrylamide gels (Johnson et al. 1967). The subspecies of T. turgidum showed nine fast‐moving albumin homologues, while those of T. timopheevii showed seven. The two species had only five albumin bands in common.
Badaeva et al. (2021) presented a comprehensive survey of genomic and cytogenetic diversity of the gene pool of T. timopheevii. Their study provided detailed insights into the cytogenetic composition of this wheat, revealed group-, and population-specific markers and show that chromosomal rearrangements play an important role in intraspecific diversity of T. araraticum. This study enabled Badaeva et al. (2021) to make several major remarks: (i) the extant timopheevii gene pool consists of three distinct lineages, two wild, designated as ARA-0 and ARA-1, and one domesticated; (ii) while ARA-0 was found to be geographically widespread, ARA-1 was restricted to southeastern Turkey and north-western Syria, where it grows sympatrically with wild emmer, Triticum turgidum ssp. dicoccoides; (iii) wild emmer is genetically more diverse, supporting a more recent origin of wild timopheevii; (iv) among the timopheevii lineages, ARA-0 harbors more genetic diversity than ARA-1; (v) Nei’s genetic distance between lineages based on all polymorphic Sequence-Specific Amplification Polymorphism (SSAP) markers or considering only the BARE-1 markers (distributed between A- and G-subgenome chromosomes) revealed that ARA-0 is phylogenetically more closely related to domesticated timopheevii than ARA-1. However, considering only the Jeli markers (target more the A subgenome chromosomes), ARA-1 was more closely related to domesticated timopheevii; and (vi) wild emmer is most closely related to the ARA-1 lineage.
An important outcome of the study of Badaeva et al. (2021) is the identification of three distinct lineages in T. timopheevii: one comprising all domesticated genotypes (including var. militinae and T. zhukovskyi), and two, ARA-0 and ARA-1, belong to the wild form. ARA-0 was found across the whole area of species distribution whereas ARA-1 was only detected in southeastern Turkey and in neighboring northwestern Syria.
Badaeva et al. (2021), concerning the characteristics, composition and geographical distribution of ARA-0 and ARA-1 lineages, are not in agreement with the taxonomic treatment of wild timopheevii by Dorofeev et al. (1980), who divided this taxon into two subspecies: subsp. kurdistanicum Dorof. et Migusch. and subsp. araraticum.
The origin of ssp. timopheevii remains unclear, but Badaeva et al. (2021) speculate that it was probably introduced from easternTurkey, on the grounds that ssp. timopheevii. is more closely related to ssp. armeniacum from Turkey or northern Iraq than to the Transcaucasian types.
ssp. armeniacum is known to have various degrees of structural chromosomal differentiations, involving several interchanges (Svetozarova 1939; Wagenaar 1966; Tanaka and Ichikawa 1968, 1972; Tanaka and Ishii 1975; Kawahara and Tanaka 1977; Jiang and Gill 1994b; Badaeva et al. 1994). In contrast, no distinct structural variations of chromosomes were found in ssp. timopheevii. Most armeniacum and all timopheevii lines in Transcaucasia have the same chromosome structure (Tanaka and Ishii 1975). Consequently, it was concluded that cultivated T. timopheevii in Transcaucasia derived from wild ssp. armeniacum bearing a similar chromosome architecture (Tanaka and Ishii 1975). Kawahara and Tanaka (1977), analyzing chromosome pairing in F1 hybrids between different accessions of ssp. armeniacum collected in southeastern Turkey and northern Iraq, observed multivalents, indicating the wide occurrence of intra-sub-specific translocations. Seed fertility of hybrids between the various accessions of ssp. armeniacum. and domesticated T. timopheevii varied from almost sterile to fully fertile. These findings supported previous studies (Tanaka and Ichikawa 1972) by showing that chromosome differentiation in ssp. armeniacum is more abundant in northern Iraq than in Transcaucasia, indicating that the wild T. timopheevii originated in the north-eastern part of the Fertile Crescent and later spread northward to Transcaucasia.
Both subspecies of T. timopheevii contain genes conferring resistance to wheat fungal and insect pathogens, such as powdery mildew (Tomerlin et al. 1984; Brown-Guedira et al. 1996, 1997, 1999b; Jarve et al. 2000; Leonova et al. 2011; Timonova et al. 2013), leaf rust (Tomerlin et al. 1984; Brown-Guedira et al. 1996, 1997, 1999a, 2003; Leonova et al. 2010; Timonova et al. 2013; Singh et al. 2017), stem rust (Sawhney and Goel 1979; Dyck 1992; Brown-Guedira et al. 1996; Leonova et al. 2011; Timonova et al. 2013), stripe rust (Brown-Guedira et al. 1996) Septoria nodorum blotch (Tomerlin et al. 1984), Septoria blotch (Brown-Guedira et al. 1996), spot blotch (Leonova et al. 2011; Timonova et al. 2013), tan spot (Brown-Guedira et al. 1996), loose smut (Leonova et al. 2011; Timonova et al. 2013) and fusarium head blight (Malihipour et al. 2017), as well as resistance to Hessian fly and curl mite (Brown-Guedira et al. 1996; El Haddoury et al. 2005).
In the production of hybrid wheat lines of T. aestivum, that yield higher than pure, true-breeding lines, and exhibit improved quality and greater tolerance to environmental and biotic stresses (Briggle 1963; Wilson and Driscoll 1983; Bruns and Peterson 1998; Jordaan et al. 1999), alloplasmic lines having T. timopheevii cytoplasm that is different from common wheat cytoplasm (Maan 1975; Tsunewaki 1989) is commonly used to create male-sterile female lines (Wilson and Ross 1962). Yet, such male sterility requires restoration of fertility in the F1 hybrids by the male parent having a restorer gene(s). Several such restorers were identified (Maan and Lücken 1968a; Chen 2003), but it is difficult to find such genes that are effective in a wide range of T. aestivum genotypes. Moreover, the system also requires breeding of the male parent to produce male lines that contain suitable restorer gene(s), thus rendering hybrid seed production more expensive and limiting of the number of male parents that can be tested for combining ability.
10.3.3.2 Ssp. armeniacum (Jakubz.) Van Slageren (Wild timopheevii)
The essential nomenclature of this subspecies is currently as follows: T. timopheevii (Zhuk.) Zhuk. ssp. armeniacum (Jakubz.) van Slageren, comb. nov. [Syn.: T. dicoccoides var. nudiglumis Nabalek; T. dicoccoides (Körn. ex Asch. & Graebn.) Schweinf. ssp. armeniacum Jakubz.; T. araraticum Jakubz.; T. armeniacum (Jakubz.) Makush.; T. timopheevii Zhuk. subsp. araraticum (Jakubz.) Mac Key; T. turgidum L. ssp. armeniacum (Jakubz.) Á. Löve and D. Löve.; T. timopheevii (Zhuk.) Zhuk. var. araraticum (Jakubz.) C. Yen; T. timopheevii (Zhuk.) Zhuk. ssp. araraticum (Jakubz.) Mac Key; Gigachilon timopheevii (Zhuk.) Á. Löve and D. Löve ssp. armeniacum (Jakubz.) Á. Löve] (Fig. 10.6a).
The geographical distribution of the wild subspecies of T. timopheevii, ssp. armeniacum, is west-Irano-Turanian phytogeographic region, including southeastern Turkey, northern Iraq, western Iran and Trans- and Cis-Caucasia. Compared to the second wild allotetraploid wheat, wild emmer (T. turgidum ssp. dicoccoides), the distribution area of subsp. armeniacum is more affected by the steppical conditions of the Irano-Turanian region. In this area, it thrives on terra rossa, basalt, and other soils that were produced from hard limestone bedrock, in the herbaceous cover of the deciduous oak-park forests, in evergreen dwarf shrub formations, and in steppe-like formations where it occupies primary habitats, as well as in secondary habitats such as abandoned fields, roadsides and edges of cultivation. In most of its habitats, ssp. armeniacum grows in patches and in mixed stands with other annual cereals and several legumes. It grows at altitudes of 300–1600 m.
Subsp. armeniacum is distributed in the north-central region of the distribution of the wild species of Triticum. In some locations in the northeastern part of the Fertile Crescent, it is abundant while in other is more sporadic. The distribution of ssp. armeniacum overlaps that of both of its putative diploid parents, Ae. speltoides and T. urartu, but it is more restricted. The putative diploid parents have massive contact in the northeastern part of the Fertile Crescent, which is the presumed center of origin of subsp. armeniacum. It grows sympatrically with Ae. speltoides, Ae. caudata, Ae. umbellulata, T. urartu, T. monococcum ssp. aegilopoides (mainly var. thaoudar), T. turgidum ssp. dicoccoides (in the northeastern part of the Fertile Crescent arc), Ae. cylindrica, Ae. columnaris and Ae. triuncialis, and allopatrically with Amblyopyrum muticum, Ae. geniculata, Ae. biuncialis, Ae. neglecta, Ae. peregrina. Ae. tauschii, Ae. crassa and Ae. juvenalis.
Ssp. armeniacum grows sympatrically with wild emmer in many sites in southeastern Turkey, northern Iraq and western Iran (Harlan and Zohary 1966), and morphological differences between the two wild wheats are not clear with respect to ear color, glume pubescence and shooting time. Distinguishing their ripe ears from one another by morphological examination is difficult (Tanaka and Ishii 1973) and requires crossing and/or by molecular tests. For these reasons, taxonomists dealing with the flora of south-west Asia (e.g., Bor 1968) frequently group all Kurdish wild tetraploid wheat material together into what they call T. dicoccoides, disregarding the fact that they are actually two reproductively well-isolated entities.
In contrast to the accessions of ssp. dicoccoides from the southwestern region of the Fertile Crescent arc, i.e., northeastern Israel, northwestern Jordan, southwestern Syria and southeastern Lebanon, that features larger and most robust plants with lax heads and heavy large awns, northeastern Fertile Crescent arc tetraploid wheat plants (ssp. dicoccoides mixed with ssp. armeniacum) are smaller and slender and characterized by somewhat small, compact heads, fine-textured awns, small spikelets, and are often hairy, with sparse pubescence on the rachis and spikelet base (Rao and Smith 1968; Rawal and Harlan 1975). These tetraploid wheats are found as a minor component of the annual herbaceous flora of the oak woodlands in the Taurus and Zagros Mountains (Rawal and Harlan 1975), where they are never dominant and occur in widely scattered patches on rocky slopes. In some areas in Turkey, e.g., near Gaziantep, the mixture of tetraploid wheats tends to converge toward the wild diploid wheats of the area (Rawal and Harlan 1975). However, the diploids always have more spikelets per head, but the spikelets are strikingly similar in size and appearance.
Differential production of semi-fertile and sterile hybrids have been reported when lines of ssp. armeniacum were crossed with lines of the domesticated form ssp. timopheevii (Tanaka and Ichikawa 1968, 1972; Tanaka and Ishii 1975). Two groups of ssp. armeniacum lines were found in crosses with a tester strain of ssp. timopheevii. The first group gave rise to semi-fertile F1 hybrids that showed normal chromosome association at first meiotic metaphase, whereas the second group yielded sterile hybrids that exhibited several chromosome interchanges. The former had dark green leaves and a procumbent tillering habit, while the latter had light green leaves and a semi-erect tillering habit (Tanaka and Ishii 1975). It seems therefore that ssp. armeniacum has undergone extensive structural changes at the chromosomal, and possibly also at the genetic, level and that genetic isolation by hybrid sterility between lines of ssp. armeniacum as well as between some of them and ssp. timopheevii is, currently, partially established (Tanaka and Ishii 1975).
High intraspecific diversity of the karyotype was detected in ssp. armeniacum by several researchers by crossing experiments (Tanaka and Ichikawa 1968, 1972; Tanaka and Ishii 1973, 1975; Tanaka et al. 1968; Kawahara and Tanaka 1977; Kawahara et al. 1996), by C-banding (Badaeva et al. 1990), by nuclear (Nave et al. 2021; Shcherban et al. 2016) and chloroplast DNA markers (Mori et al. 2009; Gornicki et al. 2014).
Using C-banding techniques, Badaeva et al. (2021) analyzed the karyotypes of a large number of accessions of ssp. armeniacum from all over across its distribution area of this subspecies. They found that this wild taxon comprises two distinct lineages, ARA-0 encompassed 342 genotypes and is geographically widespread and characterized by a wide genetic diversity, and ARA-1, encompassed 49 genotypes that has limited in its distribution to southeastern Turkey and north-western Syria, as well as in its genetic variation.
A recent detailed analysis of karyotype structure and C-banding patterns highlighted significant differences between wild emmer and wild and domesticated T. timopheevii (Badaeva et al. 2021). Wild timopheevii is characterized by a wide diversity of C-banding patterns and broad translocation polymorphisms. The karyotype lacking chromosomal rearrangements (designated normal by the authors), found in 44.6% genotypes of wild form, was the most frequent karyotype variant shared by wild and domesticated T. timopheevii.
Cytogenetic data showed that the speciation of ssp. armeniacum has been accompanied by chromosomal rearrangements involving either intra- or inter-subgenome translocations (Kawahara and Tanaka 1977, 1981; Chen and Gill 1983; Jiang and Gill 1994b; Badaeva et al. 1990, 1994; Kawahara et al. 1996; Rodriguez et al. 2006b). Badaeva et al. (2021) reported that 216 out of 391 (55.4%) wild timopheevii accessions carried a translocated karyotype. One-hundred-forty-seven genotypes differed from the ‘normal’ karyotype by one, 45 genotypes by two (double translocations), 21 genotypes by three (triple translocations) and three genotypes by four chromosomal rearrangements. While most variants of chromosomal rearrangements were unique and identified in one or few genotypes, only four following variants, representing 16% of the whole analyzed material, were relatively frequent.
Translocations occurred more frequently in the chromosomes of the G subgenome than of the A subgenome. Individual chromosomes differed in the frequencies of their involvement in translocations and each geographical region contained a unique spectrum of translocations. Karyotypic diversity was the highest in Iraq, followed by Transcaucasia and Turkey; Iran showed little karyotypic variation.
Badaeva et al. (2021), using the six DNA probes pTa-535, pSc119.2, pAesp_SAT86, GAAn, Spelt-1, and Spelt-52, estimated the intraspecific diversity of wild timopheevii and assessed its phylogenetic relationships with domesticated timopheevii. The distribution of pTa-535 was monomorphic among both the wild and domesticated forms, while the pSc119.2 site on 1AL discriminated ARA-1 and the domesticated form from the ARA-0 lineage. Whereas the distribution of the pAesp_SAT86 probe was similar in all domesticated timopheevii genotypes, the labeling patterns were highly polymorphic in wild timopheevii. Large pAesp_SAT86 sites were found only on some G-subgenome chromosomes. The A-subgenome chromosomes possessed several small, but genetically informative polymorphic sites, some of which were lineage-specific. Most obvious differences were observed for 3A, 4G and 7G chromosomes. Thus, all domesticated timopheevii and ARA-1 genotypes carried the pAesp_SAT86 signal in the middle of 3AS, while for ARA-0 it was located sub-terminally on the long arm. One large pAesp_SAT86 cluster was present on the long arm of 4G in ARA-0, but on the short arm in ARA-1 and domesticated timopheevii. Two large and adjacent pAesp_SAT86 clusters were detected on 7GS in ARA-1 and domesticated timopheevii, but they were split between opposite chromosome arms in all ARA-0 genotypes. Differences between ARA-0 and ARA-1 in pAesp_SAT86 cluster position on 4G and 7G could be caused by pericentric inversions.
FISH with Spelt-1 and Spelt-52 probes revealed high intraspecific diversity of wild. and low polymorphism in domesticated timopheevii. The broadest spectra of labeling patterns were found in genotypes from Dahuk and Sulaymaniyah (Iraq) and in the ARA-1 group from Turkey, while material from Transcaucasia exhibited the lowest variation. The Spelt-1 signals in various combinations appeared in sub-telomeric regions of either one or both arms of 2A, 6A, and all G-subgenome chromosomes. The Spelt-52 signals were observed in various combinations on 2AS, 1GS, and 6GL chromosomes.
The existence of two lineages in ssp. armeniacum is supported by the study of Mori et al. (2009) that was based on 13 polymorphic chloroplast microsatellite markers (cpSSR). Their ‘plastogroup G-2’ was distributed in south-eastern Turkey and northern Syria and was closely related to domesticated timopheevii.
The high level of karyotype diversity in wild ssp. armeniacum collected in northern Iraq (Badaeva et al. 1994, 2021), suggests that this is the region where T. timopheevii originated. Indeed, studies cof whole chloroplast genomes of wild T. timopheevii, ssp. armeniacum, and Ae. speltoides indicated that the wild subspecies of the former originated within the last 0.4 MYA, likely in the northern Iraq region around Arbil (Gornicki et al. 2014). Two accessions of wild T. timopheevii collected near Arbil had the dominant haplotype of Ae. speltoides chloroplast, hinting that they are the ancestral forms of ssp. armeniacum.
The region around Dahuk in northern Iraq can be considered the center of origin, but also the center of diversity of T. araraticum.
Gornicki et al. (2014), based on whole chloroplast genome sequence information and large taxon sampling, showed that T. timopheevii most probably originated in northern Iraq. According to Badaeva et al. (2021) data, the wild lineage that exists in northern Iraq belong to the ARA-0 lineage as no ARA-1 occurs in Iraq. This was supported by Bernhardt et al. (2017) showing that some ARA-0 and domesticated timopheevii genotypes are most closely related. Haplotype analysis of the Brittle rachis 1 (BTR1-A) gene in a set of wild timopheevii in comparison with two domesticated timopheevii accessions (Nave et al. 2021) also showed closer relationships of domesticated to wild timopheevii from Iraq.
Lineage ARA-1 of ssp. armeniacum grows in mixed populations with wild emmer, ssp. dicoccoides, in the Northern Levant, and is phylogenetically most closely related to it. ARA-1 is morphologically more similar to ssp. dicoccoides.
Based on karyotype analyses, translocation spectra and distribution of DNA probes wild populations from Dahuk and Sulaymaniyah, Iraq, harbored the highest karyotypic diversity among all ssp. armeniacum populations studied (Badaeva et al. 2021). They therefore, consider the region around Dahuk in Northern Iraq as the center of diversity of wild timopheevii, and this is probably the region where ssp. armeniacum originated. This is supported by Nave et al. (2021), who found the highest haplotype diversity among ssp. armeniacum from Iraq, and by Bernhardt et al. (2017), Gornicki et al. (2014) who traced chloroplast haplotypes from Aegilops speltoides growing in Iraq via ssp. armeniacum (ARA-0) to domesticated timopheevii and T. zhukovskyi.
However, some FISH patterns suggested that domesticated timopheevii probably originated in Turkey and probably from ARA-1 This is supported by the following observations: (i) TIM and ARA-1 carry the pSc119.2 signal in the middle of 1A long arm, while this site was absent from ARA-0; (ii) all ARA-0 and most ARA-1 possessed the Spelt-52 signal on 6GL, but it is absent in all TIM and five ARA-1 genotypes from Gaziantep-Kilis, Turkey. The distribution of Spelt-1 and Spelt-52 probes on chromosomes of these five genotypes was similar to, and in accession IG 116165 (ARA-1 from Gaziantep) almost identical with TIM; (iii) the pAesp_SAT86 patterns on chromosomes 3At, 4G, and 7G are similar in TIM and ARA-1 but differed from ARA-0. Differences between ARA-1 and TIM based on FISH patterns of some other chromosomes as well as the results of C-banding and molecular analyses suggest that extant ARA-1 genotypes are not the direct progenitors of TIM but that the ARA-1 lineage is most closely related to it. Based on AFLP, C-banding, FISH and Jeli retrotransposon markers, TIM was genetically most closely related to ARA-1. Additional evidence for the close relationship between TIM and ARA-1 lineages comes from allelic variation at the VRN-1 locus of genome A (Shcherban et al. 2016). This analysis revealed a 2.7 kb deletion in intron 1 of VRN-A1 in three T. timopheevii and four T. araraticum accessions, which, according to our data, belong to the ARA-1 lineage. However, at Vrn-G1, TIM from Kastamonu in Turkey (PI 119442) shared the same haplotype (Vrn1Ga) with ARA-1 samples, while TIM from Georgia harbored haplotype VRN-G1 as found in ARA-0. These results suggest multiple introgression events and incomplete lineage sorting as suggested by Bernhardt et al. (2017, 2020).
Iran occupies a marginal part of the distribution range of wild timopheevii. An abundance of the pericentric inversion of the 7At chromosome in the Iranian group indicates that it is derived from Iraq. The karyotypically ‘normal’ genotype was probably introduced to Transcaucasia via Western Azerbaijan (Iran). The low diversity of FISH patterns and the low C-banding polymorphism of wild timopheevii from Transcaucasia indicate that this wild taxon, ssp. armeniacum, was introduced as a single event. Interestingly, the AFLP data suggested some similarity between ARA-0 from Armenia and Azerbaijan and domesticated timopheevii.
10.3.3.3 Ssp. timopheevii (Zhuk.) Löve and Löve (Domesticated timopheevii)
Triticum timopheevii ssp. timopheevii (Zhuk.) Löve and Löve, commonly known as sanduri wheat or timopheev’s wheat, is the domesticated form of its wild progenitor. It is an endemic crop restricted to Transcaucasia, particularly to western Georgia (Zohary et al. 2012) and mainly used as a cereal for making bread, biscuits and cookies. The grains are also used to feed livestock and poultry, whereas the straw is used as a biomass for fuel, for thatching, and for making mats, carpets, and baskets.
The plant has delicate spikes and spikelets, and like the wild subspecies also ssp. timopheevii, shows close morphological similarities to ssp. dicoccon and paleocolchicum, the hulled types of T. turgidum. The relatively limited genetic diversity manifested by morphological variation of the domesticated form of T. timopheevii, was also detected at the molecular level (Fig. 10.6b).
Wild T. timopheevii contains both winter and spring types, whereas domesticated timopheevii is considered a spring type (Shcherban et al. 2016). In order to clarify the origin of the spring growth habit in ssp. timopheevii, allelic variability of the vernalization VRN-1 gene was investigated in a set of accessions of both subspecies of T. timopheevii, together with Ae. speltoides, presumed to be the donor of the G subgenome to this tetraploid species. Among accessions of ssp. armeniacum, two large mutations were found in both VRN-A1 and VRN-G1 loci, which were found to have no effect on vernalization requirements (Shcherban et al. 2016). Spring ssp. timopheevii had VRN-G1a allele in common for the two subspecies, and two alleles that were specific (VRN-A1f-ins, VRN-A1f-del/ins). These two alleles include mutations in the first intron of VRN-A1 and also share a 0.4 kb MITE insertion near the start of intron 1. Hence, Shcherban et al. (2016) suggested that this insertion resulted in a spring growth habit in a progenitor of ssp. timopheevii, which was probably selected for during subsequent domestication.
Domesticated T. timopheevii is presumably evolved in isolation from the more common T. turgidum, and hybrids between it and T. turgidum are reportedly sterile (Lilienfeld and Kihara 1934; Sachs 1953; Tanaka and Ichikawa 1972). The wild wheat from which it could have been derived is obviously ssp. armeniacum (Jakubziner 1932b; Dorofeev et al. 1980), which is also scattered across Transcaucasia, and with which the domesticated types are inter-fertile and share identical genomic constitution. It was probably domesticated in Georgia, where it was mostly grown mixed with domesticated diploid wheat, Triticum monococcum ssp. monococcum, or as a weed in fields of Triticum aestivum.
Domesticated timopheevii was part of the spring landrace Zanduri (a mixture of ssp. timopheevii and T. monococcum) (Zeven 1980). This landrace was cultivated in the humid and moderately cool climate zone of western Georgia, 400–800 m above sea level (Dorofeev et al. 1980). Martynov et al. (2018) reported that ssp. timopheevii is not drought tolerant.
Currently, the cultivation of ssp. timopheevii is limited to western Georgia, but the area of cultivation might have been larger in the past. Badaeva et al. (2021), while screened all available passport data of T. timopheevii, found two accessions of ssp. timopheevii that were collected from Turkey in the first half of the twentieth century. The two accessions harbor the normal karyotype of T. timopheevii and were characterized as a typical domesticated timopheevii. Assuming that the passport data of these two accessions is correct, Badaeva et al. (2021) supposed that T. timopheevii may have been cultivated in Turkey during the first half of the twentieth century, indicating that the cultivation range of ssp. timopheevi at this time was wider than the current one. Badaeva et al. (2021) speculate that the two ssp. timopheevii accessions were probably introduced from Transcaucasia to Turkey and may have been left over from unsuccessful cultivation or breeding experiments.
From the point of view of domestication and spread of domesticated wheats, the role of the wild and domesticated forms of T. timopheevii is apparently negligible. It is likely that in the Neolithic days, both wild T. turgidum and wild T. timopheevii were taken into cultivation in southeastern Turkey, northern Iraq, and western Iran, and that the early non-brittle, hulled wheat remains found in these places represent both stocks (Zohary et al. 2012). Judging from the present geographical distribution of wild T. timopheevii, as well as from its assumed distribution at the end of the Younger Dryas cold period (ca 12,900–11,700 years before present), the carbonized grains, spikelets, and clay impressions found at Cayonu Tepesi in southeastern Turkey (ca. 9000 BP) and Jarmo northern Iraq on the foothills of the Zagros Mountains (ca. 8750 BP) could belong to this taxon rather than to wild T. turgidum. If this is the case, then T. timopheevii was first domesticated in the northeastern part of the Fertile Crescent. Eventually, the brittle form of T. timopheevii gave rise to only a restricted number of non-brittle cultivars, all of which belong to ssp. timopheevii, which are currently cultivated in a few localities in Transcaucasia. Yet, the question remains: if such alleged domesticated T. timopheevii were indeed produced in south-west Asia, why were they fully replaced by T. turgidum, even among the local landraces (Zohary et al. 2012)? It is speculated that when emmer cultivation spread to Transcaucasia, local populations of wild T. timopheevii colonized emmer crops fields as a weed, and, became domesticated by being incorporated into the agricultural cycle of harvest and sowing (Nesbitt and Samuel 1996).
The oldest known records of prehistoric ssp. timopheevii are from Turkey, ALıklı Höyük in Cappadocia and Cafer Höyük in southeastern Turkey (Cauvin et al. 2011). At three Neolithic sites and one Bronze Age site in northern Greece, spikelet bases of a “new glume wheat” type of hulled wheat have been recovered (Jones et al. 2000). These spikelet bases are morphologically distinct from the typical hulled wheats, T. monococcum ssp. monococcum (einkorn), T. turgidum ssp. dicoccon (emmer) and T. aestivum ssp. spelta (spelt), previously observed in Greece as well as in Neolithic and Bronze Age sites in Turkey, and southern and central Europe. The taxonomic identification of this new type remains uncertain, but it seems likely that they are tetraploid, and have morphological features in common with T. timopheevii (Jones et al. 2000). At the northern Greek sites, at least, the new type may have been cultivated as a mixed crop with einkorn and emmer. At some other sites, this wheat was grown as a minor component in wheat fields (Ulaş and Fiorentino 2021). Yet, in some places, new glume wheat was a major crop in itself (Bogaard et al. 2017; Ergun 2018).
Czajkowska et al. (2020) detected DNA sequences from the G subgenome in two samples of archaeological new glume wheat, one from Turkey and the second from Poland, thus providing evidence that this wheat is indeed a domesticated type of T. timopheevii. This confirms that ssp. timopheevii was domesticated from ssp. armeniacum during early neolithic age and was widely cultivated in the prehistoric past.
Vavilov (1935) suggested that ssp. timopheevii of western Georgia was probably introduced from northeastern Turkey. The possibility of introduction of ssp. timopheevii into Georgia from northeastern Turkey is supported by Dorofeev et al. (1980).
10.3.3.4 Cytology, Cytogenetics and Evolution
T. timopheevii is an allotetraploid species (2n = 4x = 28) that exhibits a diploid-like behavior at meiosis, namely, formation of 14 bivalents of homologous chromosomes. The genomic designation of its nuclear genome is GGAA (Lilienfeld and Kihara 1934; Kihara 1963; Kihara and Tanaka 1970; Kimber and Tsunewaki 1988; Dvorak 1998) and its organellar genome is designated G (Tsunewaki et al. 1976; Ogihara and Tsunewaki 1988; Tsunewaki 1989; Wang et al. 1997) or S (Dvorak 1998). Lilienfeld and Kihara (1934) analyzed chromosome pairing in F1 hybrids between different subspecies of T. turgidum and wild and domesticated subspecies of T. timopheevii and found that the hybrids involving T. timopheevii differed from those involving subspecies of T. turgidum. The T. turgidum x T. timopheevii hybrids had poor chromosome pairing at first meiotic metaphase, and were sterile, whereas hybrids between different subspecies of T. turgidum exhibited almost complete chromosome pairing and were fertile. On the basis of chromosome pairing in these hybrids, they agreed with Zhukovsky (1928) that T. timopheevii should be considered a different species from T. turgidum, and designated the genome of T. timopheevii by the formula AAGG in contrast to the BB formula given to the genome of T. turgidum. [Note: The subgenome symbols G and B, donated by the female parents of the allotetraploid wheats (see below), should be on the left side of the genomic formula]. Moreover, Lilienfeld and Kihara (1934) placed T. timopheevii in a section of its own, thus suggesting a different origin for this species as compared to that of T. turgidum, a suggestion that was followed by Svetozarova (1939), Sears (1948, 1969). Kostoff (1937a, b, c) obtained similar results to those of Lilienfeld and Kihara, but interpreted them as showing partial homology between the genomes of T. timopheevii and T. turgidum, and therefore suggested to designate the genome of T. timopheevii by the formula ßßAA.
The formula GGAA for the genome of T. timopheevii shows that this species contains one subgenome similar to the A subgenome of T. turgidum (genome BBAA) and to that of T. aestivum (BBAADD) but differs in the second subgenome. T. timopheevii also contains a distinct cytoplasm which induces male sterility when combined with the nuclear genome of T. turgidum and T. aestivum (Maan and Lücken 1971; Maan 1973; Tsunewaki et al. 1976; Tsunewaki 1989).
The results reported by Sachs (1953) broadly agree with those obtained by Lilienfeld and Kihara (1934) and by Kostoff (1937b, c), i.e., the F1 hybrids T. timopheevii x T. turgidum showed considerably less chromosome pairing. Yet, Sachs followed Nabalek (1929) in identifying an accession, that was collected in northern Iraq, as T. dicoccoides Körn. var. nudiglumis Nabalek, in spite of the fact that the F1 hybrids between ssp. dicoccoides and var. nudiglumis, exhibited reduced chromosome pairing and were completely sterile. Notwithstanding, because of the inclusion of var. nudiglumis in dicoccoides, Sachs (1953) concluded that the latter is characterized by a wide chromosomal variation and postulated that T. timopheevii arose from dicoccoides and that cytologically intermediate genotypes between the two varieties should exist.
Wagenaar (1961a, 1966) studied chromosome pairing in F1 hybrids between T. timopheevii and T. turgidum. While his results were exactly in line with those obtained by previous researchers, he interpreted them differently. Wagenaar suggested that the pairing failure in these hybrids could be attributed to genes affecting chromosome pairing and chiasma formation and less to structural changes of the chromosomes. Consequently, he credited gene action and not chromosome structural differentiation as the origin of T. timopheevii speciation processes. Wagenaar (1966) considered the G subgenome as a modified B and proposed that ssp. armeniacum evolved after becoming isolated from ssp. dicoccoides through mutations of the gene complex controlling chromosomal pairing.
To identify accessions of tetraploid wheat that were collected by Jack R. Harlan in mixed populations of ssp. dicoccoides and ssp. armeniacum in Turkey, Rao and Smith (1968) crossed six of the accessions with four Israeli accessions of ssp. dicoccoides; the F1 hybrids were then morphologically and cytogenetically analyzed. Both groups were also crossed with a number of other tetraploid wheats including T. timopheevii, T. turgidum ssp. turgidum, and ssp. dicoccon. Cytogenetically, the four Israeli accessions were similar and exhibited very close relationships with dicoccon and turgidum, but their hybrids with timopheevii showed poor chromosome pairing and were completely sterile. Four of the six Turkish accessions were similar to the Israeli group in pairing relationships and seed set percentages (Rao and Smith 1968). The remaining two Turkish accessions showed considerable cytogenetic differentiation. The Turkish accession 11,189 showed a close pairing relationship and some fertility with timopheevii and exhibited poor pairing and complete sterility in crosses with dicoccon and the Israeli ssp. dicoccoides group. Surprisingly, the Turkish accession 11,191 exhibited almost complete chromosome pairing and some fertility in crosses with both timopheevii and dicoccon (Rao and Smith 1968).
Rawal and Harlan (1975) studied chromosome pairing in meiosis of F1 hybrids involving three Israeli accessions of ssp. dicoccoides, the six Turkish accessions of tetraploid wheat that were used by Rao and Smith (1968), and one line of T. timopheevii. Like Rao and Smith (1968), Rawal and Harlan (1975) found that four of the six Turkish accessions were cytologically similar to the Israeli dicoccoides accessions, and one Turkish accession (# 189) was cytologically similar to T. timopheevii, whereas the other Turkish accession (# 191) showed good chromosome pairing with both ssp. dicoccoides and ssp. timopheevii. Interestingly, the four Turkish accessions that were identified as ssp. dicoccoides had somewhat better chromosomal pairing with T. timopheevii (average number of chromosome association/cell was 22.0–22.8) than did the Israeli accessions (average number of chromosome association/cell was 18.8–21.5 (Rawal and Harlan 1975).
The results of Rao and Smith (1968) and those of Rawal and Harlan (1975) tend to support Wagenaar’s contention that the pairing behavior in these taxa is primarily under genetic control. It is difficult to visualize genomic differentiation based on alteration of chromosome structure that would account for this behavior. If the differences were due to structure only, then a chromosome of the B subgenome that pairs with a timopheevii chromosome, should not pair with a dicoccoides chromosome (Rawal and Harlan 1975). Yet, in accession # 191, chromosomes paired with both subspecies to approximately the same degree. The fact that there is little or no morphological differentiation between the plants of the Turkish population with different chromosome behaviors, suggests that there is no intermediate race, but rather, different genotypes within the population (Rawal and Harlan 1975).
The pattern of chromosome pairing in F1 hybrids between a synthetic amphiploid T. timopheevii-Ae. tauschii (2n = 6x = 42; genome GGAADD), used as male parent, and 19 monotelocentric lines of T. aestivum cv. Chinese Spring, each containing one dose of a known chromosome arm, instead of a pair of the relevant chromosomes, was studied by Feldman (1966b). Formation of a heteromorphic bivalent (pairing between a complete timopheevii chromosome with a telocentric Chinese Spring chromosome) at meiosis of the F1 hybrids, indicated that the telocentric chromosome was homologous or partly homologous to the corresponding arm of the timopheevii chromosome. A multivalent involving the telocentric chromosome indicated the occurrence of chromosome structural modifications. The pairing of the telocentric chromosomes clearly showed a large difference between the A and B subgenome chromosomes. Feldman (1966b) reported that six out of the eight arms of the studied A subgenome chromosomes showed high pairing and only two showed poor pairing, whereas only one arm out of the 11 arms of the B subgenome showed good pairing, whereas the other 10 arms paired very poorly. Telocentrics of the B subgenome differed markedly in pairing frequency (Feldman 1966b), indicating that some T. timopheevii chromosomes are more significantly differentiated than others. The poor pairing was mainly between chromosomes of the B and G subgenomes (Feldman 1966b). That is, while the A subgenome of T. aestivum is still relatively closely related to the A subgenome of T. timopheevii, the B subgenome is greatly diverged from the G subgenome. Indeed, recent whole genome sequencing showed that the G subgenome donor to wild T. timopheevii diverged from Ae. speltoides 2.86 (3.24–2.51) MYA (Li et al. 2022).
Multivalent chromosomes associations were observed in ten out of the 19 hybrid lines; four from A and six from B subgenomes chromosomes were involved in multivalent associations, indicating the existence of at least five translocations between the parental species. This poor chromosome pairing in hybrids between T. aestivum and T. timopheevii might be due to chromosome structural differences rather than to desynaptic genetic factors causing asynapsis when heterozygous (Wagenaar 1961a, 1966). Indeed, no such genes were found on any of the 26 arms of timopheevii tested by being made hemizygous in various hybrids. According to Wagenaar, these genes are assumed to prevent pairing of chromosomes only when a single dose of each gene from each parent is present, thereby explaining why there is asynapsis in the hybrids but not in the amphiploids derived from this hybrid, as was found by Sachs (1953). If these genes are actually present, it is difficult to understand how they can specifically affect the pairing of the chromosomes of the B-G subgenomes and why they have differential effects on different chromosome arms.
Maestra and Naranjo (1999) used the C-banding technique to study chromosome pairing at first meiotic metaphase in the F1 of hybrids T. turgidum ssp. durum x T. timopheevii (hybrid genome BGAA), T. aestivum x T. timopheevii (hybrid genome BGAAD), and T. turgidum ssp. durum x T. aestivum (hybrid genome BBAAD). C-banding enabled them to identify and differentiate between individual chromosome arms of T. timopheevii and those of T. turgidum ssp. durum and T. aestivum. Maestra and Naranjo (1999) found that homologous pairing between the A subgenome chromosomes was similar in the three hybrid types BGAA, BGAAD and BBAAD, but B-G chromosome associations were less frequent than B-B associations. Homoeologous associations were also observed, especially in the BGAAD hybrids.
Originally, it was thought that the A subgenome of T. timopheevii derived from the Am genome of T. monococcum (Lilienfeld and Kihara 1934). In accord with this, Kostoff (1937a) reported that in the F1 T. timopheevii x T. monococcum triploid hybrid, the chromosomes of the Am genome of monococcum paired most frequently with 7 chromosomes of timopheevii, while the other 7 chromosomes of timopheevii remained as univalents. Consequently, Kostoff (1937a) concluded that T. timopheevii has one subgenome homologous with genome Am. Similarly, following observations of meiotic pairing in hybrids between the two tetraploid species, Wagenaar (1961a) and Tanaka et al. (1978) suggested that T. monococcum contributed the A subgenome to both tetraploid wheats. However, Dvorak et al. (1993), studying variations in 16 repeated nucleotide sequences, detected relatively little divergence between the repeated nucleotide sequences of the A subgenome of T. timopheevii and the genome of T. urartu and noted more variation between the A subgenome of T. timopheevii and the genome of T. monococcum. They therefore, concluded that the A subgenome of T. timopheevii was contributed by T. urartu.
Following analysis of chromosome pairing in hybrids, Riley et al. (1958) proposed that Ae. speltoides was the most likely diploid species that donated the G subgenomes to T. timopheevii. This proposal was reinforced by the cytogenetic study of Shands and Kimber (1973). In agreement with the above, Dvorak and Zhang (1990), studying variations in repeated nucleotide sequences, concluded that Ae. speltoides is the closest extant species to the G subgenome of T. timopheevii. The incomplete homology between S and G is accounted for by assuming that the G subgenome has undergone modifications at the tetraploid level. Owing to uniparental transmission of the cytoplasm through the female parent, the maternal parent of the wheat species was traced back to Ae. speltoides, which chloroplast and mitochondrial DNA studies have shown is the cytoplasm donor to both the timopheevii and the turgidum lineages (Ogihara and Tsunewaki 1988; Terachi et al. 1990; Golovnina et al. 2007; Wang et al. 1997). Likewise, Kilian et al. (2007), using nuclear and cytoplasm DNA in studies of a large collection of polyploid wheats and Ae. speltoides, obtained evidence supporting the suggestion that Ae. speltoides is the donor of the B and G subgenomes to the allotetraploid wheats. In accord with the above, Gornicki et al. (2014), studying whole chloroplast genomes of a large number of Triticum and Aegilops accessions, found that the cytoplasm of Ae. speltoides is the closest to the cytoplasms of T. timopheevii and T. turgidum. However, the chloroplast genome of Ae. speltoides is more closely related to that of T. timopheevii than to the chloroplast genome of T. turgidum (Gornicki et al. 2014). Consequently, Gornicki et al. (2014), like Dvorak and Zhang (1990), assumed that either the female donor of the cytoplasm and B genome to the T. turgidum is either a relative of Ae. speltoides (perhaps even an extinct species), or the allotetraploidization event of T. turgidum occurred much earlier (about 300,000 years earlier) than that of T. timopheevii (Gornicki et al. 2014). As an older species, the T. turgidum B subgenome and cytoplasm exhibit more divergence from the S genome and cytoplasm of Ae. speltoides than the G subgenome and the cytoplasm of T. timopheevii. In addition, T. turgidum is considerably more polymorphic than T. timopheevii (Gornicki et al. 2014).
In the T. timopheevii x Ae. speltoides hybrids, chromosome pairing at first meiotic metaphase occurred preferentially between chromosomes of the G subgenome and the S genome (Rodriguz et al. 2000a). Pairing between G and S chromosomes reached frequencies higher than 50% in most of the arms. The reduced arm length (Gill and Chen 1987; Maestra and Naranjo 1998) may account for the pairing decrease between the 3GS-3SS and 5GS-5SS arms. Structural differences existing between the 1SS and 1GS and between 4SS and 4GS arms (Gill and Chen 1987; Jiang and Gill 1994b; Maestra and Naranjo 1999) affecting pairing between them. The 1GS arm with two translocated segments, an intercalary segment from 6AS, and a terminal segment from 4GS, did not pair with 1SS.
In vitro DNA: DNA hybridizations and hydroxyapatite thermal-elution chromatography were employed by Nath et al. (1985) to identify the diploid donor of the G subgenome of T. timopheevii. Total genomic, unique-sequence, and repeated-sequence fractions of 3H-T. timopheevii DNA were hybridized to the corresponding fractions of unlabeled DNAs of the five Sitopsis species. The heteroduplex thermal stabilities indicated that Ae. speltoides was the most closely related species to the G genome of T. timopheevii. Dobrovolskaya et al. (2011) transferred microsatellite (SSR) markers from Ae. speltoides to T. timopheevii and found that most of the SSRs were integrated into chromosomes of the G subgenome rather than to chromosomes of the A subgenome. This also indicates a close relationship between the G subgenome and the S genome.
Strangely enough, the results of Takahashi et al. (2010) indicated that the wild and domesticated subspecies of T. timopheevii might have arisen independently via allotetraploidization, with both subspecies obtaining the A subgenome from T. urartu, but ssp. armeniacum obtaining the G subgenome from Ae. speltoides and ssp. timopheevii obtaining it from one of the other Sitopsis species, most probably from Ae. searsii. The group compared the 19th intron (PI19) sequence of the PolA1 gene, encoding the largest subunit of RNA polymerase I. Two different sized DNA fragments containing PI19 sequences (PI19A and PI19G) were amplified both in ssp. timopheevii and ssp. armeniacum. The shorter PI19A (112 bp) sequences of both subspecies were identical to PI19 sequences of T. urartu and T. monococcum. Interestingly, the longer PI19G (241–243 bp) sequences of ssp. armeniacum showed more similarity to PI19 sequences of Ae. speltoides, whereas those of ssp. timopheevii showed more similarity to PI19 sequences of Ae. searsii.
Aegilops speltoides is in contact with T. urartu, the donor of the A subgenome, in southeastern Turkey, northwestern Iraq and western Iran. In these regions, there are also numerous mixed populations of these two species with wild T. timopheevii.
Yet, an interesting outcome of whole genome sequence of the Sitopsis species is the new insight on their relationship to the B and G subgenomes of allopolyploid wheats (Li et al. 2022). As previously shown by Marcussen et al. (2014), Glémin et al. (2019), the genomes of the Sitopsis species, the B and G wheat subgenomes, and the A. muticum genome fall into three clades corresponding to the A, B and D lineages. The A lineage consists of the genomes of diploid wheat and the A subgenomes of allopolyploid wheat. The B lineage includes the B subgenomes of the allopolyploid wheats, Ae. speltoides, and A. muticum (Glémin et al. 2019) and the G subgenome of T. timopheevii. The D-lineage includes the ancestral genomes of the subsection Emarginata species of Aegilops, the D genome and those of the remaining Aegilops species. The G subgenome sequence is not yet available, however, a substitution of most of chromosome 2B by an introgression from T. timopheevii (450 Mb in length) in the bread wheat cultivar (LongReach Lancer) whose genome has been sequenced (Walkowiak et al. 2020), enabled to include it into the phylogenetic analysis of the B lineage (Li et al. 2022). The timing of divergence between these genomes was determined based on full or partial genomic sequences. Interestingly, Ae. speltoides diverged from the B subgenome donor ~ 4.49 MYA. Considering that wild emmer wheat (genome BBAA) was formed ~ 0.8 MYA (Marcussen et al. 2014), this rules out that Ae. speltoides is the direct progenitor of the B subgenome A. muticum was confirmed as belonging to the B-lineage and diverged from Ae. speltoides and B-subgenome donor at a more ancient time (~6.37 MYA), supporting the proposal of Glémin et al. (2019) that A. muticum is the extant representative most directly related to the B-lineage ancestor. Ae. speltoides diverged from the T. timopheevii G-subgenome donor ~ 2.85 MYA, i.e., after its divergence from the B-subgenome progenitor. This makes the donor of the G-subgenome substantially older than the estimated allotetraploidization time (< 0.4 MYA) leading to speciation of ssp. armeniacum, the wild progenitor of T. timopheevii (Gornicki et al. 2014). From this analysis, Li et al. (2022) concluded that Ae. speltoides is also not the direct donor to the G-subgenome of T. timopheevii, although the latter is more closely related to the G- than to the B-subgenome. The donor of the G-subgenome is thus thought to be a distinct species related to Ae. speltoides, that is either extinct or yet undiscovered (Li et al. 2022). This is consistent with earlier reports (Ogihara and Tsunewaki 1988) showing that Ae. speltoides shares near identical cytoplasm with T. timopheevii but not with T. turgidum and T. aestivum.
Ssp. timopheevii contains 11.87 ± 0.630 pg 1C DNA (Eilam et al. 2008), similar to the amount of DNA in wild ssp. armeniacum (11.82 ± 0.071 pg 1C DNA); domestication seemingly had no effect on genome size in this species. The genome of T. timopheevii is larger than the genomes of most Aegilops allopolyploids but significantly smaller than that of T. turgidum (Eilam et al. 2008). This in accord with Rees and Walters (1965), who determined DNA amounts in tetraploid wheats and found significantly less nuclear DNA in T. timopheevii as compared to T. turgidum (ssp. durum). The 1C DNA content of the G-subgenome donor is expected to be close to that of Ae. speltoides since DNA amount in T. timopheevii is equal to the additive amount of 1C DNA of Ae. speltoides (5.81 pg) and that of T. urartu (6.02 pg) (Eilam et al. 2007).
The karyotypes of wild and domesticated forms of T. timopheevii have identical chromosome morphology (Bozzini and Giorgi 1969). Both contain two pairs of SAT chromosomes and two pairs of submetacentric chromosomes, while the rest of the pairs are metacentric chromosomes. The karyotype of T. timopheevii is quite different from the karyotype of T. turgidum; Bozzini and Giorgi (1969) observed differences in total chromosome length and arm ratio between the two species, particularly in the SAT chromosomes. Moreover, chromosomes with a median centromere are more frequent in T. timopheevii than in T. turgidum. The differences in chromosome morphology between the two tetraploid wheats, reinforce cytogenetic data showing that T. timopheevii and T. turgidum have different chromosome architectures.
Hutchinson et al. (1982), using C-banding technique, showed that the G subgenome chromosomes of the wild and domesticated forms of T. timopheevii were banded, whereas those of the A subgenome showed no bands. Only one of the two pairs of satellited chromosomes had strong heterochromatic bands. The G chromosomes paired less in the triploid hybrids between timopheevii and diploid wheats as compared to the A chromosomes. Upon assessment of the relationship between the genomes of T. timopheevii and T. turgidum ssp. dicoccon at meiosis in F1 hybrids between these two taxa, Hutchinson et al. (1982) concluded that the two species differ in the amount and distribution of heterochromatin and by several intra- and inter-subgenome translocations.
All the somatic chromosomes of domesticated T. timopheevii and those of two varieties of T. aestivum, were identified by Giemsa staining (Badaeva et al. (1986). Similar to the finding of Hutchinson et al. (1982), Badaeva et al. (1986) also found that the chromosomes of the A subgenome of T. timopheevii contained a small amount of heterochromatin located mainly in the centromeric region, whereas the chromosomes of the G subgenome contained large amounts of heterochromatin located in the telomeric, centromeric and intercalary positions. While chromosome 6G possesses a nucleolar organizer, that of chromosome 1G was translocated to chromosome 6A (Badaeva et al. 1986). Comparison of the C-banding patterns of T. timopheevii chromosomes with those of the homoeologous chromosomes of the A and B subgenomes of T. aestivum showed similarity between these chromosomes, although the G subgenome chromosome contained a larger amount of heterochromatin than the B chromosomes and exhibited differences in the location and size of these heterochromatic blocks. Studies of N-banded mitotic and meiotic chromosomes of T. timopheevii and T. turgidum revealed that the satellites are on the short arms of chromosomes 6A and 6G of T. timopheevii and of 1B and 6B of T. turgidum (Gill and Chen 1987; Badaeva et al. 1986),
Studies of C-banded somatic chromosomes of T. timopheevii (Hutchinson et al. 1982) and N-banded chromosomes of T. timopheevii and T. turgidum and studies of chromosome pairing in T. timopheevii x T. turgidum hybrids (Gill and Chen 1987) uncovered differences between these two species in several translocations. Such differences do not include translocation 5AL/4AL (Jiang and Gill 1994b; Maestra and Naranjo 1999) that both allotetraploid species inherited from T. urartu, the donor of the A subgenome to both species. In the emmer lineage, i.e., T. turgidum and T. aestivum, chromosome 4A showed three more species-specific rearrangements, i.e., translocation 4AL/7BS, a large pericentric inversion, and a paracentric inversion in the long arm. Neither translocation 4AL/7BS nor the pericentric inversion exists in T. timopheevii, and whether the paracentric inversion of 4AL is present in T. timopheevii could not be determined (Jiang and Gill 1994a, b; Gill and Chen 1987; Maestra and Naranjo 1999, 2000). C-banding analysis of meiotic pairing in interspecific hybrids, revealed four species-specific translocations in T. timopheevii (Maestra and Naranjo 1999). A double translocation involving the arms 1GS, 6AS, and 4GS is present in both domesticated and wild forms of T. timopheevii. Two more translocations between the 4GS/4AL and 3AL/4AL arms, which are present in domesticated lines, probably also exist in wild forms. In addition to the 1GS/6AS and 1GS/4GS double translocations, 4GS/4AL/3AL translocations were also identified (Jiang and Gill 1994b). Analysis of the wild and domesticated forms of T. timopheevii by sequential N-banding and genomic in situ hybridization, showed that chromosomes 6A, 1G and 4G were involved in A-G inter-genomic translocations in all six lines analyzed (Jiang and Gill 1994b). These chromosomes may have derived from a cyclic translocation that is species-specific to T. timopheevii. All the species-specific translocations of T. timopheevii and T. turgidum occurred at the tetraploid level (Maestra and Naranjo 1999, 2000).
Rodríguez et al. (2000b), using genomic in situ hybridization (GISH) and C-banding analysis of meiotic configurations in the F1 T. timopheevii x T. turgidum hybrids, found that four species-specific translocations (6AS/1GS, 1GS/4GS, 4GS/4AL, and 4AL/3AL) exist in T. timopheevii, and that T. timopheevii and T. turgidum differ in the pericentric inversion of chromosome 4A and the paracentric inversion of 4AL. Rodríguez et al. (2000b) concluded that both tetraploid species had undergone independent and distinct evolutionary chromosomal rearrangements.
Using C-banding analysis, Kawahara et al. (1996) studied the karyotypes at meiosis of F1 hybrids between different accessions of ssp. armeniacum, and found that out of 18 translocations, 12 were between the G-subgenome chromosomes, five were between G and A subgenomes and one was between A subgenome chromosomes. Within the G subgenome, chromosomes 4G and 6G had higher frequency of translocations than the other chromosomes. Evidently, the G chromosomes have cytologically diverged much more than the A chromosomes and that chromosome restructuring has played an important role in the formation of intraspecific diversity of ssp. armeniacum (Kawahara and Tanaka 1977, 1983; Badaeva et al. 1990, 1994; Kawahara et al. 1996). Seventy-nine accessions (58.5% of the studied accessions) had the same type of translocation, and the F1 hybrids between them exhibited complete chromosome pairing and regular meiosis. This translocation, considered as the standard translocation type, was found in all geographical regions, while other translocation types were mostly restricted to a single locality (Kawahara et al. 1996).
Zoshchuk et al. (2007) studied the distribution of the Spelt1 and Spelt52 repetitive DNA sequences on chromosomes of seven accessions of T. timopheevii ssp. armeniacum, two accessions of T. timopheevii ssp. timopheevii and one accession of T. kiharae (a synthetic amphiploid T. timopheevii-Ae. tauschii). Sequences of both repetitive DNA families were found mostly in the sub-telomeric chromosome regions of the G subgenome. The number, location and size of Spelt1 differed among the seven accessions of ssp. armeniacum, but were identical in the two ssp. timopheevii accessions and in T. kiharae. Spelt52 was detected in the sub-telomeric regions of chromosomes 1–4 of the G subgenome and its sites did not coincide with the Spelt1 sites. As with Spelt1, the distribution and signal intensity of Spelt52 varied in ssp. armeniacum, but were identical in ssp. timopheevii and T. kiharae. Comparison of the distributions of the Spelt1 and Spelt52 repeats in the G subgenome chromosomes of T. timopheevii and T. kiharae with those of Ae. speltoides, the putative donor of the G subgenome, revealed a decrease in both the number and size of the sites in the G subgenome. The decrease was assumed to result from repeat elimination during allopolyploidization and subsequent evolution of the allopolyploid wheats (Zoshchuk et al. 2007).
Adonina et al. (2015), using pSc119.2 (120 bp repeat from rye), pTa71 (45S RNA genes from T. aestivum), and pTm30 containing (GAA)56 microsatellite sequence from T. monococcum) as probes in FISH experiments, observed great differences in the presence and polymorphism in the sequences that bind these probes between domesticated T. timopheevii and wild and domesticated T. turgidum. ssp. timopheevii had pSc119.2 signals predominantly on the G subgenome chromosomes and on 1AL and 5AS of the A subgenome, whereas in T. turgidum, pSc119.2 hybridized to 1AS and 4AL in all lines and to 5AS, 5AL, and 2AL in some lines. The pTa71 probe detected the NOR regions on the short arm of chromosomes 6A and 6G in T. timopheevii, whereas in T. turgidum, they were located on 1BS and 6BS and smaller one on 1AS. The probe pTm30 hybridized to all T. timopheevii G subgenome chromosomes and only to one site, on 6AS, in the A subgenome, whereas among three wild accessions of T. turgidum, 4 conserved and 9 polymorphic (GAA)n sites were observed in the A subgenome. The (GAA)n loci found on chromosomes 2AS, 4AL, and 5AL in the wild forms, were retained in the domesticated form of T. turgidum (ssp. durum) and in T. aestivum.
Badaeva et al. (2016) developed a set of molecular cytogenetic landmarks, based on eleven DNA probes, to characterize the different chromosomes of T. timopheevii. They found that the pTa535 sequence, derived from T. aestivum, enabled identification of all the A subgenome chromosomes, whereas the G subgenome and some of the A subgenome chromosomes could be identified using the (GAA/CTT)n and pSc119.2 probes. The pAsSAT86, pAs1, Spelt-1 and Spelt-52 probes, as well as 5S and 45S rDNA, discriminated particular chromosomes or chromosomal regions. The distribution of (GAA/CTT)n, pTa-535 and pSc119.2 on T. timopheevii chromosomes was distinct from that of T. turgidum.
Several available DNA probes were tested in in situ hybridization experiments seeking to identify the chromosomes of T. timopheevii. Hybridization patterns generated by the (GAA)7 probe was consistent with the C-banding patterns, and enabled identification of 11 chromosome pairs. As reported by Badaeva et al. (2016), probes pAs1and pSc119.2 produced hybridization bands on all chromosomes; nine chromosome pairs were clearly distinguishable by pSc119.2, while pSc119.2 in combination with pAs1 identified all T. timopheevii chromosomes. Probing of the putative diploid progenitors with total genomic DNA clearly distinguished between both subgenomes.
In wheat, grain texture is mainly determined by the Hardness (Ha) locus consisting of the Puroindoline a (Pina) and b (Pinb) genes. These genes were conserved in all diploid species of Aegilops and Triticum, but were deleted from the A and B subgenomes of all T. turgidum lines studied (Li et al. 2008). In contrast to T. turgidum, Pina and Pinb were eliminated from the G subgenome, but were maintained in the A subgenome of T. timopheevii.
Upadhya and Swaminathan (1965) concluded that T. timopheevii does not contain the Ph1 gene that suppresses homoeologous pairing in interspecific wheat hybrids. Yet, studies of meiotic chromosomal pairing in 41- and 42-chromosome F1 hybrids between T. aestivum monosomic for chromosome 5B and the amphiplods T. timopheevii–Ae. tauschii, revealed that chromosome 5G of T. timopheevii compensated for the absence of 5B of T. aestivum, namely, it suppresses homoeologous pairing (Feldman 1966a). Thus, Feldman concluded that T. timopheevii contains a gene system, presumably Ph1, occurring on chromosome 5G, similar to that found in chromosome 5B of T. aestivum. Evidence that chromosome 5G of ssp. timopheevii carries a gene like Ph1 was also presented by Ozkan and Feldman (2001).
10.3.3.5 Theories Concerning the Phylogenetic Relationships Between T. timopheevii and T. turgidum
Since the designation of the genome of T. timopheevii GGAA (Lilienfeld and Kihara 1934), implying a genome different from the BBAA genome of T. turgidum, several theories were proposed concerning the evolutionary relationships between these two-allotetraploid wheats. Despite the intensive cytogenetic, biochemical and molecular studies, the phylogenetic relationships of these two-allotetraploid wheats still remain controversial and the question is to what extent the B and the G subgenomes are related is currently unresolved. The main theories concerning the relationships between these two-wheat species are presented below.
10.3.3.5.1 Theories Concerning Close Relationships Between the B and the G Subgenomes
Recent molecular studies show that the two allotetraploid species were formed in different times: wild emmer, T. turgidum ssp. dicoccoides, was formed 700,000–900,000 years ago (Marcussen et al. 2014; Gornicki et al. 2014; Middleton et al. 2014), and wild T. timopheevii, ssp. armeniacum, 400,000 years ago (Marcussen et al. 2014; Li et al. 2022). Wild emmer was formed via allopolyploidization process involving the B-subgenome donor, that diverged from Ae speltoides 4.49 MYA (Li et al. 2022), and the A subgenome donor that diverged from the T. urartu 1.28 MYA (Li et al. 2022). Wild ssp. armeniacum was formed from the G subgenome donor, that diverged from Ae. speltoides much later, 2.85 MYA (Li et al. 2022) and the A-subgenome donor. Since the formation of wild T. timopheevii was 300,000–500,000 years after that of wild emmer, the question is how much the B and the G subgenomes donor, both diverged from Ae. speltoides, and to a lesser extent the A subgenome donor, have diverged from one another.
Close genetic relationships between the B and the G subgenomes was suggested following observations of meiotic pairing in hybrids between the two-allotetraploid species or between T. timopheevii and T. aestivum (Sachs 1953; Wagenaar 1961a; Feldman 1966b; Tanaka et al. 1978). Sachs (1953) concluded that all the allotetraploid wheats originated from a common allotetraploid progenitor and that the hybrid sterility between T. timopheevii and T. turgidum was due to cryptic structural hybridity. This conclusion was supported by Sears (1956b), Riley et al. (1958). Wagenaar (1966) assumed that wild T. timopheevii arose from wild T. turgidum in northern Iraq, through a series of mutations which occurred simultaneously or in quick succession in both species and induced a strong sterility barrier between them. Several F1 hybrids between ssp. armeniacum and ssp. dicoccoides from a mixed stand in eastern Turkey and northern Iraq, showed considerably high chromosome pairing (Rao and Smith 1968; Rawal and Harlan 1975; Tanaka and Kawahara 1976; Tanaka et al. 1978), suggesting that the two wild allotetraploid wheats are phylogenetically closely related.
The possibility of close phylogenetic relationship between the two-allotetraploid wheat species was also supported by chromosome pairing in hybrids, reported by Upadhya and Swaminathan (1965), Feldman (1966b), Tanaka et al. (1978), and by isozyme studies performed by Jaaska (1974). Feldman (1966b) found that the G subgenome of T. timopheevii is sufficiently closely related to the B subgenome of T. turgidum and may have differentiated from the latter as a result of extensive chromosomal rearrangements. All the studied telocentric chromosomes of T. aestivum subgenome B paired to some extent with the corresponding chromosomes of T. timopheevii (Feldman 1966b), indicating that the second subgenome of T. timopheevii is close to subgenome B of T. turgidum. The relatively close relationship between these two subgenomes was especially conspicuous in the relatively high pairing in hybrids between T. timopheevii and some varieties of T. turgidum, as observed by Kostoff (1937a, b), Wagenaar (1961a), Rao and Smith (1968), Rawal and Harlan (1975). Likewise, Tanaka et al. (1978) suggested that these two allotetraploid wheat species had differentiated from a common ancestor as the result of extensive chromosomal differentiation. A similar conclusion was reached by Badaeva et al. (1986), following comparison of C-banding in T. timopheevii versus T. aestivum. They concluded that the G and B subgenomes have a common ancestor, from which they differentiated at the tetraploid level, due to chromosomal rearrangements and increased heterochromatinization in the chromosomes of the G subgenome of T. timopheevii.
None of the current diploid species of Triticum and Aegilops, from which wild T. timopheevii and T. turgidum presumably derived, possess a Ph1 gene identical to that of T. aestivum (Dhaliwal 1977c). This suggests that the Ph1 gene originated at the tetraploid level. The fact that this gene occurs in both allotetraploid species (Feldman 1966a; Dhaliwal 1977c; Ozkan and Feldman 2001)), may suggest that either the donors of subgenomes B and G possess the Ph1 gene, or a more likely alternative, Ph1 evolved in wild T. turgidum and was transferred to wild T. timopheevii via introgressive hybridization.
10.3.3.5.2 Theories Concerning More Distant Relationships Between the B and the G Subgenomes
Other researchers bearing in mind that T. timopheevii and T. turgidum originated in two independent events. The GGAA genomic formula assigned to T. timopheevii by Kihara and Lilienfeld (1934) and supported by Svetozarova (1939), Sears (1948), suggested that the G subgenome derived from a different species than the B subgenome of T. turgidum. The different species-specific chromosome rearrangements that occurred at the tetraploid level in both lineages, are consistent with a diphyletic origin (Tanaka and Ichikawa 1972; Tanaka and Ishii 1975; Kawahara and Tanaka 1977; Hutchinson et al. 1982; Badaeva et al. 1990, 1995; Naranjo et al. 1987; Jiang and Gill 1994a, b; Maestra and Naranjo 1999, 2000; Rodriguez et al. 2000b). The analyses of chloroplast DNA (Ogihara and Tsunewaki 1988; Miyashita et al. 1994), mitochondrial DNA (Terachi et al. 1990), and chloroplast and mitochondrial DNA (Wang et al. 1997), also reinforce the diphyletic origin. Phylogenetic relationships among the plastotypes (plastid genotypes) of the two-tetraploid wheat species and those of the five species of the Aegilops of section Sitopsis, suggested a diphyletic origin of ssp. dicoccoides and ssp. armeniacum (Miyashita et al. 1994). The plastotype of one Ae. speltoides accession was identical to that of ssp. armeniacum, while three of the plastotypes found in the other Sitopsis species were very similar, but not identical, to that of ssp. dicoccoides. These studies imply that two different, perhaps closely related, species were the donors of the cytoplasm to the two-tetraploid wheats.
Mori et al. (1995) studied intra- and inter-specific variations in nuclear DNA of 32 lines of ssp. dicoccoides and 24 lines of ssp. armeniacum by RFLP. The average genetic distance between the ssp. dicoccoides accessions was 0.0135 ± 0.0031 and between the ssp. armeniacum accessions was 0.0036 ± 0.0015, indicative of about a four-fold intraspecific variation in ssp. dicoccoides as compared to ssp. armeniacum. The genetic distance between the two species was 0.0482 ± 0.0022, and when corrected for intraspecific divergence was 0.0395, about three times that for ssp. dicoccoides and 11 times that for ssp. armeniacum. These results showed that in the wild state, ssp. dicoccoides and ssp. timopheevii are clearly differentiated and that ssp. dicoccoides has much greater variation than ssp. armeniacum, suggesting a relatively more recent origin for the latter and therefore, a diphyletic origin for these species.
Pairing between G subgenome and S genome chromosomes in T. timopheevii x Ae. speltoides hybrids reached a frequency much higher than pairing between B subgenome and S genome chromosomes in T. turgidum x Ae. speltoides hybrids and in T. aestivum x Ae. speltoides hybrids, and between B and G subgenome chromosomes in T. turgidum x T. timopheevii or T. aestivum x T. timopheevii hybrids (Maestra and Naranjo 1999; Rodriguez et al. 2000a). These results, demonstrating a higher degree of closeness between the G subgenome and S genome than with the B subgenome, are consistent with the claimed diphyletic origins of the two-allotetraploid species.
The diphyletic mode of origin theory is supported by the fact that B and G subgenomes derived from different, albeit related, diploid donors as female and from T. urartu as male. Subsequent introgressive hybridizations between the two allotetraploids, sharing the A subgenome and differing in the B and G subgenomes, may have led to further differentiation of the differential subgenomes (Zohary and Feldman 1962). In such hybrids, the two differentiated genomes, which have partial homologous chromosomes, can exchange genetic material and recombine. As a result of such hybridizations, the related differential subgenomes could have become more modified, acquired adaptive genetic combinations, leading to recombination of the B and G subgenomes. An intermediate types predicted by this hypothesis, was previously found by Sachs (1953) Wagenaar (1961a, 1966), Rao and Smith (1968), Rawal and Harlan (1975), and Tanaka and Kawahara (1976). Gornicki et al. (2014) provided molecular evidence that evolution of these allotetraploid wheats was also accompanied by chloroplast introgression. One accession of T. turgidum ssp. dicoccoides (G4991), for example, which showed high chromosome pairing with both T. turgidum and T. timopheevii (Rawal and Harlan 1975), carries the T. timopheevii chloroplast haplotype (H09) as a result of a cross between wild emmer and wild timopheevii. Conversely, wild T. timopheevii accession TA976 carries the emmer-lineage chloroplast haplotype (H04) (Gornicki et al. 2014).
10.3.3.5.3 An Independent Origin from Closely Related Donors
Up till now, it was accepted (e.g., Dvorak and Zhang 1990; Gornicki et al. 2014) that both, the B and the G subgenomes of the allotetraploid wheats derived from Ae. speltoides and therefore, their origin cannot be considered biphyletic. Likewise, Gill and Friebe (2002), proposed that two different genotypes of Ae. speltoides contributed to the formation of the allopolyploid wheats, one genotype participated in the formation of the T. turgidum–T. aestivum lineage and another in the T. timopheevii–T. zhukovskyi lineage. Yet, the two subgenome donors diverged from Ae. speltoides in different times and may have diverged considerably from each other in chromosome structure and cytoplasm. Moreover, these two species arose independently from two different allotetraploidization events, and as such, their origin can barely be considered monophyletic.
Hybridization between the two allotetraploids might have led to exchange of chromosomal material such as chromosome 4B of turgidum that is present in timopheevii; Gill and Chen 1987) and chromosome segments, including the possible transfer of the Ph1 gene from chromosome arm 5BL of turgidum to 5G of timopheevii (Feldman 1966a). Additional evidence for possible introgression between these two-species is evident from the high pairing (in 80% of the cells) between chromosome arm 2BL of Chinese Spring and the corresponding arm of T. timopheevii, and between chromosome arms 1BL and 5BL (in about 50% of the cells) with timopheevii chromosomes (Feldman 1966b). Hybridization with diploids, mainly Ae. speltoides or other Sitopsis species, might have led to further differentiation of the G and B subgenomes. This might align with the finding of Dvorak and Zhang (1990), who observed two bands of diagnostic restriction fragments of species of sub-section Emarginata of section Sitopsis in the allopolyploid wheats, which could be considered as evidence of introgression.
A similar conclusion was reached by Brown-Guedira et al. (1996), who studied the phylogenetic relationships between T. turgidum and T. timopheevii by assessing the genetic compensation capacity of individual T. timopheevii chromosomes that substituted missing chromosomes of T. aestivum. Six T. timopheevii chromosome substitutions were isolated: 6A (6A), 2G (2B), 3G (3B), 4G (4B), 5G (5B) and 6G (6B). The substitution lines had normal morphology and fertility. Their findings indicated a common origin for the two tetraploid wheat species, but because of the presence of a different spectrum of inter-genomic translocations, the authors concluded rightly that the two-species originated from separate hybridization events. Likewise, Kilian et al. (2007) using AFLP markers and haplotypes of several nuclear and chloroplast loci, revealed that both the B and the G subgenomes derived from Ae. speltoides at different times from different genotypes of Ae. speltoides.
Allopolyploidization in the wheat group was followed by rapid genetic and epigenetic changes (Feldman et al. 1997, 2013; Levy and Feldman 2002, 2004; Feldman and Levy 2005, 2009; 2012). The genetic changes, mainly elimination and duplication of various low-and high-copy DNA sequences, may have led to genomic rearrangements, which could have accelerated the cytological and genetic diploidization of the nascent allopolyploids. On the other hand, if recurrent allopolyploidization events occurred from different genotypes of the diploid parents, the magnitude of genomic reorganization could have also impeded the genetic flow between the newly formed allopolyploids (Maestra and Naranjo 2000).
T. turgidum is an older species than T. timopheevii and was suggested to have originated 700,000–900,000 years ago (Marcussen et al. 2014; Gornicki et al. 2014; Middleton et al. 2014), while wild T. timopheevii was formed 400,000 years ago (Marcussen et al. 2014; Li et al. 2022). The B subgenome of T. turgidum derived from a species that diverged from Ae. speltoides 4.49 MYA (Li et al. 2022) and the G subgenome of T. timopheevii from a species that diverged from Ae. speltoides 2.85 MYA (Li et al. 2022). Wild T. turgidum was formed in the southern Levant, whereas wild T. timopheevii originated in northern Iraq (Gornicki et al. 2014).
10.3.3.6 Intraspecific Hybrids Involving ssp. armeniacum and ssp. timopheevii
The F1 hybrid between ssp. armeniacum (mistakenly referred to as T. dicoccoides var. nudiglumus) and T. timopheevii had almost regular pairing at first meiotic metaphase (Table 10.8). A similar level of chromosomal pairing was observed in the F1 hybrid between ssp. armeniacum and ssp. timopheevii (Table 10.8). The multivalents observed in this hybrid by Tanaka and Ichikawa (1972) most probably resulted from reciprocal translocations occurring between the two studied lines of the two subspecies, rather than from homoeologous pairing. The high level of chromosomal pairing indicates the great homology between the genomes of the two subspecies of T. timopheevii.
10.3.3.7 Crosses with Other Wheat Group Species
Meiotic chromosomal pairing in the F1 hybrid ssp. timopheevi ix ssp. monococcum (2n = 3x = 21; genome GAAm) (Table 10.9) indicated that the A subgenome of ssp. timopheevii is closely related to that of ssp. monococcum.
Data of meiotic chromosomal pairing in F1 hybrids between ssp. timopheevii and diploid species of Aegilops, namely, Ae. speltoides (hybrid genome GAS), Ae. bicornis (hybrid genome GASb), and Ae. tauschii (hybrid genome GAD) are presented in Table 9.9. Shands and Kimber (1973) studied chromosomal pairing in F1 hybrids of ssp. timopheevii with high-, intermediate-, and low-pairing types of Ae. speltoides. In the hybrid with the high-pairing type they observed somewhat higher pairing than in the hybrids with the intermediate- and low-pairing types, but in the latter two hybrids pairing was also high. From these data, Shands and Kimber (1973) concluded that the G subgenome of T. timopheevii is very loosely related to the S genome of Ae. speltoides and most probably derived from it. Hybrids between ssp. timopheevii and the other two Aegilops species exhibited significantly lower pairing. A similar low level of pairing was reported in the hybrid ssp. timopheevii x Ae. caudata (0–5 bivalents; Kihara 1949). Low level of chromosomal pairing was also observed in the F1 tetraploid hybrids between ssp. armeniacum and Ae. peregrina (hybrid genome GASvU). The F1 hybrids between two lines of the wild subspecies of T. timopheevii and Ae. peregrina exhibited very low chromosomal pairing (Table 10.10). A hybrid with one line of ssp. armeniacum (line TIA28) had significantly lower pairing than the hybrid with another armeniacum line (TIA02). This pattern of pairing indicates that both subgenomes of Ae. peregrina (Sv and U) are not close to any of the two subgenomes of T. timopheevii.
Meiotic pairing in hybrids between T. timopheevii and different subspecies of T. turgidum indicated that only one subgenome in each species is closely related (Table 10.8). The level of chromosomal pairing in the F1 hybrid between hexaploid wheat T. aestivum ssp. aestivum and T. timopheevii ssp. armeniacum (hybrid genome BADGA and in the hybrid T. aestivum ssp. macha x T. timopheevii ssp. timopheevii (hybrid genome BADGA) included 7–14 bivalents (Kihara 1949), shows that T. timopheevii shares only one subgenome, subgenome A, with T. aestivum; the other three subgenomes, B, D, and G, are homoeologous.
10.4 Section Triticum (Speltoidea Flaksb.) (2n = 6x = 42)
10.4.1 Description of the Section
Section Triticum [Syn: Triticum L sect. Spelta Dumort; Triticum L. sect. Speltoidea Flaksb.; Triticum L. ‘congregatio’ Hexaploidea Flaksb.] contains two species: T. aestivum L. and T. zhukovskyi Menabde & Ericz. T. aestivum is an allohexaploid (2n = 6x = 42; genome BBAADD), whereas T. zhukovskyi is an allo-auto-hexaploid (2n = 6x; genome GGAAAmAm). The two species share subgenome A and differ by the other subgenomes. The cytoplasm of T. aestivum derived from the B-subgenome donor, a close relative of Ae. speltoides, and that of T. zhukovskyi derived from the G-subgenome donor which is closely related to Ae. speltoides. The donors of the B and G subgenomes are currently extinct or yet not discovered.
The two species contain only domesticated forms, except for var. tibetanum of T. aestivum ssp. aestivum which is a feral form that escaped from a domesticated cultivar of T. aestivum due to a mutation in one of the Br (brittle rachis) genes, leading to plants with fragile rachis. This subspecies is grown near edges of wheat and barley fields in Tibet (Shao et al. 1983; Guo et al. 2020). T. aestivum contains five domesticated subspecies, ssp. spelta, ssp. macha, ssp. aestivum, ssp. compactum, and ssp. sphaerococcum. ssp. aestivum (common or bread wheat) is the most important crop of wheat, constituting about 95% of global wheat production. It is cultivated in all wheat-growing regions of the world and mainly used for bread. The other extant domesticated subspecies of T. aestivum are locally grown. T. zhukovskyi is a small species and only grown as a minor crop in western Georgia. Thus, among the hexaploid wheats, two natural groups can be observed, reflecting a biphyletic process of evolution (Mac Key 1975).
10.4.2 T. aestivum L. (Genome BBAADD)
10.4.2.1 Description of the Species
Triticum aestivum L., known as Dinkel wheat, [Syn.: T. hybernum L.; T. sativum Lamarck.; T. vulgare Vill.; T. vulgare Host] is an annual, predominantly autogamous plant. Culms are erect and glabrous, hollow, with thin walls, nodes are sometimes hairy, 65–150 cm tall (excluding spikes), and with 4 to 6 internodes. The young shoots are erect, semi-erect, or prostrate. Leaf blades are flat and linear, glaucous, or more rarely, yellowish-green in color, and pubescent in most forms, but glabrous in some. The spikes are awned with short awns of uniform length all over, or only on the upper spikelets, or, in few forms, are awnless. Spikes are determinate, squarehead in cross section or lax, dense or lax, 4 to 18 cm long (excluding awns), with 14–30 spikelets. The rachis is tough and smooth, and fringed, with short hairs along its margins, and a few hairs immediately below the base of each spikelet. In some forms, the rachis is semi-tough and breaks into individual spikelets upon threshing. The spikelets are 10–15 mm long, solitary at the nodes, and glabrous or hairy. The top spikelet is fertile and at right angle to the plane of lateral spikelets, each spikelet contains 3–9 florets, and those near the center of the spike bear 2–5 grains, whereas those near the base or the tip of the spike contain 1–2 grains only. The glumes are oblong, asymmetrical in size, shorter than or almost equal in length to the rest of the spikelet, glabrous or pubescent, with white, yellow, red, brown, or blue-black, 6–11 mm long, with 5–7 nerves, and terminate with a short tooth or, in some of the bearded forms, extend into a slender, short awn (1–3 cm long). The lemmas are thin, rounded, and with 7–11 nerves. In bearded forms, they carry awns 5–10 cm long, usually straight, which are yellowish-white, reddish, black, or brown. The caryopsis is 5–10 mm long, 3.0–4.2 mm wide and 2.5–4.0 mm thick, free and non-adherent to the lemma and palea (free-threshing), but in some forms, is adherent to lemma and palea (hulled). The grains are white, yellow, orange, or red, generally plump, usually with a shallow furrow, and with a brush of hairs at the apex. The endosperm is flinty, semi-flinty, or mealy. The embryo is about 1/5 the length of the caryopsis (Fig. 10.7).
Plants and spikes of Triticum aestivum L.; a ssp. spelta (L.) Thell.; b ssp. aestivum cv. Chinese Spring on the left side and of an additional cultivar with awns on the right; c spikes of two cultivars of ssp. compactum (Host) MK (From Percival 1921); d ssp. sphaerococcum (Percival) MK; e ssp. tibetanum J. Z. Shao (feral wheat)
Currently, T. aestivum is the main cultivated wheat species, including bread (common) wheat and a number of domesticated forms, all of which are hexaploids with the BBAADD genome, and inter-fertile when crossed with one another. Mac Key (1954b) revised the classification of the hexaploid wheats based on genetic and agronomic features. He drew attention to the fact that the main differences between the various forms of T. aestivum are due to a small number of genes affecting the morphology of the plant, mainly the spike. Consequently, Mac Key (1954b) suggested to classify these forms at the intraspecific level as subspecies of T. aestivum rather than to consider them as separate species, as was done by several others (e.g., Dorofeev et al. 1980; Goncharov 2011). More specifically, Mac Key (1954b) classified T. aestivum as having five subspecies, two of which are hulled (glumed), ssp. spelta (L.) Thell., and ssp. macha (Dek. & Men.) Mac Key, and three of which are free-threshing, ssp. aestivum, ssp. compactum (Host) Mac Key, and ssp. sphaerococcum (Percival) Mac Key. The one feral form, semi-wild, ssp. tibetanum, presumably escaped from wheat cultivation of bread wheat in Tibet (Shao et al. 1983). Mac Key’s classification was adapted by van Slageren (1994), who found that it expresses the various groups as a botanical taxon, similar to the higher ranks of species and genus (van Slageren 1994).
Except for ssp. aestivum, which is of global importance, the other subspecies are only locally cultivated. The products of threshing in the hulled subspecies are individual spikelets, whereas free grains in the free-threshing ones. Currently, the hulled subspecies are cultivated as relic crops, while the free-threshing ones are more in extensive use.
The principal differences between the major forms of T. aestivum are due to one or two genes that affect gross morphology (Mac Key 1954b). Studies of the speltoid mutations occurring in ssp. aestivum and changing the morphology of the spike from a squarehead to lax and glumes from loose (free-threshing) to adherent (hulled type), showed already that these two traits were found to be genetically associated with a simple pattern of inheritance (Nilsson-Ehle 1917). Philiptschenko (1934) proposed that these two traits are controlled in T. aestivum by the genes q, which regulates the squarehead-spike and k, which suppresses speltoidy. Following the genetic association reported by Nilsson-Ehle (1917), Watkins (1940) assumed that q and k are closely linked, and Watkins and Ellerton (1940) showed that this is indeed the case. Through studies of induced deficiency-duplication mutants, Mac Key (1954a) found that the recessive q + k genes are in fact one codominant factor, which he named it Q. This factor was llocated to the long arm of chromosome 5A (Sears 1954). The phenotypic influence of Q proved to be much broader than merely suppression of its homoeologous counterpart q. It affects a large number of traits in roots, stems, leaves, and especially spikes. Investigations by Mac Key (1954a, b) showed that Q determines the main free-threshing and domestication-related traits distinguishing between free-threshing ssp. aestivum and the hulled ssp. spelta, and, as such, it is one of the most significant domestication loci. While Q on 5AL has the most significant contribution, other homoeoalleles (on 5BL and 5DL) were also shown to be involved in the domestication traits (Zhang et al. 2011).
Q is thought to be a central gene regulating floral development, encoding an AP2-like transcription factor that plays an important role in the activation of a number of genes in hexaploid wheat (Simons et al. 2006; Zhang et al. 2011). Actually, Q, being a transcription factor (Simons et al. 2006; Zhang et al. 2011), has a pleiotropically influence on several domestication-related traits in addition to free-threshing, such as spike density and length (square-head spike), fertility of the basal spikelets, glume shape and tenacity, glume keel formation, rachis fragility, plant height, spike emergence time, and chlorophyll pattern along nerves, as well as grain size and shape.
The mutation from q to Q presumably occurred at the tetraploid level, from where it was transferred to hexaploid wheat (Muramatsu 1986; Simons et al. 2006). It has been suggested (Dvorak et al. 2012) that the tetraploid parent of hexaploid wheat was a free-threshing form. This was also apparent from the fact that all the tetraploids with the genome BBAA, extracted from hexaploid cultivars, were free-threshing (Kerber and Rowland 1974). Muramatsu (1963) proposed that Q is a triplication of q, since five doses of q conferred the same phenotype as two doses of Q. However, Q was recently isolated and characterized (Faris et al. 2003; Jantasuriyarat et al. 2004; Simons et al. 2006), and was shown by Simons et al. (2006) to have likely arisen through a gain-of-function mutation, and not from a duplication of q. Q and q, differ by a single nucleotide (GAG in q and GCG in Q), leading to a change in one amino acid, namely, all q-containing forms had valine in position 329, whereas all Q-containing forms possessed an isoleucine at this position (Simons et al. 2006). Q is more abundantly transcribed than q (Simons et al. 2006). The higher expression of Q is in accord with the finding of Muramatsu (1963), who showed that extra doses (five or six) of q mimic the effect of Q in bread wheat. Increased transcription of Q was most obviously associated with spike compactness and reduced plant height, as in plants tetrasomic for chromosome 5A (Sears 1954). In fact, the increased transcription of Q is apparently not due to the valine by an isoleucine substitution at position 329, as originally thought (Simons et al. 2006), but to a SNP in miRNA 172 binding site (Debernardi et al. 2017). Subsequent work by Debernardi et al. (2017) showed that in fact the SNP within the miRNA binding site is the causal polymorphism for the functional difference between the Q and q alleles. This is consistent with Q dominance, and with the increased transcription due to the reduction of miRNA 172 suppressive effect (Debernardi et al. 2017).
The non-free-threshing trait in synthetic hexaploids, irrespective of whether their tetraploid parent carried Q or q, was linked to the Tg gene, derived from Ae. tauschii (Kerber and Rowland 1974). Monosomic and telosomic analysis of synthetic hexaploid lines revealed the presence of Tg, a partially dominant gene for tenacious glumes, on the short arm of chromosome 2D (Kerber and Rowland 1974). Some variation in the degree of glume tenacity was noted among the synthetic hexaploids; those having ssp. dicoccon as a parent and containing q and Tg were the most difficult to thresh. The interaction between Tg and Q was clearly demonstrated by extraction of the tetraploid component of a hexaploid wheat and then resynthesizing the hexaploid. The extracted tetraploids containing only the BBAA component of the original free-threshing hexaploids were also free-threshing. In further studies, crosses between the extracted free-threshing tetraploids and Ae. tauschii produced spelta-like (hulled) hexaploids. It was therefore concluded that the Tg gene of Ae. tauschii inhibits the expression of Q. The interaction between tg and Q, conferring the free-threshing character, is complementary (Kerber and Rowland 1974), with a requirement for presence of both tg and Q to obtain a free-threshing character in hexaploid wheat. Some variation in the degree of threshability occurs among the many lines of free-threshing hexaploid wheat (Kerber and Rowland 1974), which is assumed to reflect the different genetic backgrounds. The probability that the genotypes of Ae. tauschii which served as the progenitors of hexaploid wheat, possessed Tg—as apparently do all extant forms of this species—supports the above hypothesis that hulled, hexaploid wheats are more primitive than free-threshing hexaploids; they carried the Tg gene and, therefore, were non-free threshing (Kerber and Rowland 1974). The mutation from Tg to tg is presumed to have occurred at the hexaploid level.
Simonetti et al. (1999) found that while chromosome arm 2BS of wild emmer contains the Tg gene that determines tough glumes, that of domesticated emmer contains the tg allele, determining soft glumes. Thus, the free-threshing trait in tetraploid wheat is determined by two complementary genes, Q on 5AL and tg on 2BS (Simonetti et al. 1999). Faris et al. (2014) found that, in wild emmer, both chromosome arms 2AS and 2BS, carry Tg alleles, thus requiring a change of Tg to tg on 2AS as well, in order to obtain a free-threshing form. Further fine genetic mapping by Sharma et al. (2019) showed that emmer wheat contains two dominant homoeoalleles on 2A and 2B (Tg-A1 and Tg-B1), which together with the q wildtype allele are responsible for the non-free-threshing phenotype.
The key gene separating ssp. aestivum and ssp. compactum is C, dominant in compactum and recessive in aestivum (Nilsson-Ehle 1911), which is located on chromosome XX (currently 2D) (Unrau 1950). The major gene separating these two subspecies from ssp. sphaerococcum is S, which is dominant in aestivum and compactum and recessive in sphaerococcum (Ellerton 1939) and located on chromosome XVI (currently 3D) (Sears 1946). Hence, the major genes determining the differences between the subspecies of T. aestivum are described in Table 10.11.
T. vavilovii (Tumanian) Jakubz. (syn: T. vulgare Vill. var. vavilovii Tumanian; T. aestivum L. ssp. vavilovii (Tumanian) Sears), is a branching mutant discovered by Tumanian in 1930, as an admixture in a stand of a bread wheat landrace in Armenia. In the 1970s, it was also found as an admixture in Azerbaijan, by Mustafaev, and in Armenia, by Gandilyan. Plants with branched spikes of the vavilovii type were produced by Mac Key (1966), including in progenies of some intraspecific crosses. Stable mutants like vavilovii, that never were released as commercial cultivars, should be made synonyms under the cultivated subspecies from which they were isolated and not to regard them as a special species or subspecies (van Slageren 1994).
There are no wild hexaploid wheats, although feral forms of ssp. aestivum and ssp. macha are found. A feral form of ssp. aestivum, namely, var. tibetanum, presumably escaped from wheat cultivation in Tibet (Shao et al. 1983). This form has brittle rachis and grows as weed in edges of wheat and barley fields, but not in well-defined primary habitats. A feral form of ssp. macha, that grows as weed in edges of wheat fields, was identified in Georgia (Dekaprelevich 1961). Both of these forms are presumably feral derivatives of domesticated wheats, rather than a truly-wild taxa.
The free-threshing subspecies of T. aestivum, i.e., aestivum, compactum and sphaerococcum, are considered to be more advanced than the hulled subspecies spelta and macha. The primitive status of hulled T. aestivum is supported by the observation that artificial hybridizations between almost all subspecies of T. turgidum, either free-threshing or hulled, with all known races of Ae. tauschii, gave rise to hulled types (McFadden and Sears 1946; Kerber and Rowland 1974). The hulled subspecies, being the primitive forms, are the predecessors of the more advanced, free-threshing types. Among the free-threshing forms, ssp. aestivum gave rise to ssp. compactum and ssp. sphaerococcum through mutation. While ssp. aestivum is grown world-wide, ssp. compactum is grown today in restricted areas of Europe, the Near East and the north-western USA, and ssp. sphaerococcum is grown in parts of India and central Asia.
The genetic data which show that the first hexaploid wheats were hulled, spelt-like, and more primitive than the free-threshing subspecies, do not agree with the archaeological chronology. While free-threshing forms of T. aestivum were found at the middle of the 9th millennium BP and were abundant in the pre-historic Near East from the 8th millennium onwards, thus far, archaeological evidence of ssp. spelta dates to only one thousand years later. Neolithic, Near Eastern ssp. spelta is very rare, but there is evidence of spelta grains from Yarim Tepe II, northern Iraq, dating back to the 7th millennium BP and probably also from Yarim Tepe I, about one thousand years earlier (Kislev 1984). Earlier evidence for the existence of ssp. spelta is still missing. This discrepancy between the genetic and archaeological data posed some difficulties in tracing the early history of the hexaploid wheats. However, assuming that the first hexaploid wheats were hulled, their very low occurrence in the prehistoric remains of the Near East suggest their lack of advantage over domesticated emmer in that area. ssp. spelta is grown today in the Near East in extreme environments, such as the high plateau of west-central Iran, eastern Turkey, and Transcaucasia. This cultivation is possibly of an ancient origin. In central Europe, spelta appeared at ca. 4000 BP, about 2000 years later than forms of free-threshing hexaploid wheat. It could have been brought to Europe, where it replaced the free-threshing type in many sites of the upper Rhine region, particularly at high altitudes where extreme temperatures prevail. Alternatively, spelta could have arisen in the Rhine valley through mutation of Q to q, or tg to Tg, or as a result of a cross between a free-threshing hexaploid form and a hulled tetraploid form, ssp. dicoccon, both of which were grown in that area. The relatively wide distribution of ssp. spelta in central Europe in the past was presumably due to its winter hardiness and ability to out-yield the other crops on poor soils. It was also preferred for its good quality. Spelt wheat is still cultivated today in several areas of central Europe and in the plateau of western Iran.
Ssp. macha was derived from mutations in either ssp. spelta or from ssp. aestivum. Some forms of this subspecies may contain the C (compact spike) allele, but others contain the c allele for normal spike. It is cultivated in a restricted area in Transcaucasia.
Ssp. aestivum gave rise to ssp. compactum (club wheat) and sphaerococcum, through mutations. This assumption is based on the fact that no line of Ae. tauschii has been found to carry the compactum gene C or the sphaerococcum gene s, both of which are located on D-genome chromosomes (Rao 1972, 1977), indicating that these mutations appeared at the hexaploid level. The fact that hulled hexaploid wheat does not carry these genes, shows clearly that neither ssp. compactum nor ssp. sphaerococcum could have been the first free-threshing hexaploids. The lineage of ssp. compactum from ssp. aestivum, entails only a single mutation from c to C, believed to have occurred in the Near East. Subsequently, compactum was transported to Europe as an admixture with emmer-einkorn, and was established as the dominant form in several locations, such as in the Lake Dweller area in Switzerland. ssp. compactum is grown today in a few restricted areas of Europe, the Near East, and the northwestern United States. Similarly, ssp. sphaerococcum originated from a single mutation in aestivum (S to s). This mutation presumably occurred in an aestivum that had been carried eastward, since sphaerococcum has not been found in the prehistoric Near East and its culture nowadays is largely confined to India. ssp. sphaerococcum is known to have been in India as early as the 5th millennium BP, and currently grows, to some extent, in India and Pakistan.
T. aestivum originated southwest of the Caspian Sea (Wang et al. 2013). As man migrated to new areas, cultivated wheats encountered new environments, to which they responded with bursts of variation resulting in many endemic forms. Secondary centers of variation for tetraploids in the Ethiopian plateau and the Mediterranean basin and for hexaploids in the Hindu Kush area of Afghanistan, were described by Vavilov (1987). Transcaucasia is one such secondary center for both tetraploid and hexaploid types. Secondary centers of diversity are valuable to wheat breeders, as they present gene pools additional to those existing at the primary centers of variation. More recent studies are also pointing to the Caspian-sea origin of the D subgenome: whole genome analysis of a core collection of 278 accessions covering the eco-geographic distribution of Ae. tauschii, in arid and semi-arid habitats from central Asia, Transcaucasia to China, confirmed that the wheat D subgenome is mostly derived from the strangulata subgroup originating from the south Caspian-sea and further narrowing down the origin to accessions from the Mazandaran province (Zhou et al. 2021). A recent analysis of 242 Ae. tauschii accessions showed that a rare and distinct lineage (different from strangulata) from Transcaucasia also contributed ~ 1% on average to the current wheat D subgenome (Gaurav et al. 2021).
An enormous amount of variation has developed in T. aestivum, as reflected in its very wide morphological and ecological variation. This hexaploid wheat species exhibits a wide range of genetic flexibility, as shown in its adaptation to a great variety of environments. While tetraploid wheats, in keeping with their Near Eastern origin, are adapted to mild winters and rainless summers, the addition of the central Asiatic tauschii (genome D) must have contributed to the adaptation of hexaploid wheats to a more continental climate and northern latitudes. This could have greatly facilitated the spread of bread wheat into parts of Europe and through the highlands of Iran to central and eastern Asia.
10.4.2.2 Ssp. spelta (L.) Thell. (Dinkel or Large Spelt)
10.4.2.2.1 Description of Subspecies
Ssp. spelta, known as large spelt, Dinkel, or hulled 6 x wheat [Syn.: T. spelta L.; T. zea Host; Spelta vulgare Seringe; T. vulgare spelta Alef.; T. aestivum var. spelta (L.) L. H. Bailet; T. aestivum ssp. transcaucasicum Dorof. & Laptev], is an annual, predominantly autogamous, plant. Culms are erect, stiff, 60–120 cm long (excluding spikes), glabrous or pubescent, hollow and with thin walls. Leaf sheathes have few hairs or glabrous, auricles are very large, curved, and fringed, with long hairs, and ligules are membranous. Leaf blades are 30–60 cm long, glabrous or sparsely hairy, those of young plants are dark green, and relatively narrow, whereas the leaves of the older culms are pale greenish-yellow, and broader. The spikes are relatively long, 10–15 cm long, lax, straight or slightly curved, white, red, grey-blue or blue-black, determinate, and awned or awnless. Each spike possesses from 16 to 22 spikelets, which are usually well separated from each other on the rachis. The rachis is flattened and smooth, with hairy margins, with a very small or absent frontal tuft. It is semi-brittle at the nodes and breaks easily with pressure (as during threshing), with each spikelet carrying the rachis segment below it (wedge type) and/or beside it (barrel type). The spikelets are oval, 12–16 mm long, solitary at nodes, and glabrous or hairy. The top spikelet is fertile and at right angle to the plan of lateral spikelets. Each spikelet contains 3–4(–5) florets, those near the center of the spike bear 2 (rarely 3) grains, whereas those near the base or the tip of the spike contain 1 grain only. The Two glumes of each spikelet have a similar length, 8–12 mm long, white, yellow, red, brown, or blue-black, shorter than the spikelet, broad, with a truncate apex, 2 keels that are keeled all along, 11 nerves, with one ending in a short tooth or, in some of the awned forms, extending into a slender, short awn (1–3 cm long). The lateral nerve ends in a blunt bulge, which is always far from the apical tooth. The lemma is boat-shaped relatively thin, 9–13-mm-long, keeled above, and with 9–11 nerves. In the awned varieties, it terminates in a stiff, 6–8 cm long awn. Sometimes the lemma of the third flower bears a short, 2-cm-long awn. The palea is about as long as the lemma, oval, with two keels, 2 veins, and short hairs on their fringe. The caryopses is reddish, 7–10 mm long, with a flinty endosperm, and long and pointed at both ends. The apex is covered with a brush of white hairs, adhered to the palea and lemma and enclosed by the firm glumes (hulled type). The furrow of the grain is shallow. The weight of one thousand grains is 50–58 g (Fig. 10.7a).
The three domesticated hulled wheats, einkorn (T. monococcum ssp. monococcum), emmer (T. turgidum ssp. dicoccon), and spelt (T. aestivum ssp. spelta), are known as farro (Szabó and Hammer 1996; van Slageren and Payne 2013). In early times, the European ssp. spelta was not distinguished from domesticated emmer, and only during the thirteenth century, a distinction was made between the two crops (Percival 1921).
The hulled character of the three crops results from the semi-brittle nature of the rachis, and the toughness of the glumes. Because of these features, the products of threshing are not grain but rather individual spikelets. While in einkorn and emmer the rachis segment below the spikelet remains attached to the threshed spikelet, in spelt, the segment attached is either below or beside the spikelets or both. After threshing, an additional grinding process is required to separate the grain from the closely investing glumes (Percival 1921). This enclosure in the glumes of hulled wheats gives excellent protection to the grains against birds and animals and ensures extended viability of the grains (Nesbitt and Samuel 1996).
Ssp. spelta was formed, presumably repeatedly, in cultivated fields, as a result of hybridization between domesticated tetraploid wheat T. turgidum, and a diploid Aegilops species, Ae. tauschii, that infested cultivated fields of tetraploid wheat as weed (McFadden and Sears 1944, 1946; Kihara 1944). Such infestation of wheat fields, either tetraploid or hexaploid, by the weedy Ae. tauschii, also exists today in northern Iran (Matsuoka et al. 2008). All synthetic amphiploids turgidum–tauschii are hulled, similarly to spelt and irrespective of the threshability of the tetraploid parent (McFadden and Sears 1946; Kerber and Rowland 1974). Thus, the first hexaploid wheat would, therefore, have been a hulled wheat.
ssp. spelta exhibits wide morphological variation, mainly in spike awnedness, glume pubescent, glume and awn color and grain color (Percival 1921; Szabó and Hammer 1996). It contains many botanical varieties, which are classified according to the presence or absence of awns, presence or absence of hairs, and spike color (Percival 1921; Szabó and Hammer 1996).
Spelt distributes over two large geographical areas, Europe and Asia. While the European spelts are known for several millennia (ca. 4000 years), the Asiatic group was discovered in the 1950s (Kuckuck and Schiemann 1957). In fact, ssp. spelta had already been discovered earlier in Iran. In 1877, Andre Michoux saw spelt wheat growing wild north of Hamadan, western Iran, and, in 1807, Olivier (1807) found wheat, barley, and spelt in uncultivated areas northwest of Anah, on the right bank of the Euphrates, and mentioned that he had already seen such wheat several times in northern Mesopotamia. Both these finds are quoted by de Candolle (1886).
The Asiatic type presumably originated from the hybridization of tetraploid x Ae. tauschii and yielded the free-threshing wheat, ssp. aestivum, through mutation(s), whereas the European spelta apparently descended from a cross between ssp. aestivum and ssp. dicoccon (Tsunewaki 1968, 1971). To distinguish between these two spelt types, Kislev (1984) designated the Asiatic spelta “TgQ spelta” and the European spelt, carrying the tg gene, “tgq spelta”. Thus, a TgQ spelta arose as a result of crosses between Ae. tauschii and the free-threshing (naked) tetraploid wheat ssp. parvicoccum or ssp. durum, which presumably contained the Q factor (Muramatsu 1986). Only one mutation, from Tg to tg, was required to derive free-threshing hexaploid wheats from such spelta (Kerber and Rowland 1974). On the other hand, ssp. spelta formed from domesticated emmer and Ae. tauschii would have carried both the Tg and q alleles, supplying a double dosage for hulledness. Since the chance for the occurrence of mutations in both of these genes within several centuries is small, it is more likely that the first mutation, q to Q, occurred in domesticated emmer fields, forming naked tetraploid wheat, while the second mutation, Tg to tg, occurred in TgQ spelta fields, forming bread wheat. The synthetic spelta obtained by McFadden and Sears (1946), likely contained both factors responsible for hulledness, namely, q and Tg, as it was obtained by hybridization of the hulled domesticated emmer and Ae. tauschii.
After bread wheat and emmer were established in Europe, the European type of ssp. spelta appeared, mostly north of the Alps. This spelta, which carries q, could have been derived from bread wheat through a back-mutation of Q to q or, more likely, via hybridization with emmer wheat (genotype Tgqq), as suggested by Tsunewaki (1968, 1971). While the European ssp. spelta is of the tgq spelta type, some of the Iranian spelta contain Tg (Dvorak et al. 2012). Thus, on the basis of genetic data, one can explain how Kuckuck obtained free-threshing types, ssp. aestivum, among the progenies of crosses between Iranian and European spelt wheats (see Kuckuck 1964). A cross between a TgQ spelta and a tgq spelta yields, besides the two parental types, the two recombinants, tgQ and Tgq, with the former being a free-threshing type.
Flaksberger (1925) already proposed that the European spelt derived in Europe from bread wheat. Such a hypothesis suggesting an independent origin of European and Asian spelt, was confirmed by several biochemical studies. von Büren (2001), based on polymorphisms of two γ-gliadin genes in various diploid, tetraploid and hexaploid species of wheat, and Blattner et al. (2002), based on analysis of genes of high molecular weight glutenin subunits of European and Asian spelt, concluded that the European spelt originated from crosses of free-threshing hexaploid wheat and domesticated emmer. Support for this hypothesis was also presented by Poltoretsky et al. (2018), who reviewed literature dealing with the genetic evolution of the European and Asiatic groups of ssp. spelta.
10.4.2.2.2 Archaeological Evidence
Nesbitt and Samuel (1996) reviewed the early archaeological evidence of ssp. spelta in the Near East and in southeast Europe. As mentioned above, evidence of Neolithic Near Eastern spelt is very rare. One of the earliest pieces of evidence is from Yarim Tepe II, northern Iraq, dating back to the 7th millennium BP (Bakhteyev and Yanushevich 1980). Other forms of evidence are from the 7th millennium BP in Transcaucasia (Lisitsina 1984), from north of the Black Sea (Janushevich 1984). A large number of glume imprints of spelt from Moldavia date to between 6800 and 6500 BP (Körber-Grohne 1987), while Popova (1991) reports three minor Neolithic and Chalcolithic occurrences in Bulgaria. These findings led Zohary and Hopf (1993) to regard the archaeobotanical evidence from Transcaucasia and the Balkans as consistent with the hybridization of emmer and Ae. tauschii near the Caspian belt, and its travel to Europe by way of the north shore of the Black Sea. However, Nesbitt and Samuel (1996) questioned this conclusion. They drew attention to the facts that, in all the archaeological records from outside of Europe, spelt was usually present in small proportions as compared to the other wheats, and its identification criteria were poorly documented. The most common identification criterion of spelt in these wheat mixtures is the barrel-type of disarticulation. However, fragmentary remains of spelt spikelets can be difficult to distinguish from those of the Aegilops species that also have barrel-type disarticulation and are common weeds in wheat fields, namely. Ae. tauschii, Ae. cylindrica, Ae. crassa and Ae. juvenalis. While most of these Aegilops species grow in the Near East, Ae. cylindrica does grow north of the Black Sea and in the Balkan, which could account for some spelt identifications there. Hence, these records of spelt from outside of Europe are still doubtful (Nesbitt and Samuel 1996).
Spelt was discovered in the 1950s in central Iran, growing as a crop at elevations of 2000–2300 m (Kuckuck and Schiemann 1957). Both domesticated emmer and ssp. aestivum were also important crops in the same area (Kuckuck and Schiemann 1957). The presence of spelt in this Iranian region is either a remnant of the original spelt form, resulting from the ancient hybridization of T. turgidum and Ae. tauschii, or, alternatively, a relatively younger crop derived from a recent hybridization(s) of tetraploid wheat and Ae. tauschii or of ssp. aestivum and domesticated emmer.
The absence of spelt from archaeological remains of southwest and central Asia remains a mystery. While spelt is expected to be well adapted to the highlands of Turkey or Afghanistan, there are no ancient or modern records of its existence in these areas (Nesbitt and Samuel 1996). Perhaps spelt was replaced, shortly after its formation, by the free-threshing ssp. aestivum that derived from it by a mutation of Tg to tg, and, since it was free-threshing, it was preferred by the Near Eastern farmers.
In contrast to the Asiatic spelt, ssp. spelta appeared in central Europe about 1000 years later than forms of free-threshing wheat (Nesbitt and Samuel 1996). Spelt remains occur at later Neolithic sites (4500–3700 BP) in eastern Germany and Poland, Jutland and possibly two sites in southwest Germany (Körber-Grohne 1989). During the Bronze Age, it spread widely in northern Europe (Nesbitt and Samuel 1996).
Spelt wheat replaced the dense-ear, free-threshing type (thought to be ssp. compactum (Heer 1866) but suggested by Kislev (1979/1980) to a free-threshing tetraploid form) grown by the lake-dwellers in the upper Rhine region, particularly at high altitudes where temperatures were extreme. Alternatively, and more likely, it could have arisen in the Rhine valley as a result of a cross between a hexaploid dense-eared form and tetraploid ssp. dicoccon, both of which were grown in the area.
Spelt was not grown in Egypt, and all the currently available evidence suggest that it was not known to the ancient Greeks and Romans (Percival 1921; Nesbitt and Samuel 1996). No remains of spelt have been found in the Neolithic Age in Europe. Yet, spelt was an important staple in parts of Europe from the Bronze to medieval times. Currently, spelt wheat is a relic crop, with cultivation confined to small areas in Europe and Asia. In Europe, the largest volume is grown in Bavaria, where it has been cultivated from the earliest times instead of bread wheat. It is grown on a smaller scale in parts of Prussia, Hesse and Alsace. Some is also grown in Switzerland, Austria, northern parts of Spain, France, and Italy. Small amounts are also grown in north Africa. In Asia, it is grown in several regions in Iran, central Asia, and Transcaucasia (Kuckuck and Schiemann 1957; Dorofeev 1969; Zohary et al. 2012). Spelt was introduced to the United States in the 1890s, but during the twentieth century, it was replaced by bread wheat in almost all areas where it was grown. However, with the growing trend for organic agriculture and “health food”, there is increasing interest in this wheat. In addition to its higher nutritional value as compared to bread wheat, spelt is more tolerant to poor soil conditions, and resistant to a range of fungal diseases, such as smut, bunt, and rust. It is one of the hardiest of cereals, rarely affected by cold and frosts, and also grows well at all elevations. Because of its stiff culms, it is also more resistant to lodging than the other subspecies of hexaploid wheat and tolerates sprouting.
Although spelt is slightly less productive than bread wheat and possesses the disadvantage of a semi-brittle rachis and tough glumes, from which the grain cannot be easily threshed, it has advantages which enable it to compete successfully with bread wheat in areas with more marginal conditions. Its greater winter hardiness is of greatest importance. Another point in its favor is its smaller loss from attack of birds. Most spelt cultivars in Europe are winter forms, although a few less hardy spring varieties are also cultivated.
10.4.2.2.3 Nutritional Quality of ssp. spelta
The nutritional value of spelt is somewhat higher than that of bread wheat, with larger amounts of grain protein, dietary fibers, B vitamins and minerals (e.g., Suchowilska et al. 2019). In addition, Ruibal-Mendieta et al. (2005) found that ash, copper, iron, zinc, magnesium, and phosphorus contents were higher in spelt samples than in bread wheat. On the other hand, phytic acid content was 40% lower in spelt than in bread wheat. Analysis of two spelt cultivars showed differences in protein, iron and Zinc content (Rodríguez-Quijano et al. 2019).
Spelt has a relatively high-grain protein content, although a great variation of protein content, presumably due to different growing conditions, has been documented. The average grain protein percentage ranges from 12.7 to 19.0% (Belitz et al. 1989; Graber and Kuhn 1992; Perrino et al. 1993; Ranhotra et al. 1995; Cubadda and Marconi 1996).
The gluten of spelt flour is suitable for pastry, pasta, muesli, flakes, puddings, and soups. It is also used to make special kinds of bread. In comparison to hard red winter wheat of ssp. aestivum, spelt has a more soluble protein matrix, characterized by a higher gliadin:glutenin ratio. The subunits composition of high molecular weight glutenin shows extensive polymorphism, covering a large number of different allelic combinations in all loci. The wet gluten content in spelt varieties is about 40% higher than in a compared cultivar of bread wheat, but the quality of gluten in spelt varieties is lower. The total yield of flours in spelt varieties was only 70% of that of a check bread wheat cultivar (Capouchova 2001). In mean quality parameters, a marked difference was observed between the bread wheat and spelt cultivars, indicative of weaker gluten and dough in the spelt varieties studied.
In Germany and Austria, spelt loaves and rolls (Dinkelbrot) are widely available in bakeries, as is spelt flour in supermarkets. In addition, the unripe spelt grains are dried and eaten as green grain. In Poland, spelt breads and flour are commonly available as health foods and easy to find in bakeries (Defrise and Jacqmain 1984; Graber and Kuhn 1992; Boller 1995). Beer brewed from spelt is sometimes seen in Bavaria and spelt is distilled to make vodka in Poland.
Organic agriculture and health food products have been gaining increasing popularity (Cubadda and Marconi 1996; Lacko-Bartošová et al. 2010) and has revived spelt popularity, as consumption of spelt-wheat-based products provides for increased intake of minerals, vitamins and dietary fibers. With an important role in decreasing the glycemic index of final products (Lacko-Bartošová et al. 2010), spelt has become a common wheat substitute for making breads, pastas, and flakes.
10.4.2.3 Ssp. macha (Dek. & Men.) MK
Triticum aestivum ssp. macha, known as macha wheat [Syn.: T. Macha Dekapr. & Menabde; T. sativum spelta Hackl.; T. spelta ssp. macha (Dek. & Men.) Dorof; T. aestivum L. group macha Bowden] is an annual, predominantly autogamous, plant. Culms are erect, 60–100 cm long (excluding spikes), glabrous or pubescent, hollow, and thin-walled. The leaf sheath hairy, auricles are curved, and ligules are membranous. Leaf blades are 20–60 cm long, and 10–15 mm wide, with a scabrous, glabrous, or pubescent surface. The spikes are relatively compact, 10–12.5 cm long, 8–10 mm wide, bilateral, vary in density from open to dense, determinate, solitary at nodes, and glabrous or hairy, and bear short awns. The top spikelet is fertile and lies at right angle to the plane of lateral spikelets. Each spike possesses 15–23 spikelets. The rachis is flattened, hairy on the margins, and with a very small or absent frontal tuft. Spikelets are densely packed broadside to the rachis. Rachis internodes are oblong, 3–5 mm long, fragile (semi-brittle) at the nodes and break easily with pressure (as during threshing), with each spikelet carrying the rachis segment below it (wedge type). Spikelets are solitary, sessile, ellipsoid, laterally compressed, and 15–18 mm long, and are comprised of 2–3 fertile florets, of which the upper one is sterile. Glumes are similar in length and shorter than the spikelets. The lower glume is lanceolate, or elliptic; 10–11 mm long, with 2-keels, keeled all along. The surface of the lower glume is hairy, its apex bearing a unilateral tooth, truncate. The upper glume is lanceolate or elliptic, pubescent, and 10–11 mm long, with 2 keels, and lateral veins divergent at the apex, which has a truncate tooth. Lemma is ellipsoid, pubescent, 11–13 mm long, and keeled, with an acute, awned, 4.0–6.5 cm long. Palea are two –veined and keeled. The caryopsis is elliptical, red, intermediate in hardness, hairy at its apex, with a linear hilum, and adheres to the lemma and palea.
Ssp. macha was discovered in 1928 and described by Dekaprelevich and Menabde (1932). It is endemic to western Georgia, growing as a minor component in admixture with the hulled west Georgian tetraploid T. turgidum ssp. paleocolchicum (Dorofeev et al. 1980). The two taxa are morphologically similar and it is difficult to distinguish one from the other (Jakubziner 1959). The similarity is so great that Flaksberger (1938) considered them as one species. However, the leaves of ssp. macha are coarser than those of ssp. paleocolchicum. Being at two different ploidy levels, hybridization between ssp. macha and ssp. paleocolchicum is difficult and produces highly sterile hybrids, whereas it crosses relatively easily with different subspecies of T. aestivum, yielding a fertile progeny (Jakubziner 1959).
Bhaduri and Ghosh (1955) stated that although very restricted in distribution, ssp. macha shows remarkable diversity of forms, with as many as eight varieties already described. Mosulishvili et al. (2017) also noted the great morphological variation of ssp. macha, particularly in the brittleness of the rachis. They mention that 16 varieties were recognized in this subspecies.
Ssp. macha has been assumed to descend from ssp. palaecolchicum (Jakubziner 1959). Its discoverers, Dekaprelevich and Menabde (1932) regarded the two hulled subspecies of T. aestivum, ssp. macha and ssp. spelta, as closely related, resembling each other in the semi-brittleness of the rachis and the toughness of the glumes. Because of this variation, they consider ssp. macha as a basic polymorphic group from which ssp. spelta probably originated. However, it is distinct from ssp. spelta in the method of disarticulation of the rachis (Cao et al. 1997). In ssp. macha, disarticulation of the rachis, due to pressure during threshing, results in individual spikelets, with the rachis internode attached below each spikelet (like in emmer wheats; wedge type) (Kabarity 1966; Singh et al. 1957). In contrast, ssp. spelta frequently disarticulates into spikelets, each with the rachis segment beside each spikelet (like in Ae. tauschii; barrel type) (McFadden and Sears 1946). Another difference between ssp. macha and ssp. spelta is in the shape of the spike; in ssp. macha, the spike is dense, while ssp. spelta has a lax spike. By means of monosomic analysis, Joshi et al. (1980) allocated the gene which controls spike compactness in ssp. macha to chromosome 6B. A gene symbol Cm was proposed for this character, to distinguish it from the C gene of ssp. compactum, which is located on 2D. In addition, the F1 hybrids between spelta and macha exhibit some pairing failure at meiosis (Chin and Chwang 1944). Hybrids between macha and spelta or free-threshing T. aestivum are weak and are sterile, indicating that ssp. macha also differs cytogenetically from the other hexaploid wheats.
Poltoretsky et al. (2018) mentioned that according to several Russian scientists, ssp. macha was regarded as the likely parent of the free-threshing hexaploid subspecies of T. aestivum. This hypothesis is based on the fact that free-threshing forms are obtained among progenies of crosses between ssp. macha and Asiatic ssp. spelta. Conversely, in view of its limited distribution and its status as a minor crop component, Nesbitt and Samuel (1996) regarded ssp. macha as a local form that evolved in isolation, rendering it unlikely to have played any role in the evolution of the other forms of T. aestivum.
Tsunewaki (1971) determined the necrosis and chlorosis genotypes (Ne and Chl genes) of 13 lines of ssp. macha and 105 cultivars of ssp. spelta, by crossing them with appropriate testers. Results of this and previous investigations (Tsunewaki 1968) indicated that common wheat, ssp. aestivum, differentiated into two geographical populations, i.e., Asian and western. The Asian population is characterized by a high frequency of Ne1-carriers, while the Western population has more Ne2-carriers. A strong isolation barrier was found between ssp. macha and the other subspecies of T. aestivum, due to the complementary chlorosis genes, Chl and Ch2. Tsunewaki (1968, 1971) assumed that European spelt originated from Ne2-carrying free-threshing ssp. aestivum and q-carrying hulled ssp. dicoccon, while the origin of ssp. macha was assumed to have derived from crosses between ssp. aestivum and Chl-carrying ssp. dicoccon. Accordingly, at least, two independent introgressions of genes from domesticated emmer wheat seem to have played important roles in subspecies differentiation in hexaploid wheat.
Comparative and molecular genetic analyses suggest that macha wheat is a segregant from a cross between wild emmer wheat, ssp. dicoccoides, and bread wheat, ssp. aestivum (Tsunewaki 1968, 1971). These researchers suggested that it is likely that ssp. macha, as well as other west Georgian wheats, are sibling cultivars that arose in a hybrid swarm involving ssp. aestivum and wild emmer wheat. Corroborating this suggestion, Gornicki et al. (2014) found that the ssp. macha cytoplasm derived from the haplotype H04 of wild emmer cytoplasm.
The ssp. macha cytoplasm is of the B type, as that of the other subspecies of T. aestivum and T. turgidum (Wang et al. 1997). To assemble a phylogeny tree of Georgian allopolyploid wheats containing the B cytoplasm, Gogniashvili et al. (2018) determined complete nucleotide sequences of chloroplast DNA of 11 representatives of these wheats. According to the simplified scheme based on SNP and indel data, the predecessor of plasmon B (chloroplast DNA) is an unknown X taxon. Four lines were formed from this X taxon: one SNP and two inversions (38 and 56 bp) caused the formation of the paleocolchicum line, two SNPs formed the macha line, three SNPs formed the durum line, and four SNPs formed the carthlicum lines. The carthlicum line includes tetraploid subsp. carthlicum and hexaploid ssp. aestivum.
The hypothesis that the cytoplasm of ssp. macha derived from wild emmer, demands an explanation of how wild emmer and ssp. aestivum contacted each other. Wild emmer is native to the Fertile Crescent and is not found in Georgia and in other regions of the South Caucasus, and ssp. aestivum was formed northeast to the fertile Crescent, namely, in the southwestern belt of the Caspian Sea. One possible explanation is transfer of some wheat species and subspecies by current inhabitant of south Caucasus who lived several millennia ago in the Fertile Crescent area (Gogniashvili et al. 2018). It is also tempting to assume that early farmers (circa 1000–8000 years ago) brought various wheats into present-day Georgia and that wild emmer was brought as an admixture with domesticated emmer but did not established there.
Ssp. macha, one of the modern subspecies of T. aestivum, probably developed around 7000 years ago as a result of a cross between wild or domesticated emmer wheat, and ssp. aestivum. It is a late-maturing winter wheat and grows well in most well-drained soils. ssp. macha shows a good resistance to Fusarium head blight (FHB (Burt et al. 2015), and to common bunt (Tilletia tritici) and rust (Puccinia sp.) (Borgen 2010).
Ssp. macha is used as cooked seed, or ground into a flour and used as a cereal for making bread, and biscuits. Its straw is used as a biomass for fuel, for thatching, and as a mulch in the gardens. Fibers obtained from the stem are used for making paper.
10.4.2.4 Ssp. aestivum (Bread or Common Wheat)
10.4.2.4.1 Description of Subspecies
T. aestivum L. ssp. aestivum, also known as bread wheat or common wheat [Syn.: Triticum aestivum L. (bearded); T. hybernum L. (beardless); T. sativum Lam.; T. vulgare Vill.; T. sativum Pers.; T. cereale Schrank.; Frumentum triticum E. H. L. Krause] is an annual, predominantly autogamous, plant. Culms are erect, vary in length from 60 to 150 cm (excluding spikes) (50 cm dwarf wheat; 80–100 cm semi-dwarf wheat, 140–150 cm standard-height wheat), usually hollow and with thin walls, but in several forms, they are solid, possessing 5–6, glabrous internodes, nodes sometime are hairy. The young shoots are erect, semi-erect, or prostrate. Leaf blades are 20–60 cm long, 10–20 mm wide, flat and linear, usually glaucous, or more rarely, yellowish-green, and pubescent in most forms, but glabrous in a few. The spikes are either awned all over with short awns of uniform length or, only awned on the upper spikelets in the forms called beardless; very few forms are truly awnless. Spikes are determinate, squarehead in cross section, dense or lax, 6–18 cm long (excluding awns), with 14–30 spikelets. The rachis is tough, not brittle, and smooth, and fringed with short hairs along its margins, with a few hairs immediately below the base of each spikelet. The spikelets are 10–15-mm-long, solitary at the nodes, and glabrous or hairy. The top spikelet is fertile and at right angle to the plane of the lateral spikelets. Each spikelet contains 4–9 florets, and those near the center of the spike bear 3–5 grains, whereas those near the base or the tip of the spike contain 1 or 2 grains only. The glumes are oblong, asymmetrical in size, shorter than or almost equal in length to the rest of the spikelet, glabrous or pubescent, with white, yellow, red, brown, or blue-black color, 6–11 mm long, with 5–7 nerves, terminating in a short tooth or, in some of the bearded forms, extend into a slender, short awn (1–3-cm-long). The lemmas are 10–15 mm long, thin and pale, rounded on the back, with 7–11 nerves, In bearded forms, they carry awns 5–10 cm long, are usually straight, and yellowish-white, reddish, black, or brown. The caryopsis is 5–9 mm long, 3.0–4.5 mm wide, 2.5–4.0 mm thick and free and not adherent to lemma and palea (free-threshing). The grains are white, yellow, orange, or red, generally plump, usually with a shallow furrow, and with a brush of hairs at the apex. The endosperm is flinty, semi-flinty, or mealy. The embryo about 1/5 the length of the caryopsis (Fig. 10.7b).
Ssp. aestivum, bread wheat, is by far the most economically important wheat growing today on a world-wide scale. It is the most widely adapted crop, growing in diverse environments and climates, from 67˚ N in Norway, Finland and Russia, to 45˚ S in Argentina, but in the tropics and subtropics, its cultivation is restricted to higher elevations (Feldman et al. 1995). The world’s main wheat-producing regions are north-central China, southern Russia and the Ukraine, the central plains of the USA and adjacent areas in Canada, northwest Europe, the Mediterranean basin, India, Argentina and south-western Australia. Based on growth habit, wheat is classified into spring wheat and winter wheat, covering about 65% and 35% of the total global wheat production area, respectively (Braun et al. 2010).
Bread wheat is high-yielding in a wide range of ecosystems, and, as such, accounts for about 95% of world wheat production (durum wheat comprises the other 5%). It is the most important staple food of about two billion people (35% of the world population), providing nearly 55% of the carbohydrates and 20% of the food calories consumed globally. It is grown on more land area than any other food crop (219 million hectares in 2021), and in 2021, worldwide annual wheat production reached a record of ~ 770 mt with China and India as the top 2 producers (Table 10.12). Global demand for wheat is increasing due to the unique viscoelastic and adhesive properties of gluten proteins, which facilitate the production of processed foods, whose consumption is increasing as a result of the worldwide industrialization and adoption of western diet in the east (Shewry and Hey 2015; Day et al. 2006).
10.4.2.4.2 Genetic Diversity and Genetic Erosion
Having originated from a small number of genotypes of the parental species, the nascent bread wheat harbored only a small fraction of the genetic diversity of its parental species. Yet, recurrent formation over time from different genotypes of the parental species (Caldwell et al. 2004; Pont et al. 2019) and gene flow via introgressive hybridizations from different domesticated and wild wheat taxa, different genotypes of Ae. tauschii, and from various other wild relatives, have increased considerably the genetic base of ssp. aestivum. Moreover, from the time of its origin in west Asia ssp. aestivum was taken to many parts of the globe where it had to adapt to a wide range of new climatic, edaphic and biotic conditions on the one hand, and to different human demands on the other. This exerts strong stresses to which ssp. aestivum could adapt thanks to its exceptional capacity to sustain high dosage of mutations (Dvorak and Akhunov 2005; Akhunov et al. 2007), enabling its spread to new environments. The cultivation of this subspecies in many parts of the world in admixtures of genotypes, facilitated inter-genotypic hybridizations and establishment of new recombinant types. Selection under domestication by different farmers, seeking different nutritional profiles, for different end-uses in different regions of the globe, brought about additional variation.
The fast increase in genetic diversity of bread wheat has also aided by its genetic structure, reinforced by a diploid-like meiotic cytological behavior and predominantly self-pollination. These features have proven a very successful genetic system, facilitating a rapid build-up of genetic diversity. Being a hexaploid, most of the gene loci are present in six doses, and the accumulation of genetic variation through mutations or hybridizations is tolerated more readily than in tetraploid and diploid species. Moreover, allopolyploidy facilitates genetic diploidization—the process whereby genes existing in multiple doses can be diverted to new functions. Furthermore, its system of predominant self-pollination could have helped in the fixation of desirable mutants and recombinants resulting from rare outcrossing events. Thus, hexaploid wheat can accumulate a significant amount of genetic variability through mutations, hybridizations and introgressions. Mutability may have been triggered and accelerated by the activity of various factors, such as transposable elements, gametocidal genes, and genome-restructuring genes that induce various kinds of chromosomal rearrangements and mutations (cf. Kashkush et al. 2002, 2003; Endo 2007; Feldman and Strauss 1983). Activation of these elements by various stresses, such as new, unexpected and extreme environmental conditions might have been of critical significance in the build-up of the genetic diversity of this crop.
Hybridization has also played an important role in building up the genetic variation in ssp. aestivum. For thousands of years, farmers have been growing admixtures of different genotypes of land races in polymorphic fields. Such admixtures allow gene flow between different genotypes, creating new genetic combinations, some of which were better adapted to the farmer requirements in specific regions. Moreover, some admixtures included, in addition to bread wheat, other subspecies of T. aestivum, e.g., compactum and spelta, and even different representatives of T. monococcum and T. turgidum (Zeven 1980; Feldman 2001), thus facilitating massive intra- and inter-specific gene flow.
The B and A subgenomes of wild emmer are homologous to the B and A subgenomes of ssp. aestivum and the genome of Ae. tauschii is homologous to the D subgenome. Hybrids between wild emmer or Ae. tauschii and bread wheat are semi-fertile, or sterile, respectively, but a few seeds are produced upon backcrossing to the hexaploid parent. Further backcrossing may fully restore fertility. So, genes can be transferred from these wild forms into bread wheat chromosomes at hybrid meiosis simply through crossing over. The cultivation of hexaploid wheat in the Near East next to stands of wild emmer for more than 8000 years facilitated the production of many hybrids and hybrid swarms, resulting in almost constant gene flow from the wild into the domesticated background. Even today, spontaneous hybridizations between bread wheat and wild emmer have been described (Percival 1921; Zohary and Brick 1962).
Highly sterile hybrids have also been frequently obtained as a result of hybridizations between bread wheat and more distant diploid and tetraploid species of Aegilops (see Kimber and Feldman 1987), as well as species of Secale, Elymus, Haynaldia and other related Triticeae genera which grew within or near wheat fields. The few seeds that these hybrids produce upon backcrossing yield more-fertile plants. Such occasional intergeneric hybridizations may often result in successful introgression, thereby maintaining a weak but constant flow of genes into the hexaploid domesticated background.
Pont et al. (2019) used exome sequencing of a worldwide panel of almost 500 genotypes selected from across the geographical range of the wheat species complex, to explore how 9000 years of hybridization, selection, adaptation and plant breeding shaped the genetic makeup of modern bread wheats. They observed considerable genetic variation at the genic, chromosomal and subgenomic levels, and used this information to decipher the likely origins of modern-day wheats, the consequences of range expansion and the allelic variants selected since its domestication. Zhou et al. (2020a, b), evaluating nucleotide diversity of bread wheat and its progenitors, found that the genetic bottleneck of bread wheat, resulting from allopolyploidization, has been largely compensated by a massive gene flow from multiple groups of tetraploid wheat and wild relatives. According to them, the extent of introgression in bread wheat genome is much higher than it in other species; about 13–36% of bread wheat genome was directly contributed by introgressions from other wheats, including wild emmer, and various other wild relatives. The increase of genetic diversity from alien introgression has been essential to the global expansion of bread wheat. Their study confirmed earlier studies showed that bread wheat has asymmetric distribution of nucleotide diversity on the three subgenomes, with diversity in B being greater than in A, and in A being greater than in D. Reinforcement of these findings was recently provided by He et al. (2019), Cheng et al. (2019), who showed that introgression from wild emmer is one of the primary reasons for the relatively high diversity of the B and A subgenomes in bread wheat. Indeed, bread wheat adaptability to diverse environments and end-uses is surprising, given the diversity bottleneck expected from the allopolyploid speciation events (Dubcovsky and Dvorak 2007). Buckler et al. (2001) reviewed the present knowledge of molecular diversity among the grass crops and relate diversity mainly to genes involved in domestication and to yield gains.
As an outcome to increased mutability and introgression, bread wheat exhibits a large amount of morphological, physiological, biochemical, and molecular variations. This subspecies surpasses all other wheats in the number of forms and cultivars that have been classified on the basis of morphological, physiological, and quality traits; more than 25,000 different cultivars have been produced up to the 1990s of the 20th Century (Feldman et al. 1995). Already in 1921, Percival (1921) wrote, in his comprehensive book on wheat, that this wide variation resulted from a collection of mutants and hybrids, which originated from intraspecific (between races and cultivars), interspecific (with other wheat species) and intergeneric hybridization (with wild relatives, e.g., several closely related Aegilops species).
Under modern conditions, the wheat field has become genetically uniform so that spontaneous gene exchange between different genotypes is less likely. On the other hand, gene migration has been greatly increased by world–wide introduction and exchange of cultivars. At the same time, new techniques have become available for the identification and introduction of desirable genes from one cultivar to another, as well as from wild to domesticated type. But, until now, hybridizations have mainly been confined to intraspecific crosses and relatively little use has been made of diploid and tetraploid gene pools of wild and domesticated taxa in improvement of the bread wheat (Feldman and Sears 1981).
Today’s selection techniques can achieve the objectives of the primitive farmer with much greater certainty. High-yielding cultivars owe their improved performance to genetic increases in the number of fertile florets in the spikelet, to the size of the ear and to the number of ears per plant. This is, to a large extent, determined by the harvest index, and the ratio of grain to straw weight, but is also much influenced by resistance to diseases and pests and to loss by lodging and shattering or by ability of the crop to utilize heavy doses of nitrogenous fertilizers, with the effects of these components largely interrelated.
Still, the diversity in bread wheat is only a fraction of that in its parental species. Haudry et al. (2007) reported that the diversity of bread wheat is only 69% of that of its tetraploid parent. Also, it has been estimated that the genetic diversity of the D subgenome of modern bread wheat cultivars only accounts for 15% of that of Ae. tauschii growing in the Transcaucasia area (Dvorak et al. 1998a, b). Talbert et al. (1995) observed that the amount of DNA sequence variability in wheat is low, although somewhat more variability existed in the B subgenome than in the D subgenome. Estimates of RFLP diversity at the RbcS loci have indicated that bread wheat has perhaps 30% of the diversity levels found in its diploid relatives, but there are substantial differences between the A, B, and D subgenomes; the A subgenome was somewhat more polymorphic than the B subgenome, while the D subgenome was the most conserved (Galili et al. 2000). Akhunov et al. (2010) estimated nucleotide diversity in 2114 wheat genes and found it to be similar in the A and B subgenomes and reduced in the D subgenome. Nucleotide diversity varies within a subgenome, and along chromosomes. Low diversity was always accompanied by an excess of rare alleles (Akhunov et al. 2010). Whole-genome shotgun sequencing of the bread wheat genome indicated that upon allopolyploidization and domestication, between 10,000 and 16,000 genes and several gene families were lost in hexaploid wheat, compared with its three diploid progenitors, (Brenchley et al. 2012). At the same time, several classes of gene families with predicted roles in defense, nutritional content, energy metabolism, and growth increased in size in the domesticated wheats, possibly as a result of selection during domestication (Brenchley et al. 2012).
A major advance in wheat productivity was achieved in the1960s, following a cross by an American breeder, Orville Vogel, of an economically unimportant dwarf Japanese cultivar Norin 10, with the North American winter wheat cultivar Brevor. This led to the release in 1961 of the high-yielding cultivar Gaines, which was widely used as a parent by breeders in US and western Europe. Under the leadership of Norman E. Borlaug at the International Maize and Wheat Improvement Centre in Mexico (CIMMYT), Norin 10 was crossed with spring varieties, resulting in the production of high-yielding, semi-dwarf wheats which became the basis of the Green Revolution in India, Pakistan, Iran, and the Mediterranean basin. By the end of the twentieth century, 81% of the developing world’s wheat area was grew semi-dwarf and dwarf wheats, giving both increased yields and better response to nitrogenous fertilizer.
Modern varieties of bread wheat have short stems (semi-dwarf wheat is about 80–100 cm tall and dwarf wheat is 50–60 cm tall), due to Rht dwarfing genes that reduce the plant’s sensitivity to Gibberellic acid (Gale and Youssefian 1985; Lenton et al. 1987; Youssefian et al. 1992). Short stems are important because harvest index (the proportion of grains to the straw) is improved and they allow for the application of high levels of chemical fertilizers that in traditional tall wheat (140–150 cm tall), would cause lodging of the stems, and consequently, loss of yield (Brooking and Kirby 1981).
During the green revolution, in the 1960s, numerous polymorphic traditional admixtures were replaced in many parts of the globe by a small number of elite high-yielding cultivars, each grown mono-genotypically on large areas. A very large number of the land races was not preserved and their germ plasm was lost, causing a massive erosion in the bread wheat gene pool. Awareness among wheat geneticists and breeders of the negative effects of this erosion has been increasing (e.g., Feldman and Sears 1981; Feldman et al. 1995; Feldman 2001). Yet, based on the high mutation rates in hexaploid wheat and the buffering effects caused by allopolyploidy, Dubcovsky and Dvorak (2007) pointed out that the loss in bread wheat diversity can be reverted to some extent. In fact, Warburton et al. (2006) showed a recovery in genetic diversity among the most modern CIMMYT lines. The extent of this recovery is however not an absolute trend in all breeding programs and in spite of recent advances, some traits of interest may have been neglected (Nazco et al. 2014b).
Ssp. aestivum originated and entered cultivation only after the more or less simultaneous domestication of diploid and allotetraploid forms. In the past, archaeological remains of ssp. aestivum were difficult to separate from those of free-threshing forms of T. turgidum. Grain shape, that was considered a valuable diagnostic trait, proved to be problematic because tetraploid and hexaploid wheats overlap considerably in this trait (Zohary et al. 2012). This overlap is more prominent in archaeological remains, because of swelling and other deformations caused by charring (Hopf 1955; van Zeist 1976; Harlan 1981). Similar difficulties have been encountered with the shape of the scutellum, which, although it is somewhat morphologically different in tetraploid versus hexaploid free-threshing wheats, it exhibits some overlapping in grains of these to taxa. For these reasons, most archaeobotanists in the past did not attempt to distinguish between tetraploid and hexaploid free-threshing wheats and tended to group them together as ‘aestivo-compactum’ or T. turgidum-T. aestivum finds (Zohary et al. 2012). Yet, Hillman (2001) showed that archaeological remains of free-threshing T. turgidum can be separated from free-threshing T. aestivum by the morphology of their rachis segments, enabling a more precise identification of the two forms in the archaeological remains.
Ssp. aestivum appears in archaeological data from the middle of the 9th millennium BP. The earliest finds were at Can Hasan, south Anatolia (see Hillman 1996). Free-threshing forms of ssp. aestivum were abundant in the prehistoric Near East, from the 8th millennium BP onwards. Indeed, finds from the 8th millennium BP, identified as ancestral forms of free-threshing ssp. aestivum, have been unearthed at Tepe Sabz in Iranian Khudistan, at Tell Sawwan in Iran, at Çatal Huyük in central Anatolia, in Haciar in west-central Anatolia and at Knossos on Grete (Kislev 1984). Between 8000 and 7000 BP, ssp. aestivum penetrated, together with domesticated emmer, into the irrigated agriculture of the plains of Mesopotamia and western Iran. In the 7th millennium, it appeared also in finds from the central and western Mediterranean basin. Dense forms of ssp. aestivum, sometimes mixed with ssp. compactum, were cultivated in central and western Europe at the end of the 6th millennium BP, where they were found associated, together with einkorn and emmer, with the first traces of agricultural activities. Bread wheat first reached North America with Spanish missions in the sixteenth century, and Australia in 1788, with the arrival of the colonists.
While tetraploid wheats, in keeping with their Near Eastern origin, are adapted to mild winters and rainless summers, the addition of subgenome D from the central Asiatic species Ae. tauschii, must have contributed to the adaptation of hexaploid wheats to a more continental climate and northern latitudes. This could have greatly facilitated the spread of bread wheat into parts of central, eastern and northern Europe and through the highlands of Iran, to central and eastern Asia.
The bread wheat grain contains most of the nutrients essential to man. It contains 13% water, 60–80% carbohydrates (mainly as starch), 1.5–2.0% fat, 8–15% protein, including adequate amounts of all amino acids except lysine, tryptophan and methionine which exist in relatively small amount, 1.5–2.0% minerals, and vitamins such as the B complex and vitamin E (Table 10.13). Of the protein, 75–80% is gluten. Each 100 g of bread wheat provides 327 cal and is a rich source of multiple essential nutrients, such as protein, dietary fiber, Manganese, Phosphorus, and Niacin. Significant quantities of several B vitamins and other dietary minerals are also present (Table 10.13).
Wheat is an important source of carbohydrates and the leading source of vegetable protein in human food (Shewry and Hey 2015) (Table 10.13). While wheat protein content is relatively high compared to that of other major cereals, it is of relatively low protein quality with low levels of essential amino acids. In addition, in a small part of the general population, gluten—the major part of wheat protein—can trigger Coeliac disease, non-celiac gluten sensitivity, gluten ataxia and Dermatitis herpetiformis (Ludvigsson et al. 2013).
Because of the high gluten content of its endosperm, bread wheat, especially its harder grained cultivars, are highly valued for bread making. The sticky gluten protein entraps the carbon dioxide formed during yeast fermentation and enables the leavened dough to rise. Nowadays, bread wheat is a central ingredient in foods such as bread, porridge, crackers, biscuit, muesli, pancakes, pie, pastries, Pizza, cake, cookies, muffins, rolls, doughnuts, gravy, beer, vodka, boza (a fermented beverage) and breakfast cereals. Worldwide, bread wheat has proven highly adaptable to modern industrial baking, and has displaced many of the other wheat, barley, and rye species that were once commonly used for bread making, particularly in Europe. The most common forms of ssp. aestivum are white and red wheat. In North America, bread wheat is classified dark-colored or light-colored. The dark-colored bread wheats include Hard Red Winter, characterized by grain, brownish color, and high protein content, and used for bread, and other baked goods and the Hard Red Spring, characterized by hard grains, brownish color, and high protein content, used for bread and other baked goods. The light-colored bread wheats include the Soft Red Winter, which is soft, low-protein wheat, used for cakes, pie crusts, biscuits, and the Hard White, which is hard, light-colored, opaque, chalky, medium-protein wheat, used for bread and brewing, and the Soft White, which is soft, light-colored, very low-protein wheat grown in temperate moist areas, used for pie crusts and pastry.
In addition to its high nutritive value, the low water content, ease of processing and transport and good storage qualities of the bread wheat crop have made it the most important staple food of about 35% of the world’s population. There is an increasing demand for wheat in countries undergoing urbanization and industrialization. As a result, over the last 70 years, the global wheat area has increased by 50%, reaching 220 Mha in 2014. During the same period, average yields increased, mainly due to broader use of fertilizers and improved cultivars. In 2017, global wheat production was 772 million tones (MT), with China (134.3 MT), India (98.5 MT), Russia (85.9 MT), United States (47.4 MT), and France (36.9 MT) being the main producers (FAOSTAT 218). This production accounted for more than 25 per cent of the total cereal crops consumed throughout the world.
10.4.2.5 Ssp. compactum (Host) MK (Club Wheat)
T. aestivum ssp. compactum (Host) Mac Key, known as club, dwarf, cluster or hedgehog wheat, [Syn.: T. compactum Host; T. vulgare compactum Alef.; T. sativum compactum Hackel.] is an annual, predominantly autogamous, plant. Culms are erect, vary in length from 70 to 140 cm long (excluding spikes), possess 5–6 internodes above ground, and are generally hollow, with thin walls, but in several varieties, are solid. In most varieties, the young shoots are erect, but in some, they are semi-erect or prostrate. Leaf blades are yellowish-green or blue-green, sparsely hairy, and 10 mm wide. The spikes are determinate, bilateral, squarehead in cross section, awned (bearded) or awnless (beardless), and usually appear from the side of the leaf sheath and not from the apex, as in most wheats. They are short, stiff and compact, 3.5–6.0 cm long (excluding awns), 10–15 mm wide, and generally with 17–25 closely packed spikelets that are arranged almost at right angles to the rachis. Typical spikes are with a uniform density, while in some forms they are more crowded towards the apex and more loosely arranged at the base. The rachis is tough, flattened, and fringed, with short hairs along the side and across the upper part of each notch immediately beneath the points of insertion of the spikelets. Spikelets pack broadside to the rachis, are crowded, oblong to ovate, 10–13 mm long, 13–15 mm wide, solitary at the nodes, and usually hairy. The top spikelet is fertile and at right angle to the plane of lateral spikelets. Each spikelet contains 6–7 florets, with fewer florets at the apex, 2–4 of which frequently produce grain. Those near the center of the spike bear 2–4 grains, whereas those near the base or the tip of the spike contain 1 or 2 grains only. The glumes are stiff, oblong, symmetrical in size, shorter than or almost equally long as the rest of the spikelet, white, yellow, red, brown, or blue-black, either glabrous or covered with soft hairs, 8–9-mm-long, and with 5 to 6 nerves. In beardless varieties, the apical tooth of the glume is blunted, 0.5–1.5 mm long, whereas in bearded varieties, it generally extends into a fine awn, usually not more than 0.5- 3.0-cm-long. In most forms, there is no single prominent keel, except for in the upper half of the glumes; some Asiatic forms, however, are keeled from the tip to the base. The lemmas are elliptic, thin and pale, inflated, 10 mm long, with 9 to11 nerves, and without a keel. In bearded varieties, the lemmas terminate in a stiff awn, 50–90-cm-long, which in some forms the awns diverge widely. The palea is of the ordinary bicarinate form, two-veined, and keeled. The caryopsis is ellipsoid, small, oval, narrow towards the apex and generally plump and hairy at the apex, 5–7 mm long, 3.0–3.7 mm wide, and 2.8–3.6 mm thick, free (free-threshing), white, yellow, or red, usually shallow and generally with a filled furrow. The endosperm in the majority of forms is opaque and starchy, but in some, it is flinty (Fig. 10.7c).
Ssp. compactum contains many varieties that were classified on the basis of awn presence (bearded or beardless), glume color and hairiness, and grain color. Most cultivars are spring types, although there are several winter-type forms.
Ssp. compactum is similar to bread wheat (ssp. aestivum) but can be straightforwardly distinguished by its more compact spike, due to its shorter rachis segments, and smaller grains than those of most bread-wheat cultivars. Therefore, in 1807, Host first gave this taxon a specific rank, but Mac Key (1954b) later classified it as a subspecies of T. aestivum. Percival (1921) considered ssp. compactum as closely related to ssp. aestivum. In contrast, Mac Key (2005) stated that there are no genetic reasons to consider ssp. compactum more closely related to ssp. aestivum than to the other subspecies of T. aestivum. He was of the opinion that ssp. compactum is even more phylogenetically closely related to ssp. spelta than is ssp. aestivum. Mac Key based this opinion on the cytological evidence presented by Thompson and Robertson (1930), who found somewhat better pairing in the F1 compactum × spelta hybrids than in compactum x aestivum or aestivum x spelta hybrids. The serological analysis of Zade (1914) provides additional supporting evidence.
Helbaek (1959) identified the archaeological samples of naked, small, somewhat spherical grains (< 5 mm) and short internodes found in Near Eastern sites from 8900 to 7000 BP, as club wheat, ssp. compactum. However, it is difficult to accept that these Near Eastern wheat remnants from such an early period are hexaploids, as explained by Kislev (1979/1980): (1) Modern forms of the hexaploid wheat T. aestivum are more adapted to the northern (Vavilov 1926) than to the Near East latitudes, where Helbaek found his remnants, the latter area being dominated by tetraploid wheats. (2) In the south-western flank of the Fertile Crescent, hexaploid wheat was only grown as a crop of little importance (Jakubziner 1932a). (3) If Helbaek’s remnants are indeed hexaploids, this implies that hexaploid naked wheat, found in the earliest periods in the Near East, preceded cultivation of tetraploid naked wheats. However, on an evolutionary basis, one would expect that the tetraploids developed first. (4) The earliest samples are probably from too early a period for hexaploid wheats to have come into existence; the spread of agriculture had not yet made geographic contact between the domesticated, free-threshing tetraploids and Ae. tauschii, the wild diploid progenitor of the D subgenomic of T. aestivum. Based on the morphological characteristics of this archaeological material and the difficulty in defining ancient Near Eastern naked wheat as hexaploid, Kislev (1979/1980), van Zeist and Bakker-Heeres (1973), Zohary (1973) concluded that these wheat remnants belong to an extinct free-threshing tetraploid form, T. turgidum ssp. parvicoccum Kislev. It is assumed that ssp. compactum originated later in the Near East and subsequently, was transported to Europe as an admixture with other wheats, and later established in several places as the dominant form (Feldman 2001).
According to Schiemann (1932, 1948), ssp. compactum is to be considered as an older wheat than ssp. aestivum. However, it is generally assumed that ssp. compactum derived from ssp. aestivum by a mutation of c to C, as was suggested by Nilsson-Ehle (1911), Mac Key (2005), Johnson et al. (2008). This gene is located on chromosome 2D (formerly XX) (Unrau 1950), and was either mutated on the hexaploid level or contributed by a line of Ae. tauschii containing the C allele. Since they grew in many places in mixture, hybridization and gene exchange between ssp. compactum and ssp. aestivum has repeatedly occurred.
Percival (1921) considered ssp. compactum one of the most ancient of free-threshing wheats widely grown by Neolithic man in many parts of Europe. According to him, ssp. compactum was found in many Neolithic and Bronze Ages deposits in Hungary, Germany, Switzerland, Italy, Spain, and Sweden. The grains of this wheat are small, and more or less hemi-spherical, with a blunt apex, and well-developed furrow. On average, they are 4.6 mm long, 3.4 mm broad, and 3–3.3 mm thick. Examples of ssp. compactum, with somewhat larger grains (5.5–7 mm long), similar to those of the common forms of the present day, have only been found in the Neolithic and Bronze Age deposits of Switzerland and northern Italy.
The small, naked wheat grains found in many sites of Neolithic Europe, were considered to belong to hexaploid wheat and were named by Heer (1866) Triticum compactum antiquorum. Because of the difficulty to distinguish between the fossil grains of ssp. compactum and those of many forms of ssp. aestivum, Schiemann (1932) and Bertsch and Bertsch (1949) referred the European remains of hexaploid wheat of this epoch as aestivo-compactum.
Yet, since it is difficult to distinguish between 4x and 6x seeds in archaeological finds (Nesbitt 2001), and since the spike morphology and grain size of T. compactum antiquorum resemble those of the extinct T. turgidum ssp. parvicoccum and the extant T. turgidum ssp. durum var. Hourani (Fig. 10.4e), Kislev (1979/1980) suggested that it may well be a tetraploid rather than a hexaploid taxon. That these primitive types may be of the same category as Kislev’s (1979/1980) tetraploid, small-seeded ssp. parvicoccum, was also suggested by Mac Key (2005), Zohary et al. (2012).
Rao (1972) assigned the dominant allele, C, of ssp. compactum to the left (beta) arm (currently long arm; Sears and Sears 1979) of chromosome 2D, i.e., 2DL, close to the centromere. Johnson et al. (2008), studying the location of C on chromosome 2D, localized C to an interval flanked by the markers Xwmc245 and Xbarc145, but could not unambiguously localize the C locus to a chromosome bin because markers that were completely linked to C or flanked this locus were localized to chromosome bins on either side of the centromere. Consequently, following Rao’s work (1972) localizing C near the centromere on chromosome arm 2DL, and based on the locations of flanking and linked markers, Johnson et al. (2008) placed it in deletion bin C-2DL3, which is located on both sides of 2D centromere. On the other hand, Tg1 was localized to a more distal position on the short arm of chromosome 2D (Nalam et al. 2007).
Johnson et al. (2008) also studied the relationship between C and another spike-compacting gene in wheat, namely, soft glume (Sog) in T. monococcum ssp. monococcum var. sinskajae (Lebedeva and Rigin 1994). This recessive factor on chromosome 2Am yields a compact spike, as well as soft glumes that are longer and broader than those of T. monococcum ssp. monococcum. They suggested that C and Sog are present in homoeologous regions on chromosomes 2D and 2Am, respectively. However, Sog is located on the short arm of 2Am (Taenzler et al. 2002; Sood et al. 2009) and C on the long arm. Thus, it is possible that these loci are orthologous, but their positions with respect to the centromere, are under debate. Alternatively, Sog and C might not be orthologous, despite their similar locations. The C allele of ssp. compactum seems to be homologous with the gene causing spike-compactness in ssp. macha (Swaminathan and Rao 1961). Similarly, C is not allelic to the gene controlling the compact spike of spp. sphaerococcum (Goncharov and Gaidalenok 2005).
There have been a number of QTL analyses dealing with spike compactness in bread wheat (Sourdille et al. 2000; Jantasuriyarat et al. 2004; Nalam et al. 2007; Ma et al. 2007). No QTLs affecting spike compaction have been found to coincide with the location of C. This suggests that there is no allelic variation at the c locus of ssp. aestivum and that variation in spike dimensions is due to other factors (Johnson et al. 2008). Ausemus et al. (1967) showed that genes affecting spike compaction are present in every chromosome except for chromosomes 2B, 4D, 5A and 5D, suggesting that spike compactness may be affected by many genes other than C. Thus, using the compact spike characteristic as a taxon-defining trait may not always be appropriate.
Club wheat, ssp. compactum, is grown today in a few restricted areas of Europe (south-east Russia, Germany, France, Italy, Switzerland, Spain, and Portugal), in Asia (Transcaucasia, Turkestan, Siberia, Mongolia, China and India), in the Near East (Turkey), North and South Africa, in the northwestern United States (California, Oregon, Washington, and Idaho), in South America (Chili), and in Australia. In many regions, ssp. compactum is currently predominantly distributed as a constituent in admixtures with ssp. aestivum or ssp. durum, with pure crops rarely seen. In North America, however, they are cultivated as a pure crop on a somewhat extensive scale. An extinct variety of ssp. compactum, California Club Wheat (Triticum compactum erinaceum), named for its appearance which resembles a hedgehog, had a compact (2–5-cm-long) and bearded spike, hairy rachis, red chaff, and small, soft, and red kernels. This variety, introduced to California by the Spaniards via Mexico in 1787, was farmed extensively during the beginning of California’s agricultural history. However, most of it disappeared during the first half of the nineteenth century, whereas a small amount was grown until the middle of the twentieth century.
Most ssp. compactum varieties tolerate frost, drought, and several fungal diseases, and grow well on poor soils. Club wheat better adapts to certain agro-climatic regions (Johnson et al. (2008), and it was suggested that this subspecies may be more competitive than ssp. aestivum in dryland areas, where stand establishment is difficult (Gul and Allan 1972; Zwer et al. 1995). They are mainly spring forms, many of them exceptionally early; only a few late-ripening winter forms exist. The straw of most varieties is not liable to lodge. While the spikes have a large number of grains, the yield in volume or weight per unit area is comparatively lower than that of ssp. aestivum, as the individual grains are smaller. The grains are firmly held by the glumes, a character which renders these wheats particularly suited for cultivation in districts where it is the practice to leave the crop on the field for considerable periods of time before harvesting can be completed. The grain is of soft or medium hardness, and of quality resembling that of several varieties of bread wheat.
Ssp. compactum are used for cake, crackers, cookies, pastries, and flours. Some varieties are also used for the production of starch, paste, malt, dextrose, gluten, alcohol, and other products.
10.4.2.6 Ssp. sphaerococcum (Percival) MK (Indian, Dwarf or Shot Wheat)
Triticum aestivum ssp. sphaerococcum (Perc.) Mac Key, known as Indian dwarf wheat, and shot wheat [Syn.: T. sphaerococcum Percival; T. compactum A. et G. Howard; T. aestivum gr. sphaerococcum (Percival) Bowden; T. aestivum convar. sphaerococcum (Percival) Morris and Sears], is an annual, predominantly autogamous, plant. Culms are erect, short, 50–100 cm long (excluding spikes), very stiff, hollow, with 4–5 internodes, and frequently bent below the spike in a winding manner. In some varieties, the culm has a reddish-pink color. The young shoots are erect, with leaves as in ssp. aestivum. The culm leaf-blade are somewhat rigid, comparatively short,10–16 cm long, 1.2–1.5 cm wide, taper towards the tip, and with scabrid upper surfaces, and a few coarse hairs on the ribs. The auricles are long, narrow, and fringed with a few hairs. The spikes are determinate, dense, short, 4–6 cm long (excluding awns), with 14–20 spikelets, and squarehead in cross-section. The rachis is tough, non-brittle, and fringed with very short white hairs along its margins, which also extend across the front of the rachis at the base of each spikelet. The spikelets are solitary at the nodes, about 10 mm long, 10 mm across, and 4 mm thick. The top spikelet is fertile and at right angle to the plane of lateral spikelets. Each spikelet contains 6 or 7 flowers, 4 or 5 of which may produce grain. The glumes have an inflated appearance, are shorter than the rest of the spikelet, 8–9 mm long, possess 6 or 7 nerves, glabrous or pubescent, white or red in color, are generally keeled in the upper part only, and terminate in a broad curved scabrid tooth. The lemmas are inflated, 8–9 mm long, and rounded on the back with 9 nerves. In the beardless varieties, the tip terminates in a short awn 3–4-mm-long, whereas the bearded forms possess very stiff short awns, 1.5–2 cm long, which are frequently bent near the base and which in ripe ears, spread outwards irregularly. The palea is 7–8 mm long and fringed with hairs along the two keels. The grains are of very characteristic form, distinctly shorter and rounder than those of other wheats. They are 4–5.5 mm long, 3–3.7 mm wide, and 3–3.7 mm thick, free and not adherent to lemma and palea (free-threshing), and often somewhat unsymmetrical due to pressure of the lemmas. The apex is truncate with a short “brush” at the apex, and the furrow is shallow. Grains color is white or red (Fig. 10.7d).
Ssp. sphaerococcum is a very early wheat; all varieties have a spring habit. There are several varieties that are classified on the basis of bearded or beardless spikes, white or red glume color, glabrous or pubescent glumes, and white or red grain color.
This subspecies was first described by Percival (1921). Based on its difference from other hexaploid wheats in its short stature (averaging 54–70 cm), small spikes, characteristically small, round grains and practically hemi-spherical, inflated glumes, Percival (1921) considered it as a separate species, but Mac Key (1954b) classified it as a subspecies.
Ssp. sphaerococcum is one of the more modern subspecies of T. aestivum, probably originating as a mutation in cultivated fields of bread wheat. Archaeological evidence dates the contribution of this wheat to ancient civilization in the Indus valley back to the 5th millennium BP (Feldman et al. 1995). According to Percival (1921), ssp. sphaerococcum only resembles ssp. compactum in their short dense spike, while it also has a tufted appearance and erect, stiff straw. The two glumes are different from each other in form and texture. The spikes are bearded or beardless, the former never having long awns, but irregularly spreading ones are 1.5–2.0 cm long at the apex of the spike and much shorter at the base. It has a red or white, glabrous or pubescent chaff, and the grain is very small and characteristically hemispherical in shape.
ssp. aestivum gave rise to sphaerococcum through a single mutation (Feldman et al. 1995; Feldman 2001). This mutation presumably occurred in an aestivum that had been carried eastward, since sphaerococcum has not been found in the prehistoric Near East and its culture nowadays is largely confined to India. This assumption is based on the fact that no line of Ae. tauschii has been found to carry the sphaerococcum allele s, indicating that these mutations appeared at the hexaploid level.
Miczynski (1930) crossed ssp. sphaerococcum with ssp. aestivum and concluded that the entire characters of ssp. sphaerococcum that distinguish it from ssp. aestivum is inherited as if it were determined by a single gene. He designated ssp. aestivum, bearing the dominant allele, as SS, and ssp. sphaerococcum as ss. While the s allele was recessive to the S allele, several intermediates were found, and the F2 population classified as aestivum varied somewhat in its characters. Miczynski (1930) concluded that the s allele also determines short awns, which were 2 cm long in fully bearded forms.
Ellerton (1939) crossed a bearded form of ssp. sphaerococcum with a beardless variety of ssp. aestivum. The F1 closely resembled aestivum, although dominance was not complete. The spikelets were rather shorter and more inflated than in the aestivum parent, tough the grains closely resembled those of aestivum in shape. F2 segregated in a ratio of 1:2:1 indicating a difference of a single gene. The absence of crossover types in the above cross showed that the entire complex of characters differentiating between sphaerococcum and aestivum behaves as if determined by a single gene and not by a group of closely but incompletely linked genes. Ellerton (1939) assumed that the magnitude and diversity of the effects of this single Mendelian factor are much greater than one would normally associate with a recessive mutation at a single locus, particularly in a hexaploid species. Consequently, he suggested that the s mutation involved a structural change in a short chromosomal section. Since the general characteristic of the mutation suggests that it is the effect of gene deficiency, one likely hypothesis is that the two subspecies differ by a single deletion covering several loci (Ellerton 1939). Such a deletion would be conserved and inherited as a single Mendelian factor.
In contrast, Swaminathan and Prabhakara Rao (1961), Swaminathan et al. (1963) claimed that ssp. sphaerococcum could not have arisen through a deletion in ssp. aestivum, since back-mutations to ssp. aestivum readily occur in sphaerococcum. In addition, induced mutations via gamma rays from sphaerococcum-type to aestivum-type were also obtained by Josekutty (2008). Moreover, the sphaerococcum locus, which tends to behave as one Mendelian unit in recombination, can be broken up by irradiation, resulting in phenotypes lacking the compact growth habit and rigidity of leaves, but possessing hemispherical glumes and spherical grains (Swaminathan and Prabhakara Rao 1961; Swaminathan et al. 1963).
Sears (1947), using monosomic analysis, showed that the sphaerococcum phenotype is due to a hemizygous-ineffective recessive gene, which in two doses produces the sphaerococcum phenotype but in a single dose, is relatively ineffective. Sears located the gene on chromosome 3D (formerly XVI). Using the telomeric method, Prabhakara Rao (1977) mapped the sphaerococcum gene s 5.7 crossover units away from the centromere on the beta (short) arm of chromosome 3D of wheat. In contrast, Koba and Tsunewaki (1978) located the s gene on the very proximal region of the long arm of 3D, approximately 5.0 cM from the centromere. Singh (1987) observed that the 1030 F2 plants of the cross between monosomic 3D of var. Pb. C 591 of ssp. aestivum and ssp. sphaerococcum, formed two distinct classes, parental-type (812 (78.8%) plants, morphologically sphaerococcum and aestivum types) and recombinant-type (218 (21.2%) plants having hybrid characters of sphaerococcum and aestivum). The occurrence of the recombinant subclasses showed that the sphaerococcum phenotype is not governed by a single gene, but by at least three closely linked genes that are located very close to the centromere on the long arm of chromosome 3D.
Cheng et al. (2020) studied the genetic basis of the semispherical grain trait in ssp. sphaerococcum, by generating an F2 segregating population from a cross of the wheat line HeSheng 2 of ssp. aestivum with Nongda 4332 (ND4332, derived from a cross between ssp. aestivum and ssp. sphaerococcum. The corresponding segregation ratio fit a Mendelian model of 3:1, indicating that the semispherical grain trait is controlled by a single nuclear gene, which is consistent with previous findings (Miczynski 1930; Sears 1947). In accordance with the official nomenclature rules of gene designation in wheat, Cheng et al. (2020) named the gene determining semispherical grain Tasg-D1. This gene was mapped between markers Xgwm341 and Xgdm72 on the short arm of chromosome 3D, near the centromeric region. Fine mapping of Tasg-D1 confirmed that the locus is located between markers 3DS-68 and 3DS-44. Cheng et al. (2020) narrowed the candidate region to a 1.01-Mb region between markers 3DS-68 and 3DS-94, a region containing 13 predicted high-confidence genes. Resequencing of these genes revealed only one single-nucleotide polymorphism (SNP) in the coding sequences. This SNP (A/G) is located in exon 9 of TraesCS3D01G137200, between ND4332 (Tasg-D1) and HS2 (TaSG-D1). This SNP in the coding region led to an amino acid substitution from lysine (286 K) to glutamic acid (286E). Studies of the expression profiles of TaSG-D1 in different tissues showed that it was highly expressed in shoot meristem, root, spike, grain, shoot axis and ovary tissue. TaSG1 has three homoeologs that share expression patterns, each located in a different subgenome.
Previous studies have revealed a discrepancy in the inheritance pattern of the sphaerococcum gene, which either has a hemizygous-ineffective recessive effect or an incompletely dominant effect (Sears 1947; Schmidt et al., 1963; Salina et al. 2000). Since it was determined that Tasg-D1 is a gain-of-function allele in wheat line ND4332, Cheng et al. (2020), evaluated its genetic effects on grain shape and other traits in a segregating population. The grain length showed a 1:2:1 segregation ratio in the examined populations, supporting the notion that Tasg-D1 shows incomplete dominance. Moreover, the phenotypes of heterozygous individuals were significantly different from those of homozygous ones, in traits such as grain length, plant height, spike length, spikelet density, and thousand-grain weight. This suggests that the effects of Tasg-D1 on plant architecture associated with the s locus are indeed pleiotropic (is it a transcription factor?).
According to Cheng et al. (2020), the mutant allele Tasg-D1 encodes a serine/threonine protein kinase glycogen synthase kinase 3 (STKc_GSK3) that negatively regulates brassinosteroid signaling. Expression of TaSG-D1 and the mutant form Tasg-D1 in Arabidopsis thaliana, suggested that a single amino acid substitution in the TREE domain of TaSG-D1 enhances protein stability in response to brassinosteroids, likely leading to formation of round grains in wheat. This gain-of-function mutation has pleiotropic effects on plant architecture and exhibits incomplete dominance. Cheng et al. (2020) proposed that the Tasg-D1 gene of ssp. sphaerococcum might have originated at the hexaploid level from ssp. aestivum by a spontaneous mutation in the TREE domain of TaSG-D1.
Mutations determining the sphaerococcum phenotype were described in hexaploid, tetraploid and diploid wheats. Schmidt et al. (1963) reported the appearance of a drastic mutation in bread wheat, ssp. aestivum, simulating ssp. sphaerococcum. This effect was controlled by an incompletely dominant gene not allelic to the sphaerococcum gene. The chromosome carrying the gene could not be identified in monosomic crosses because of sterility interactions in 10 of the 21 chromosomes. Therefore, the chromosomal location of this mutant could not be assigned to a specific subgenome of bread wheat.
Further evidence that the sphaerococcum phenotype is not restricted to the D subgenome of hexaploid wheat, came from the report by Schmidt and Johnson (1963, 1966) of the same character in a tetraploid wheat. Sphaerococcum-like plants were seen in a plot of a durum introduction from China. Cytological studies showed that the sphaerococcum-like plants had 14 bivalents at first meiotic metaphase and regular pairing in crosses with other durum lines. One possibility is that a translocation of the gene from the D subgenome to one of the tetraploid subgenomes had occurred. However, an alternative hypothesis is that this variant may represent a mutation of a normal allele to a sphaerococcum allele in either the A or the B subgenome. In this respect, it is interesting that Georgiev (1979) reported that EMS treatment produced mutants with phenotype similar to ssp. sphaerococcum in diploid wheat, T. monococcum.
Likewise, treatment of ssp. aestivum with chemical mutagens, produced three independent mutants with morphological features resembling those of ssp. sphaerococcum (Maystrenko et al. 1998). A monosomic analysis situated the three mutant genes, designated S1, S2, and S3, on chromosome 3D, 3B, and 3A, respectively (Maystrenko et al. 1998). Salina et al. (2000) reached similar results using microsatellite markers from a homoeologous group 3 of ssp. aestivum and mapped the S1, S2, and S3 genes of the induced sphaerococcoid mutation to chromosome 3D, 3B, and 3A, respectively. The S1 locus was found to be closely linked to the centromeric marker Xgwm456 of the long arm (2.9 cM) and mapped not far (8.0 cM) from the Xgdm72 marker of the short arm of chromosome 3D. The S2 gene was tightly linked to two centromeric markers (Xgwm566 and Xgwm845) of chromosome 3B and S3 was located between Xgwm2 (5.1 cM), the marker of the short arm, and Xgwm720 (6.6 cM), the marker of the long arm, of chromosome 3A. Thus, the sphaerococcum trait is not only restricted to the responsible gene in the D subgenome but can also be attributed to its homoeologs on the A and B subgenomes (Cheng et al. 2020).
Ssp. sphaerococcum is endemic to southern Pakistan and northwestern India (Elleton 1939; Josekutty 2008). It was one of the main crops grown by ancient Indian cultures. In modern times, it was grown as a major crop on a larger area in northwestern India and in southern Pakistan, but during the Green Revolution, in the 1960s, it was mostly replaced by high-yielding varieties of bread wheat (Mori et al. 2013). Currently, it is grown as a relic crop in northwestern India and southern Pakistan.
Indian dwarf wheat, ssp. sphaerococcum, presented the lowest nucleotide diversity among all T. aestivum subspecies (Zhou et al. 2020a). The extremely low diversity of Indian dwarf wheat is likely the result of its early migration to remote areas at the southwest of the Himalayas, which lacks wild relatives, and a consequential escape from alien introgressions.
Ssp. sphaerococcum resists drought well (Ellerton 1939) and is generally grown in areas of relatively little rain. Many varieties are resistant to yellow rust caused by Puccinia striiformis (Josekutty 2008). The grain has a high protein content compared to other hexaploid subspecies of T. aestivum, (Singh 1946; Josekutty 2008), but its yield is lower than that of ssp. aestivum. Its grains are usually ground into a flour and used as a cereal for making bread, biscuits, etc. The straw is used as a biomass for fuel, for thatching, or as a mulch in the garden. A fiber obtained from its stems is used the paper industry.
Kihara (1937) reported that Lilienfeld and Kihara in 1934 found a modal arrangement of 21 bivalents, most of which were ring bivalents, in both aestivum x sphaerococcum and the reciprocal cross. Occasional multivalents were also observed. The fertility of the F1 hybrid was good. Similarly, in crosses made by Ellerton (1939), 21 bivalents (mostly ring) were observed in most cells. Percival (1930) described an Ae. ovata (currently Ae. geniculata) x ssp. sphaerococcum cross in which he found a maximum of four bivalents, and similar pairing in hybrids between ovata and other hexaploid wheats. These results show that sphaerococcum is very closely related to aestivum.
Vakar (1932) studied chromosome pairing at first meiotic metaphase in F1 hybrids involving ssp. sphaerococcum and two forms of tetraploid wheat, i.e., two ssp. sphaerococcum x ssp. turgidum crosses and one sphaerococcum x var. pyramidale cross. All three hybrids exhibited fourteen bivalents and seven univalent. One of the sphaerococcum x turgidum hybrids showed a chromosome bridge and acentric fragment in several cells, indicating that the hybrid was heterozygous for a paracentric inversion. Baghyalakshmi et al. (2015) studied F1 hybrids between T. timopheevii ssp. timopheevii and ssp. sphaerococcum and observed 11.36 (5–12) univalents, 4.48 (4–11) bivalents, 4.49 (1–5) trivalents, and 0.60 (0–1) quadrivalents at meiosis.
10.4.2.7 Ssp. tibetanum J. Z. Shao (Semi-Wild, Feral Wheat)
No wild hexaploid progenitors of T. aestivum are known, but the two distinguishing characteristics of wild Triticum species, i.e., fragile rachises breaking into wedge-shaped units and closely appressed glumes, are found in plants in Tibet and named T. aestivum ssp. tibetanum J. Z. Shao. It is an autogamous plant, whose height ranges from 90 to 130 cm, leaves are light green, and culm and nodes are glabrous. Spikes are square, somewhat denser at the upper portion, 9–15 cm long, and awnless or awned, with short straight or curved white awns. The rachis is brittle, and at maturity, the spike disarticulates into individual spikelets, each falling with the rachis segment below it (wedge-type disarticulation). Spikes contain 15–27 spikelets, with each spikelet containing 5–6 florets, rachilla is hairy. Glumes are ovate, stiff and rigid, glabrous or pubescent and red or white in color. Lemmas are ovate, glabrous and awned. The grains are adherent to the palea and lemma and threshing results in spikelets rather than naked grains, their number per spikelet in the middle portion of spike is 3–5. All forms have spring habit (Fig. 10.7e).
Morphological, physiological and genetic studies have shown that ssp. tibetanum is closely related to bread wheat landraces of the white wheat complex native to the Sichuan province of south-west China (Yen et al. 1988). It has a brittle rachis, different from that of ssp. spelta of west Asia. It closely resembles the Chinese white wheat complex by its thin leaves, light green color, square spike, with multi-floret spikelets, rounded glume, with hooded lemma and tipped or curly awn. The crossability genes and non-interchanged chromosomes phylogenetically connect ssp. tibetanum with the white wheat complex (Yen et al. 1988). Its chloroplast genome is similar to that of bread wheat, its mitochondrial genome is only slightly different from that of the latter, and its cytoplasm does not induce male sterility in all studied bread wheat genotypes (Tsunewaki et al. 1990). These facts suggest that it is an off-type of Tibetan bread wheat.
Ssp. tibetanum has a very primitive compliment of the D subgenome chromosomes since their D-subgenome chromosomes are structurally similar to the chromosomes of Ae. tauschii; at meiosis of F1 hybrids between ssp. tibetanum and Ae. tauschii, no multivalents form and 7 ring bivalents and 14 univalents are always observed (Yen et al. 1988).
In 1974, this subspecies was collected in five counties in the Tibet plateau, by a Chinese scientific expedition (Shao et al. 1980, 1983). Based on its morphology and chromosome number, Shao et al. (1980, 1983) suggested to regard this semi-wild wheat as a new T. aestivum subspecies, namely, ssp. tibetanum. The new subspecies, considered to be an off-type of Tibetan bread wheat (Tsunewaki et al. 1990), usually grows as weed within or on edges of barley and wheat fields (Shao et al. 1983). It is a polymorphic taxon, exhibiting variation in almost all morphological characters, and based on this variation, Shao et al. (1983) classified the collected samples into three varieties.
Ssp. tibetanum has a brittle rachis, different from that of ssp. spelta of west Asia. Although it is a hulled form having brittle rachis and stiff glumes, significant differences exist between it and ssp. spelta and ssp. macha, the two other hulled subspecies of T. aestivum, (Shao et al. 1983; Tsunewaki et al. 1990). Seedlings of all three ssp. tibetanum lines studied have broad, light green leaves. In contrast, the two spelt-type wheats ssp. spelta and ssp. macha, have rather narrow leaves of dark green color (Tsunewaki et al. 1990). The spikes of the three ssp. tibetanum lines are like those of the two other hulled subspecies of T. aestivum, however, the spikes of ssp. tibetanum disarticulate spontaneously from the tip, as the spikelets mature, and the spikelets drop off the culm at the time of ear ripening. Such strong disarticulation is not observed in any other forms of T. aestivum, including spelta and macha. The mode of disarticulation of ssp. tibetanum is of the wedge-type, i.e., with the rachis segment below each spikelet, and is clearly different from the barrel-type, in which each spikelet contains the rachis segment beside it, a type exhibited by ssp. spelta (Shao et al. 1983; Tsunewaki et al. 1990).
Analysis of root tip cells revealed that ssp. tibetanum is a hexaploid with 2n = 42 chromosomes (Shao et al. 1983; Tsunewaki et al. 1990). It can easily be crossed with bread wheat, yielding fully fertile F1 hybrids, with complete chromosomal pairing at meiosis, although three interchanges exist between the studied lines of ssp. tibetanum and cultivar Chines Spring of ssp. aestivum (Tsunewaki et al. 1990).
Shao et al. (1983) found that F1 hybrids of a bread wheat cultivar (white glume, white grain, glabrous glumes, non-brittle rachis) with a line of ssp. tibetanum (red glume, red grains, pubescent glumes, fragile rachis) exhibited dominance of the four studied traits, i.e., the F1 hybrids had a fragile rachis, red glumes and red grains. Data obtained by Tsunewaki et al. (1990) support the conclusion of Shao et al. (1980, 1983), i.e., that ssp. tibetanum is genetically very closely related to bread wheat. The observed mode of spike disarticulation, chromosomal instability and the genotype of hybrid chlorosis clearly favor the hypothesis that ssp. tibetanum originated rather recently as an off-type of domesticated forms of Tibetan bread wheat (Tsunewaki et al. 1990).
Sun et al. (1998) used RAPD analysis of seven accessions of ssp. tibetanum, 22 cultivars of ssp. aestivum from China, and 17 lines of European ssp. spelta, to study the genetic relationships between these three subspecies of T. aestivum, and to assess genetic diversity among and within these taxa. RAPD polymorphism was found to be much higher within ssp. spelta and ssp. tibetanum than within ssp. aestivum. The genetic distance between ssp. tibetanum and ssp. aestivum was smaller than that between ssp. tibetanum and ssp. spelta. Cluster analysis clearly classified all the studied genotypes into two groups: one included all the European spelta lines, and the second included all cultivars of ssp. aestivum and the lines of ssp. tibetanum, thus supporting classification of the Tibetan wheat as a subspecies in T. aestivum. Similar results were obtained by Cao et al. (2000b), who used RAPD to assess the phylogenetic relationships among the subspecies of T. aestivum. Their RAPD data, are in-agreement with those based on morphological classification, suggesting that, of the subspecies of T. aestivum, ssp. tibetanum is most closely related to bread wheat.
Study of the genetic control of rachis fragility and glume tenacity in ssp. tibetanum was carried out by Cao et al. (1997), in an attempt to help establish the taxonomic status and genetic origin of semi-wild wheat. Progenies of crosses and backcrosses of semi-wild wheat with cultivar Columbus of bread wheat indicated that the fragile rachis and non-free-threshing character of ssp. tibetanum were dominant over the tough rachis and free-threshing character of bread wheat. F2 and backcross data indicated that the rachis fragility and glume tenacity of the semi-wild wheat were each controlled by a single gene. On the other hand, in the cross between ssp. tibetanum and spp. spelta, the F2 and F3 populations did not segregate by glume tenacity, but did segregate by rachis fragility. These data suggest that three genes interact to control three types of rachis fragility in hexaploid wheat: in semi-wild wheat-type, in spelta-type and in the tough rachis of common wheat. Semi-wild wheat differs from bread wheat in rachis fragility and glume tenacity and from the hulled subspecies of T. aestivum (ssp. spelta, and ssp. macha) in the pattern and degree of rachis disarticulation. Cao et al. (1997) concluded that semi-wild wheat is likely a subspecies within T. aestivum, at the same taxonomic level as spp. spelta and macha.
Chen et al. (1998), using monosomic and ditelosomic lines of bread wheat, found that the gene controlling the brittle rachis of ssp. tibetanum, designated Br1, is dominant and located on the short arm of chromosome 3D i.e., on 3DS. Consequently, it was designated Br-D1. So, it seems that this gene in ssp. tibetanum derived from Ae. tauschii. It is interesting to note that the brittle rachis gene in ssp. tibetanum, like those in some related genera such as Aegilops, is also located on homoeologous group 3 chromosomes. Interestingly, the Br gene in Ae. tauschii determines barrel-type disarticulation in the diploid species and not wedge-type disarticulation but exhibits the wedge-type of disarticulation in hexaploid background. As was found earlier (Shao et al. 1983; Tsunewaki et al. 1990), Br-D1 is different from the gene determining brittle rachis in ssp. spelta. In the progenies of the cross spelta x tibetanum, F1 plants exhibited the wedge and barrel types of disarticulation indicating that wedge-type disarticulation in ssp. tibetanum is codominant with the barrel type in spelt wheat.
The genes for brittle rachis were mapped using aneuploid stocks in hexaploid and tetraploid wheat (Watanabe et al. 2002). Similar to Chen et al. (1998), also Watanabe et al. (2002) located the Br-D1 in the Tibetan weed races on the short arm of chromosome 3D. The average distance from centromere was 20.6 cM. In accordance with the rule for the symbolization of genes in homoeologous sets, they propose to designate the group 3 brittle rachis genes, Br‐A1, Br‐B1 and Br‐D1.
Guo et al. (2020) present a draft genome sequence of a Tibetan semi-wild wheat accession Zang1817 and re-sequence 245 wheat accessions, including world-wide wheat landraces, cultivars as well as Tibetan landraces. They demonstrate that high-altitude environments can trigger extensive reshaping of wheat genomes, and also uncover that Tibetan wheat accessions accumulate high-altitude adapted haplotypes of related genes in response to harsh environmental constraints. Moreover, Guo et al. (2020) find that Tibetan semi-wild wheat is a feral form of Tibetan landrace, and identify two associated loci, including a 0.8-Mb deletion region containing Brt1/2 homologs and a genomic region with TaQ-5A gene, responsible for rachis brittleness during the de-domestication episode. Gheir study provides confident evidence to support the hypothesis that Tibetan semi-wild wheat is de-domesticated from local landraces, in response to high-altitude extremes.
This feral wheat has an established growth habitat and a distinct morphology and should therefore be considered a sub-species. It grows as weed within and on edges of wheat and barley fields. A feral form of ssp. macha, that grows as weed in edges of wheat fields in Georgia, was also described (Dekaprelevich 1961). This form is also considered a feral derivative of domesticated wheats rather than a truly wild species.
Kuckuck (1964) suggested that the hexaploid wheat with a fragile rachis found by Dekaprelevich, may have originated as an amphiploid between wild emmer, ssp. dicoccoides, and Ae. tauschii, independently of the origin of domesticated hexaploids, which are believed to have involved free-threshing tetraploid wheat as their tetraploid parent. Sears (1976a) crossed wild emmer, ssp. dicoccoides, with Ae. tauschii and obtained a F1 hybrid with a brittle rachis. Thus, it remains uncertain whether Dekaprelevich’s brittled-rachis hexaploid wheat actually originated in this way or as a segregate from a cross of ssp. macha with wild tetraploid wheat, or as result of back-mutation of Q to q in the domesticated hulled-wheat ssp. macha.
Kuckuck (1970) suggested that a brittle-rachis form of ssp. macha, var. megrelicum Dek. et Men., could be a genuinely wild hexaploid wheat, and therefore a candidate ancestor species. However, its fully brittle-eared form, var. megrelicum, is not described as growing outside cultivated fields, and is therefore not a truly wild wheat.
10.4.2.8 Cytology, Cytogenetics, Genomics, and Evolution
10.4.2.8.1 Origin of T. aestivum
Hexaploid wheat, T. aestivum (2n = 6x = 42; genome BBAADD), evolved through two allopolyploidization events. The first event, involving two diploid species, T. urartu, the male donor of the A subgenome, and a species related to Ae. speltoides, the B-genome donor, the female parent, led to the formation of wild emmer, T. turgidum ssp. dicoccoides, about 700,000–900,000 years ago (Marcussen et al. 2014; Gornicki et al. 2014; Middleton et al. 2014). Subsequently, following mutations, several domesticated subspecies of T. turgidum evolved. The second allopolyploidization event that produced hexaploid wheat, occurring during the 9th millennium BP (Feldman 2001), presumably involved the free-threshing tetraploid wheat, ssp. parvicoccum as the female donor of the B and A subgenomes, and a diploid species, Ae. tauschii, the male donor of the D subgenome. This event first formed the hulled allohexaploid wheat, ssp. spelta, from which the more advanced free-threshing forms developed (Feldman et al., 1995; Feldman 2001). Almost all F1 hybrids between the different subspecies of T. aestivum show complete chromosome pairing at meiosis and high fertility, justifying their categorization at the sub-specific rank (Mac Key 1954b).
Earlier chromosome counts of the various wheat species were wrong. Several cytologists reported the presence of 16 chromosomes in the diploid wheat, T. monococcum, while others reported 40 in the hexaploid, T. vulgare (= ssp. aestivum) (reviewed in Sax 1922). Conversely, Sakamura (1918), analyzing root tip cells of different wheats, obtained the following results: T. monococcum had 14 chromosomes, the subspecies of T. turgidum, namely, dicoccon, durum, turgidum and polonicum had 28, and the subspecies of T. aestivum, compactum and spelta, had 42. At the same time, Sax (1918) found 28 chromosomes in the first division of the fertilized egg of ssp. durum. These chromosome counts reinforced Schultz’s (1913b) classification showing that his three wheat groups comprise a polyploid series; einkorn is a diploid (2n = 14), emmer is a tetraploid (2n = 28), and dinkel is a hexaploid (2n = 42).
Soon after the discovery of the correct chromosome count in wheats, Kihara (1919, 1924), Sax (1918, 1921, 1922, 1923, 1927), Sax and Sax (1924) started to cross representatives of the different ploidy levels to study the cytogenetic relationship between these groups. In F1 hybrids involving representatives of the hexaploid species T. aestivum, and those of the tetraploid species T. turgidum (called pentaploid hybrids; 2n = 5x = 35), Kihara (1919) observed at first meiotic metaphase 14 bivalents (mostly ring) and 7 univalents, indicating that the hexaploid parent shares 14 chromosome pairs with tetraploids wheats and differs by an extra 7 pairs. Consequently, Kihara concluded that hexaploid wheat originated from a cross between a form(s) of T. turgidum that contributed 14 chromosomes, while an alien diploid species contributed the additional seven chromosomes. Such a cross yielded F1 triploid hybrid (2n = 3x = 21) that underwent spontaneous chromosome doubling.
Since the indication that the third chromosome set (subgenome) of T. aestivum was donated by an alien diploid species, extensive attempts have been made to identify the diploid donor of this subgenome. In these endeavors, studies extended to the wild relatives of wheat, particularly to species of the closely related genera Aegilops that also comprises a polyploid series with diploid, tetraploid and hexaploid species (Percival 1923; Schiemann 1929; Sorokina 1937; Lilienfeld 1951, and reference therein). These works resulted in much speculation as to which species of Aegilops may have contributed the third subgenome of hexaploid wheat. In this regard, Percival (1921, 1923) expressed the belief that the free-threshing hexaploid wheats were segregants from crosses between wild emmer and Ae. geniculata (formerly Ae. ovata). However, cytological studies by Sax and Sax (1924) and others, including Percival (1930), have proven quite conclusively that Ae. geniculata could not have played a major role in the origin of the hexaploid wheats.
Morphological indication as to the donor of the third subgenome of T. aestivum was obtained from the comparison of the spikelet structure in the hulled hexaploid wheat ssp. spelta, with that of wild Triticum and Aegilops species. ssp. spelta spikelets show two types of rachis breaks upon maturity, one like that of wild emmer, ssp. dicoccoides, namely, rachis breaks yield spikelets having arrow-head shape, each with the rachis segment below it (wedge-type), and the second like that of several species of Aegilops from sections Vertebrata (including the diploid Ae. tauschii and the allotetraploids Ae. crassa and Ae, ventricosa) and from section Cylindropyrum (including the allotetraploid Ae. cylindrica). In these Aegilops species the brittle rachis disarticulates into spikelet containing the rachis segment beside them (barrel type). Hence, this type of rachis disarticulation implies that the donor of the third subgenome to hexaploid wheat is from one of these Aegilops species.
In fact, several years earlier, Stapf (1909) suggested, based on morphological characteristics, that ssp. spelta derived from Ae. cylindrica. Percival (1921, 1923) assumed that this species had contributed certain characters to ssp. spelta, but was not involved in its origin. Conversely, Sax and Sax (1924) reported that the third chromosome set in T. aestivum is found in Ae. cylindrica (2n = 4x = 28), since F1 hybrids between this species and T. aestivum, a pentaploid hybrid with 2n = 5x = 35, had 7 bivalents and 21 univalents, indicating that they share one subgenome. Also, chromosomal pairing at meiosis of the F1 hybrid between the amphiploid cylindrica–durum (2n = 8x = 56) and T. aestivum (2n = 6x = 42), a heptaploid hybrid with 2n = 7x = 49, which showed 21 bivalents (14 bivalents between the A and B subgenomes of aestivum with those of durum and 7 bivalents between one of the subgenomes of Ae. cylindrica and that of T. aestivum) and seven univalents, indicated again that Ae. cylindrica and T. aestivum share one subgenome (Sears 1944b). The intensity of pairing and the absence of heteromorphic bivalents indicated fairly complete homology between one of the aestivum subgenomes and one of the Ae. cylindrica sets. Since average chromosome pairing in the F1 hybrid cylindrica x durum (2n = 4x = 28) was only 0.50 bivalents per cell, the shared subgenome of Ae. cylindrica and T. aestivum should involve the third subgenome of T. aestivum. Taken together, Ae. cylindrica contains one subgenome which is homologous to one subgenome of ssp. spelta and ssp. aestivum.
An allopolyploid resulting from a cross between Ae. cylindrica and a tetraploid wheat, would have 56 chromosomes instead of the required 42. This, therefore, appears to eliminate Ae. cylindrica, and other allotetraploid species of Aegilops with barrel-type disarticulation, as possible parents of the hexaploid wheats. Ae. cylindrica has been shown by Sax and Sax (1924), Bleier (1928), Kihara (1937) to be an allopolyploid carrying the C subgenome from Ae. caudata, and the D subgenome from Ae. tauschii, and Sears (1941a) produced an amphiploid from the cross of Ae. caudata x Ae. tauschii that morphologically resembles Ae. cylindrica. In addition, Sears (1941a) produced a hexaploid from the cross ssp. dicoccoides x Ae. caudata, but the resulting amphiploid did not morphologically resemble ssp. aestivum or ssp. spelta, thus eliminating Ae. caudata (genome C) as the third subgenome donor and leaving Ae. tauschii (genome D) as the probable one.
In accord with the above, Pathak (1940), following an analysis of figures of Aegilops chromosomes prepared by Senjaninova-Korczagina (1932), suggested that, Ae. tauschii may have been the donor of the third subgenome of T. aestivum. This aligns with the morphological evidence of rachis disarticulation, suggesting that the third subgenome of ssp. spelta most likely derived from hybridization between tetraploid wheat and Ae. tauschii (Kihara 1944; McFadden and Sears 1944b, 1946). Ae. tauschii has both the barrel-type dispersal unit, and the square-shouldered glumes which characterize T. aestivum (Nesbitt and Samuel 1996).
Indeed, the F1 of ssp. dicoccon x Ae. tauschii resembled the taxonomic characters of ssp. spelta but was completely sterile (McFadden and Sears 1946). In contrast, the amphiploid dicoccon–tauschii, derived from colchicine treatment of the F1 hybrid, had the hexaploid number of chromosomes (2n = 6x = 42; genome BBAADD), exhibited regular pairing at meiosis and high fertility, and closely resembled ssp. spelta in most traits (McFadden and Sears 1946). Moreover, crosses involving the synthetic amphiploid and ssp. spelta or ssp. aestivum produced fertile F1 hybrids with 21 bivalents at meiosis, and no multivalents (McFadden and Sears 1946), thus, demonstrating unequivocally that Ae. tauschii is the donor of the third subgenome of T. aestivum. For the origin of the A and B subgenomes of T. aestivum, see Sect. 10.3.2.12.
The cytoplasm of T. aestivum, designated B, is identical to that of its maternal parent, T. turgidum, and closely related to the S cytoplasm of Ae. speltoides (Terachi and Tsunewaki 1992; Wang et al. 1997; Tsunewaki 2009, and reference therein). Similarly, Provan et al. (2004), utilizing polymorphic chloroplast microsatellites to analyze cytoplasmic relationships in the genera Triticum and Aegilops, reported that the allopolyploid Triticum species have cytoplasm similar to that of Ae. speltoides. Similar results were obtained by Gornicki et al. (2014), who found that Ae. speltoides is the closest relative to the diploid donor of the chloroplast of the emmer lineage, that is, the allopolyploids containing the B subgenome. This further demonstrates that Ae. speltoides or a closely related specie was the B-subgenome donor of allopolyploid wheats.
Following identification of the donors of the subgenomes of T. aestivum and consequently, the three diploid species involved in the ancestry of this hexaploid species, i.e., T. urartu, an extinct or yet not discovered B-subgenome donor, and Ae. tauschii, it became possible to investigate the cytogenetic relationships and to estimate the cytological similarities between these three subgenomes of the hexaploid. Mochizuki and Okamoto (1961) studied chromosomal pairing at first meiotic metaphase of the 21-chromosome hybrid, T. monococcum ssp. aegilopoides (very close to the donor of the A subgenome), Ae. speltoides (close to the donor of the B subgenome), and Ae. tauschii (the donor of the D subgenome) and found more than 5 bivalents and several multivalents (an average of 12 chromosomes out of the 21 were involved in pairing). These results were directly comparable to those of Kimber and Riley (1963), who observed a similar level of pairing in haploids of bread wheat lacking chromosome 5B that carries the homoeologous-pairing suppressor gene, Ph1. Likewise, euhaploids of bread wheat (2n = 3x = 21; genome BAD), with deletion of Ph1, as in the mutant ph1b, exhibited extensive homoeologous pairing, with 1.53–1.74 ring bivalents, 2.90–3.57 rod bivalents, and 0.53–1.16 trivalents (Jauhar et al. 1991). The most reasonable conclusions to draw from these data is that the genomes of the three diploid species still have not diverged considerably from each other, that chromosomes of the three subgenomes of T. aestivum have undergone little change during the evolution of the allopolyploid, and that the regular behavior in the allopolyploid is due to the presence of two doses of homologous chromosomes and to the action of the Ph1 gene. Accordingly, despite it being a segmental allopolyploid (i.e., an allopolyploid that exhibits partial homology between chromosomes of its subgenomes that that derived from relatively closely related species), T. aestivum, underwent complete cytological diploidization), and behaves as a genomic allopolyploid (i.e., an allopolyploid having little homology between chromosomes of its subgenomes that derived from relatively distant species), with exclusive pairing of homologous chromosomes, i.e., 21 bivalents always form at first meiotic metaphase of this species.
Hexaploid wheat originated from spontaneous chromosome doubling of the triploid F1 hybrid between the domesticated form of T. turgidum and Ae. tauschii. Indeed, Fukuda and Sakamoto (1992), Matsuoka and Nasuda (2004), Zhang et al. (2010) reported occasional production of unreduced gametes and consequently, fertility, in such hybrids. At first meiotic division of such F1 hybrids, Fukuda and Sakamoto (1992) observed that unreduced gametes were formed as a result of restitution of the first meiotic division, and normal second division, followed by formation of dyads which developed into two fertile 2n pollen grains. Further studies (Matsuohka and Nasuda 2004) involved crossing of a durum wheat cultivar that carried a gene for meiotic restitution with a line of Ae. tauschii. Some of the F1 hybrids were highly fertile and spontaneously set hexaploid F2 seeds. Cytological analyses of F1 male gametogenesis showed that meiotic restitution was responsible for the high fertility of the triploid F1 hybrids.
Matsuoka et al. (2013) examined the genetic basis of the spontaneous genome doubling of triploid F1 hybrids between T. turgidum ssp. durum and Ae. tauschii. They found six QTLs in Ae. tauschii that are involved in hybrid genome doubling, presumably through the production of unreduced gametes. In addition, Hao et al. (2014) detected a major QTL controlling the production of unreduced gametes in two F2 populations that derived from F1 T. turgidum x Ae. tauschii hybrids. The QTL, named QTug.sau-3B, is located in chromosome 3B of the T. turgidum parent and situated between the markers Xgwm285 and Xcfp1012. QTug.sau-3B is a haploid-dependent QTL, as it was not detected in doubled haploid populations.
Farming of this durum wheat is limited today to several mountainous regions in northern Iran (Matsuoka et al. 2008), but the situation may have been different in the past. If tetraploid wheat farming was predominantly adopted in low elevations of Caspian Iran, and if the distribution of Ae. tauschii was similar to its present-day distribution, most likely sources of the D genome are genotypes of Ae. tauschii ssp. strangulata that grow in the area. Indeed, biochemical and molecular studies indicated that the birthplace of hexaploid wheat was in Transcaucasia and in Iran, southwest to the Caspian Sea (Tsunewaki 1966; Nakai 1979; Jaaska 1980; Dvorak et al. 1998a, b) or southeastern Caspian Iran (Nishikawa et al. 1980).
The accumulated data indicate that plants of Ae. tauschii native to the south-west part of the Caspian Sea (mainly forms taxonomically placed in ssp. strangulata) had genome similar to that of subgenome D found in the hexaploid wheats. This led to the consensus concept that Ae. tauschii ssp. strangulata was the wheat progenitor (Nishikawa 1973; Nakai 1979; Jaaska 1980; Hammer 1980; Nishikawa et al. 1980; Lagudah et al. 1991; Lubbers et al. 1991; Dvorak et al. 1998a, b, 2012; Wang et al. 2013). ssp. strangulata is distributed from Transcaucasia to eastern Caspian Iran (Kihara et al. 1965; Jaaska 1980). In the southwestern and southern Caspian Iran, subsp. strangulata overlaps with subsp. tauschii var. meyeri and var. typica.
Wang et al. (2013), using the 10 K Infinium single-nucleotide polymorphism (SNP) array, studied genetic relationships between 477 Ae. tauschii lines and the D subgenome of bread wheat. They found that Ae. tauschii consists of two lineages (designated 1 and 2), each consisting of two closely related sub-lineages. The distinct separation of lineages 1 and 2 from each other, the scarcity of intermediate genotypes between the two lineages, and the relative lengths of branches in the phylogenetic tree obtained, agreed with trees constructed with AFLP markers (Mizuno et al. 2010), RFLP markers (Dvorak et al. 2012), diversity arrays technology (DarT) markers (Sohail et al. 2012), and haplotype sequencing (Dvorak et al. 2012). A population within lineage 2 in the southwestern and southern Caspian appears to be the main source of the wheat D subgenome.
Ecogeographic and genetic evidence strongly favors the origin of hexaploid wheat from domesticated tetraploid wheat rather than from the wild emmer (Triticum timopheevii, either domesticated or wild, cannot be considered a putative parent because of its different genomic constitution). In the middle of the 9th millennium BP, when hexaploid types first appeared, there was no geographical contact between wild emmer and Ae. tauschii. Moreover, any dicoccoides-tauschii amphiploid would have had a brittle rachis (Sears 1976a) and, hence, little chance to be selected by ancient farmers. By the time hexaploid wheat evolved, domesticated tetraploid wheat was already grown in eastern Turkey and western and north-western Iran, and came into contact with Ae. tauschii, which presumably was growing as a weed within and at the edges of wheat fields. Therefore, the most likely area of origin of the hexaploid bread wheat is the south-western corner of the Caspian belt. Such association between domesticated T. turgidum and weedy Ae. tauschii in cultivation can still be found in this area (Matsuoka et al. 2008). A recent analysis of 242 Ae. tauschii accessions showed that a rare and distinct lineage (different from strangulata) from Transcaucasia also contributed ~ 1% on average of the current wheat D sub-genome (Gaurav et al. 2021), in accordance with earlier studies that analyzed allelic variation of high molecular weight (HMW) glutenins (Giles and Brown 2006).
Although several sources of evidence point to domesticated emmer, ssp. dicoccon, rather than ssp. dicoccoides, as the tetraploid parent (Tsunewaki 1966; Porceddu and Lafiandra 1986; Kimber and sears 1987), it is more likely that the donor of the BA subgenomes to hexaploid wheat was a free-threshing tetraploid wheat (Dvorak et al. 2012), or more specifically, ssp. durum (Matsuoka and Nasuda 2004; Pont et al. 2019). Indeed, based on the ability to induce the production of unreduced gametes in the F1 hybrid, Matsuoka and Nasuda (2004) suggested that T. turgidum ssp. durum was the tetraploid parent of hexaploid wheat. While surveying current cultivation areas of ssp. durum in northern Iran, they observed that, Ae. tauschii occurred widely as a weed in the durum fields. This finding showed that the T. turgidum–Ae. tauschii association hypothesized in the theory regarding T. aestivum evolution, still exists in the area where bread wheat likely evolved.
Extraction of the BA subgenomes from hexaploid wheat has given an indication of the type of tetraploid that was involved in the synthesis of the hexaploid. This was done by Kerber (1964), who crossed aestivum cultivars with a tetraploid, and backcrossed the pentaploid hybrids to the hexaploid parents for several generations, each time using only those plants that were themselves pentaploids. Finally, he selfed the pentaploids and selected tetraploid progeny that contained the BBAA subgenomes of hexaploid wheat. These extracted tetraploids were similar in spike morphology to the primitive free-threshing tetraploid, ssp. parvicoccum (Kislev 1979/1980). In accord with this, at the time when T. aestivum was formed, during the ninth millennium BP, ssp. durum was scarce or possibly nonexistent, whereas ssp. parvicoccum was widely cultivated and presumably was in massive contact with Ae. tauschii. Later on, when ssp. durum replaced ssp. parvicoccum, additional hybridizations between ssp. durum and Ae. tauschii presumably occurred.
Since no wild prototype of the hexaploid group is known to exist, many theories have been proposed as to the time, place, and way of origin of the various subspecies of T. aestivum. The fact that ssp. spelta has a brittle rachis and hulled seeds, led de Candolle (1886), Hackel (1890), Schulz (1913b), Carleton (1916) to consider it more primitive than the free-threshing hexaploid forms, and thus, as the oldest form of T. aestivum. This conclusion is further supported by the fact that all crosses of either hulled or free-threshing tetraploid wheats with all used lines of Ae. tauschii yielded only hulled forms resembling ssp. spelta, indicating that this subspecies is the prototype of hexaploid wheat (McFadden and Sears 1946; Kerber and Rowland 1974), and therefore, the predecessor of the more advanced, free-threshing forms.
Already Schroder (1931), based on anatomical evidence, proposed that ssp. aestivum arose from ssp. spelta. With the understanding that ssp. spelta is the most primitive subspecies of T. aestivum, it was assumed that the free-threshing forms of T. aestivum derived from it as a result of mutations (McFadden and Sears 1946). Indeed, the principal differences between the major hexaploid taxa are due to one or two genes that affect gross morphology (Mac Key 1954b) (Table 10.11).
Yet, the genetic data suggesting that the first hexaploid wheats were hulled, spelt-type, and more primitive than the free-threshing forms, do not agree with the archaeological chronology. While free-threshing forms of T. aestivum, i.e., ssp. aestivum, were found at the middle of the 9th millennium BP and were abundant in the pre-historic Near East from the 8th millennium onwards, thus far there is archaeological evidence for ssp. spelta only a thousand years later (Kislev 1984). Neolithic, Near Eastern ssp. spelta is very rare and earlier evidence for the existence of ssp. spelta is still missing. There is evidence of spelta grains from Yarim Tepe II, northern Iraq, dating back to the 7th millennium BP and probably also from Yarim Tepe I, about one thousand years earlier (Kislev 1984). These discrepancies between the genetic and archaeological data pose some difficulties in tracing the early history of the hexaploids. Indeed, several researchers (see Tsunewaki 1968) postulated that spelt wheat could not be the progenitor of bread wheat, but rather, its derivative. On the other hand, assuming that the first hexaploids were hulled, their absence from the prehistoric remains of the Near East may indicate their lack of advantage over domesticated emmer and free-threshing forms of T. turgidum in that area. ssp. spelta is grown today in extreme environments of the Near East, such as the high plateau of west-central Iran, eastern Turkey, and Transcaucasia. This cultivation is possibly of an ancient origin.
The earliest hexaploid wheats, seemingly originating south-west of the Caspian Sea, were hulled, spelta-type, presumably carrying the Q factor contributed by the free-threshing tetraploid wheat parent, and Tg (tenacious glume) from Ae. tauschii (Kerber and Rowland 1974). So, only a single mutation from Tg to tg was necessary to produce a free-threshing form (Kerber and Rowland 1974). If free-threshing hexaploid wheats indeed derived from spelta, formed from domesticated emmer and Ae. tauschii, and thus, carrying both the Tg and q genes, they carried a double dosage for hulledness. Since the chance for the occurrence of mutations in both of these two genes within several centuries is small, it is more likely that the first mutation, q to Q, occurred in domesticated emmer fields, forming naked tetraploid wheat (Muramatsu 1986), and the second mutation, Tg to tg, occurred in TgQ spelta fields, forming free-threshing wheat. The artificial spelta obtained by McFadden and Sears (1946) should contain both factors responsible for hulledness, namely, q and Tg, as they hybridized the hulled domesticated emmer, ssp. dicoccon and Ae. tauschii.
The non-free-threshing trait of the synthetic hexaploids, irrespective of carriage of Q or q by their tetraploid parent, was found to be due to the Tg gene derived from Ae. tauschii (Kerber and Rowland 1974). Some variation in the degree of glume tenacity was noted among the synthetic hexaploids; those having ssp. dicoccon as a parent and containing q and Tg were the most difficult to thresh (Kerber and Rowland 1974). The interaction between Tg and Q was clearly demonstrated by extraction of the tetraploid component of a hexaploid wheat and then resynthesizing the hexaploid (Kerber and Rowland 1974). The extracted tetraploids containing only the BBAA component of the original free-threshing hexaploids were also free-threshing. In later studies, crosses between the extracted free-threshing tetraploids and Ae. tauschii produced spelta-like hexaploids. It was concluded that the Tg gene of Ae. tauschii inhibits the expression of Q (Kerber and Rowland 1974). The interaction between tg and Q conferring the free-threshing character, is complementary (Kerber and Rowland 1974), namely, both tg and Q must be present for the expression of the free-threshing trait in hexaploid wheat. The probability that the genotypes of Ae. tauschii which served as the progenitors of hexaploid wheat possessed Tg—as apparently do all extant forms of this species—supports the above hypothesis that hulled, hexaploid wheats are more primitive than free-threshing hexaploids; they carried the Tg gene and, therefore, were non-free threshing (Kerber and Rowland 1974). The mutation from Tg to tg is presumed to have occurred at the hexaploid level.
The mutation from q to Q most probably occurred not so long after the creation of ssp. spelta. The free-threshing ssp. aestivum thus formed, was preferred by the early farmers of the region and quickly replaced the hulled forms. As man migrated to new areas, cultivated wheats encountered new environments, to which they responded with bursts of variation, resulting in many endemic forms. Secondary centers of variation for hexaploids in the Hindu Kush area of Afghanistan were described by Vavilov (1951). Transcaucasia is a secondary center for both tetraploid and hexaploid types. Such secondary centers of diversity provide valuable gene pools to wheat breeders, beyond those existing at the primary centers of variation.
ssp. spelta appears to be comprised of two genetic types: the Asiatic type which gave rise to the free-threshing ssp. aestivum, and the European spelta, which apparently descended from ssp. aestivum (Tsunewaki 1968). To distinguish between these two types, Kislev (1984) designated the Asiatic one “TgQ spelta” and the European type, carrying the tg gene, “tgq spelta”. ssp. spelta appeared in central Europe at ca. 4000 BP, about 2000 years later than forms of free-threshing hexaploid wheat. It could have been brought to Europe, where it replaced the free-threshing type in many sites of the upper Rhine region, particularly at high altitudes, where extreme temperatures prevail. Alternatively, ssp. spelta could have arisen in the Rhine valley through back-mutation of Q to q, or, more likely, as a result of a spontaneous hybridization between a hexaploid, free-threshing form (genotype QQtgtg) and tetraploid dicoccon (genotype qq), both of which were grown in that area, as suggested by Schiemann (1929), Tsunewaki (1968). This hybridization yielded, among others, hulled, spelt-type hexaploid progenies (genotype qqtgtg). The relatively wide distribution of ssp. spelta in central Europe in the past was presumably due to its winter hardiness and ability to out-yield the other crops on poor soils. ssp. spelta was also preferred for its good quality and it is still cultivated today in several areas of central Europe.
The possibility that European spelt is a form of comparatively recent origin that originated independently of the Asiatic spelt, was already proposed by Flaksberger (1939), Bertsch (1943, 1950), Kuckuck and Schiemann (1957). This hypothesis claimed that after establishment of bread wheat and domesticated emmer in Europe, the second type of ssp. spelta originated, mostly north of the Alps. While the European ssp. spelta is of the tgq spelta type, the genetic structure of the Iranian spelta is not known. On the basis of these genetic data, one can explain how Kuckuck in 1959, obtained free-threshing types, ssp. aestivum, among the progenies of crosses between Iranian and European spelt wheats (see Kuckuck 1964). A cross between a TgQ Asiatic spelta and a tgq European spelta yields, besides the two parental types, the two recombinants, tgQ and Tgq, of which the former is a free-threshing type. An important contribution to that hypothesis was presented by Blatter et al. (2002), who supported the claim of a European origin of ssp. spelta by analyzing the glutenin subunit genes B1-1 and A1-2 in 58 accessions of hexa- and tetraploid wheats from Europe and Asia. Their findings suggested that European spelt originated by introgression of a tetraploid wheat into free-threshing hexaploid wheat, as a secondary evolution after the development of bread wheat.
Dekaprelevich and Menabde (1932) assumed that ssp. macha is the primary form of hexaploid hulled wheats, from which ssp. spelta branched off. However, based on the morphological similarity between synthetic hexaploid wheat, formed from a cross of tetraploid wheat with Ae. tauschii, and ssp. spelta, the accepted view is that ssp. macha derived from spelta through mutations. Dekaprelevich and Menabde (1932) assumed that forms of ssp. macha contain the C allele, conferring a compact spike, while others contain the recessive c allele for normal spike. Cultivation of ssp. macha subspecies is currently limited to a restricted area in Transcaucasia. Another hulled form, ssp. vavilovii, characterized by branched spikes, has a restricted cultivation in Armenia and is considered to be a form of ssp. spelta (van Slageren 1994).
The advanced, free-threshing subspecies of T. aestivum, aestivum, compactum and sphaerococcum, differ from each other in only single genes (Mac Key 1954a, b). ssp. aestivum, bread wheat, is, by far, the most economically important wheat growing today on a world-wide scale. The earliest remnants of ssp. aestivum are from Can Hassan III, south Anatolia and Cafer Hoyuk from about the middle of the 9th millennium BP (see Hillman 1996; Bilgic et al. 2016). Finds of free-threshing hexaploids from the 8th millennium, have also been unearthed in western Iran, northern Iraq, eastern, central and western Anatolia, and other sites. Between 8000 and 7000 BP, ssp. aestivum, together with domesticated emmer, penetrated into the irrigated agricultural plains of Mesopotamia and, in the 6th millennium BP, into the Nile basin (Fig. 13.1). ssp. aestivum also appeared in archaeological finds of the 7th millennium BP, in the central and western Mediterranean basin. Forms of free-threshing hexaploid wheat appeared in central and western Europe at the end of the 6th millennium BP, associated (together with einkorn and emmer) with the first traces of agricultural activities. T. aestivum spread into central Asia and, by way of the highlands of Iran (8th millennium BP), to the Indus valley, where it appeared at the beginning of the 5th millennium BP (Fig. 13.1).
ssp. aestivum is assumed to have given rise to ssp. compactum (club wheat) and sphaerococcum (Indian dwarf wheat) through mutations. This assumption is based on the fact that no line of Ae. tauschii has been found to carry the compactum allele C or the sphaerococcum allele s, both of which are located on D-subgenome chromosomes (Rao 1972, 1977), indicating that these mutations appeared at the hexaploid level. The fact that ssp. spelta does not carry these genes clearly shows that neither ssp. compactum nor ssp. sphaerococcum could have been the first free-threshing hexaploids. The lineage of ssp. compactum from ssp. aestivum, entailed only a single mutation from c to C, believed to have occurred in the Near East. Subsequently, compactum was transported to Europe as an admixture with other wheats and was established in several places as the dominant form. ssp. compactum is grown today in a few restricted areas of Europe, the Near East, and the northwestern United States. ssp. sphaerococcum originated from aestivum by a single mutation as well (S to s), which presumably occurred in an ssp. aestivum that had been carried eastward, since sphaerococcum has not been found in the prehistoric Near East and its culture nowadays is largely confined to northwestern India and southern Pakistan. ssp. sphaerococcum has been documented in India as early as the 5th millennium BP, and currently grows, to some extent, in India and Pakistan.
A free-threshing wheat very similar to ssp. compactum was grown by the Neolithic Lake Dwellers of Switzerland at least 1000 years before ssp. spelta reached that part of Europe. This “Lake Dweller wheat”, now believed to be extinct, was described by Heer (1866) as T. vulgare antiquorum. It was a dwarf wheat with extremely small, stubby grains and compact, awnless spikes. Because of its resemblance to ssp. compactum, it has generally been assumed to have been a hexaploid wheat. The similarity between the tetraploid ssp. carthlicum (formerly T. persicum) and the Lake Dweller wheat eliminates the only reason for assuming that the latter was a hexaploid (Kislev 1979/1980).
Hexaploid T. aestivum originated only after the domestication of diploid and tetraploid wheats. While there is no wild progenitor to domesticated hexaploid wheat, a feral, semi-wild weedy form of hulled and brittle hexaploid wheat, ssp. tibetanum, which grows near the edges of wheat and barley fields, was discovered in Tibet (Shao et al. 1983). Since wild tetraploid wheats are not grown in China, this emmer-type brittle wheat is considered a derivative of a domesticated plant that underwent back-mutations at brittle rachis loci (Yen et al. 1988). Another emmer-type brittle hexaploid wheat, growing wild in Georgia, was described by Dekaprelevich in 1961. Kuckuck (1964) suggested that this wheat was derived from hybridization between a wild tetraploid wheat, most probably T. timopheevii ssp. armeniacum, and Ae. tauschii. Alternatively, this wheat was derived by back-mutations either from the free-threshing form, ssp. aestivum, or the hulled forms, ssp. spelta or macha.
To retrace the origin of the genome of modern bread wheat, ssp. aestivum, El Baidouri et al. (2017) investigated the evolutionary dynamics of gene-based transposable elements (TEs) and of single-nucleotide mutations across homoeologs of the A, B and D subgenomes of ssp. aestivum, as well as across hexaploid, tetraploid and diploid wheats. Based on these studies, they proposed a novel concept clarifying the structural asymmetry observed between the A, B and D subgenomes in bread wheat. Their concept derives from the cumulative effect of diploid progenitor divergence, the hybrid origin of the D subgenome, as was suggested by Marcussen et al. (2014), and subgenome partitioning following allopolyploidization events. In this model, the evolution of the A subgenome appears quite simple, whereas that of the other two subgenomes is more complex than initially reported. According to El Baidouri et al. (2017), the B subgenome in tetraploid/hexaploid wheat derived from an ancient S-genome progenitor, from which the modern S genome of Ae. speltoides had considerably diverged. The D subgenome of the progenitor Ae. tauschii hexaploid wheat derived from an ancient hybridization between A and S (Marcussen et al. 2014), as well as between other species (Li et al. 2015b), which that accounts for at least 19% of the origin of the modern D genome.
10.4.2.8.2 The Contribution of the D Subgenome to the Wide Adaptability of ssp. aestivum
The isozyme study conducted by Jaaska (1981) revealed intraspecific differentiation of Aegilops tauschii into two groups of biotypes, which essentially correspond to its two morphological subspecies, subsp. tauschii, with cylindrical spikes, and subsp. strangulata, with a bead-like arrangement of spikelets. Jaaska identified subsp. tauschii as the contributor of a D genome to the allotetraploid Ae. cylindrica (genome DDCC) and of the third subgenome, D, to the allohexaploid Ae. crassa ssp. crassa (genome DcDcXcXcDD), and ssp. strangulata as the contributor of a D subgenome to allohexaploid wheats, to the allotetraploids Ae. crassa subsp. macrathera (genome DcDcXcXc), to Ae. ventricosa (genome DDNN), and to the allohexaploid Ae. juvenalis (genome DcDcXcXcUU). Reinforcement of Jaaska’s (1981) conclusion, came from additional isoenzyme studies (Jaaska 1993), as well as biochemical and molecular studies (Wang et al. 2013, and reference therein), which confirmed that ssp. strangulata is the donor of the D subgenome to hexaploid wheat. ssp. strangulata has a narrower distribution than ssp. tauschii, mainly growing in the southwest fringes of the Caspian Sea (Jaaska 1993). This reinforces the suggestion that hybridization of tetraploid wheat with Ae. tauschii occurred in the Caspian region.
Ae. tauschii grows in a wide range of ecological conditions. It occupies both primary and segetal habitats (Eig 1929; Kimber and Feldman 1987; van Slageren 1994; Zohary et al. 2012) and thrives in areas characterized by continental climatic conditions, from the dry sagebrush steppes of the elevated Iranian and Afghan plateaus, to desert margins, as well as in more temperate climates, such as the rain-soaked southern coastal plain of the Caspian Sea. At the same time, throughout this, area Ae. tauschii is a successful colonizer of secondary, manmade habitats, and a common weed in cereal fields. Towards the periphery of its distribution, it is almost exclusively a weed in cultivation (Zohary et al. 2012).
Consideration of the ecology and distribution of Ae. tauschii reveals that this wild grass contributed substantially to the adaptation and worldwide success of bread wheats (Zohary et al. 2012). This is the easternmost diploid species in the wheat group, with a center of distribution lying in continental or temperate central Asia. It is widespread and very common in northern Iran and adjacent Transcaucasia, Transcaspia, and Afghanistan (Eig 1929; van Slageren 1994). From this geographic center, Ae. tauschii spreads west to east Turkey and Syria, and east to Pakistan. Ae. tauschii is a variable species represented by a multitude of forms, from slender types with cylindrical spikes (ssp. tauschii), to more robust plants with thick, beaded spikes (ssp. strangulata).
The wheat D subgenome appeared anomalous among the three wheat subgenomes, in its great fluctuation chromosomal diversity (Akhunov et al. 2010). Gene flow from A. tauschii has been an important source of wheat genetic diversity and influenced its distribution along the D‐subgenome chromosomes. Yet, despite its growth as a weed in bread wheat fields, and ample opportunities for hybridization between hexaploid wheat and its D-subgenome donor (Kihara et al. 1965), direct hybridization of Ae. tauschii with hexaploid wheat is arduous. On the other hand, Aegilops tauschii readily hybridizes with tetraploid wheat, and triploid hybrids often produce many unreduced gametes and are fertile (Matsuoka and Nasuda 2004; Zhang et al. 2010). This wide variation of forms may indicate recurrent formation of hexaploid wheat from many independent crosses, involving different genotypes of tetraploid wheat and Ae. tauschii (Kuckuck 1964; Mac Key 1966; Jakubziner 1959; Morris and Sears 1967; Feldman et al. 1995). This recurrent origin presumably occurred throughout the area where tetraploid wheat was farmed in the distribution area of Ae. tauschii, i.e., from eastern Turkey in the west up to western China in the east.
While tetraploid wheats, either hulled or free-threshing, in keeping with their Near Eastern origin, are adapted to the Mediterranean-type environments (with mild winters and warm, rainless summers), addition of the D subgenome of the central Asiatic tauschii greatly extended the range of adaptation of hexaploid wheats to a more continental climate and northern latitudes (Zohary 1969; Zohary et al. 2012; Feldman 2001). Incorporation of the Ae. tauschii subgenome rendered the hexaploid plants more capable of withstanding continental winters and humid summers, facilitating the spread of hexaploid bread wheat over the continental plateaus of Asia and the colder temperate areas in eastern, central, and northern Europe, explaining their prevalence in these regions.
The D subgenome confers many desirable bread wheat qualities, including bread making quality (Orth and Bushuk 1973), cold hardiness (Limin and Fowler 1981; Le et al. 1986), and salt tolerance (Schachtman et al. 1992). Bread wheat is the dominant crop in temperate countries and is used for human food and livestock feed. Its success, resulting from the addition of the D subgenome to the BA of tetraploid wheat, depends partly on its adaptability and high yield potential, but also on its gluten protein fraction, which confers the viscoelastic properties that allow dough to be processed into bread, pasta, noodles, and other food products (Shewry 2009). Bread wheat also contributes essential amino acids, minerals, and vitamins, and beneficial phytochemicals and dietary fiber components to the human diet and are particularly enriched in whole-grain products. However, wheat products are also known or suggested to be responsible for a number of adverse reactions in humans, including intolerances (notably celiac disease) and allergies (respiratory and food). Current and future concerns include sustaining wheat production and quality with reduced use of agrochemicals and developing lines with enhanced quality for specific end-uses, notably for biofuels and human nutrition (Shewry 2009).
In addition, accessions of Ae. tauschii, particularly those of subsp. strangulata, show resistance to many diseases (Yildirim et al. 1995; Cox et al. 1995; Appels and Lagudah 1990; Knaggs et al. 2000). The increase in cold hardiness ascribed to the D subgenome, supports Tsunewaki’s (1968) suggestion that the addition of this subgenome to tetraploid wheat enabled the spread of the cultivation of the resulting hexaploid to colder northern countries. Analysis of inter-varietal substitution lines, in which a chromosome of a cold hardiness cultivar of hexaploid winter wheat substituted its homologous chromosome in a spring cultivar, showed that chromosomes 4D and 5D accounted for much of the difference in cold hardiness between these two cultivars (Law and Jenkins 1970; Cahalan and Law 1979).
Hexaploid wheat has greater tolerance to frost and other environmental extremes than tetraploid wheat, and cultivation of hexaploid wheat consequently became far more widespread than that of tetraploid wheat (Dubcovsky and Dvorak 2007). Because farming of tetraploid wheat has been very limited in the Far East, such as China, introgression from Ae. tauschii did not take place in the Far East, while it continued in west Asia. The absence of introgression in the Far East subdivided Asian hexaploid wheat into two populations, western and Far Eastern (Dvorak et al. 2006; Balfourier et al. 2007). Because of the importance of tetraploid wheat as a bridge in gene flow from Ae. tauschii to hexaploid wheat, and because of the paucity of tetraploid wheat in the eastern area of wheat distribution, Far Eastern hexaploid wheat more faithfully documents the original hexaploid wheat than the west Asian hexaploid wheat (Dvorak et al. 2006). Since the identification of the parental species of T. aestivum (McFadden and Sears 1946), many synthetic hexaploids were produced by various researchers and breeders using a variety of different lines of tetraploid wheat and Ae. tauschii. These synthetic hexaploids were crossed with cultivars of ssp. aestivum, enriching the genetic basis of this important crop (Mujeeb Kazi et al. 1996; Dreisigacker et al. 2008).
10.4.2.8.3 Karyotype and Chromosome Morphology
The chromosomes of bread wheat ssp. aestivum cv. Chinese Spring were numbered from I to XXI by Sears (1954). But, on the basis of resemblance between different nullisomics (plants deficient for one pair of homologous chromosomes, and from study of nullisomic-tetrasomic combinations, the 21 chromosomes have been placed in seven homoeologous groups of 3 (Sears 1952). Within these groups each tetrasome (plant with four homologous chromosomes) shows the ability to compensate to some degree for either of the two other two nullisomes. The placement of the various chromosomes to one of the subgenomes was followed. For subgenome D this determination involved crossing each momsome (2n = 41; 20II + 1I) with tetraploid wheat (2n = 14II) and observing whether the F1 has 14 bivalents and 6 univalents or 13 bivalents and 8 univalents. Okamoto (1957b) identified the A- and B-subgenome chromosomes by the occurrence of a heteromorphic bivalent in F1 hybrids involving telocentrics of particular A- and B-subgenome chromosomes and the amphiploid AADD. The allocation of the various chromosomes to subgenomes and homoeologous groups made possible the assignment of each chromosome to its respective genome and homoeologous group and to suggest a more logical system of renumbering the chromosomes of bread wheat (Sears 1959). This renumbering assigned the 21 chromosome pairs toto their respective subgenomes and homoeologous groups (Table 10.14).
Previous efforts to identify the chromosomes of hexaploid wheat in somatic cells by their morphological characteristics (Levitsky et al. 1939; Camara 1943, 1944; Schulz-Schaeffer and Haun 1961; Khan 1963), failed to yield satisfactory results because of the similarity between some of the chromosomes. With monosomics (chromosomes that exist in a single dose rather than in two), it is possible to study chromosome morphology, because a monosome appears as a univalent at first meiotic metaphase and lags behind the other chromosomes during first and second meiotic anaphases (Sears 1954). After measuring the size of monosomic ssp. aestivum cv. Chinese Spring chromosomes at second meiotic telophase, Morrison (1953) noted two chromosomes with a secondary constriction that was assumed to contain the nucleolar-organizing regions (NORs), one in chromosome 1B and a second in 6B.
Giorgi and Bozzini (1970), using aneuploid lines of hexaploid wheat cv. Chinese Spring, succeeded to study, with sufficient accuracy, the morphology of somatic metaphase chromosomes in root tip cells and compared them with those of tetraploid wheat, T. turgidum ssp. durum cv. Cappelli, and of the diploid Ae. tauschii. Using relative chromosome length and arm ratio as criteria, they observed that, apart from minor differences, the chromosomes of the A and B subgenomes of hexaploid wheat are very similar to those of tetraploid wheat, and the chromosomes of the D subgenome are similar to those of Ae. tauschii, showing that there were no major structural changes at the hexaploid level. Whereas homoeologous chromosomes generally have similar arm ratios, no simple relationship exists between chromosome homoeology and chromosome lengths. Giorgi and Bozzini (1970), like Morrison (1953), identified two pairs of satellited chromosomes (1B and 6B), 5 medians (7B, 7A, 6A, 7D, and 6D), 10 submedian (3B, 2A, 3A, 2B, 4B, 4A, 1A, 3D, 2D, and 4D), and 4 subterminal (5B, 5A, 1D, and 5D) chromosomes in the complement of Chinese Spring.
Measurements presented by Sears (1954), of the monosomes of the bread wheat cultivar Chinese Spring at second meiotic telophase, were in reasonable agreement with Morrison’s (1953) results. The measurements obtained at first meiotic metaphase and second meiotic telophase by Sears (1954) (Table 10.15) showed that average chromosome length at MI in the B subgenome is 6.43 µ, at TII is 10.14 µ, and total B subgenome length at MI is 44.98 µ and at TII 70.97 µ. Chromosome 5B is the most brachial and 6B is the least brachial, almost metacentric. Average chromosome length in the A subgenome at MI is 5.6 µ and at TII 8.15 µ, and total A subgenome length at MI is 39.56 µ and at TII 57.03 µ. Chromosome 1A is the most brachial and 6A is the least brachial, submetacentric and almost metacentric. Average chromosome length in the D subgenome at MI is 5.22 µ and at TII 6.97 µ, and total D subgenome length at MI is 36.57 µ and at TII 48.76 µ. Chromosomes 5D and 1D are the most brachial and chromosome 6D is the least brachial. Chromosomes 3B and 2B are the longest and 6D is the shortest in the complement.
Sasaki et al. (1963), measuring monosome length at first meiotic metaphase of the bread wheat winter cultivar Cheyenne, and Gill et al. (1963), measuring monosome length at first meiotic metaphase and at second meiotic anaphase of the bread wheat winter cultivar Wichita, found, similar to Sears’s (1954) measurements in the spring cultivar Chinese Spring, that the B subgenome included the longest chromosomes, while the D subgenome had the shortest ones. Like Sears (1954), Sasaki et al. (1963), Gill et al. (1963) also Giorgi and Bozzini (1970) found that the chromosomes of the D subgenome are usually the smallest in the complement, i.e., the total chromosome length of the D subgenome is 28.2% of the total chromosome complement length of hexaploid wheat.
In the 1970s, modern staining techniques were used to analyze the structures of cereal chromosomes, and a cytogenetic karyotype of wheat was developed (Gill and Kimber 1974a; Gill et al. 1991; Jiang and Gill 1994a). Among the several staining methods, two techniques, namely, C-banding and N-banding, have been most useful in cytogenetic studies of wheat (Gill 1987). While C-bands mark constitutive heterochromatin and stain all somatic metaphase chromosomes in hexaploid wheat, N-bands reveal specialized heterochromatin on only nine of the 21 chromosome pairs, i.e., all of the B genome chromosomes and chromosomes 4A, and 7A (Gerlach 1977). The remaining chromosomes show either faint bands or no bands at all. Later, Endo and Gil (1984) identified 16 of the 21 chromosomes of hexaploid wheat using an improved N-banding technique.
Endo and Gill (1984), using N-banding, and Gill (1987), using C-banding, measured chromosome length at metaphase in somatic cells of the bread wheat cultivar Chinese Spring and found, like Sears (1954), Giorgi and Bozzini (1970), that the B subgenome included the longest chromosomes and the D subgenome the shortest chromosomes. Like Morrison (1953), Gill et al. (1963), Giorgi and Bozzini (1970), Endo and Gill (1984), Gill (1987) also observed secondary constrictions and satellites on the short arms of chromosomes 1B and 6B.
There are some discrepancies between the measurements of Sears (1954) and those of Endo and Gill (1984), Gill (1987) which presumably resulted from the sample preparation and measurements techniques. Yet, in all these studies, the B subgenome was the largest (38%), the A subgenome was intermediate (33%), and the D subgenome was the smallest (28%) of the chromosome complement. The chromosomes of the B and the D subgenomes were more heterobrachial than those of the A subgenome, with chromosome 5B being the most and 7A the least heterobrachial. implying perhaps that the chromosomes of subgenomes B and D underwent more chromosomal rearrangements than those of subgenome A. Since cv. Chinese Spring has been shown to possess a ‘primitive’ chromosome structure and has been extensively used for the development of cytogenetic stocks, and in genetic studies, its idiogram was adopted as the wheat standard.
Pedersen and Langridge (1997), using the Ae. tauschii clone pAs1, together with the barley clone pHvG38 (a GAA-satellite sequence) for two-color FISH, were able to identify the entire chromosome complement of hexaploid wheat, facilitating easy discrimination of the three genomes of wheat. A detailed idiogram was constructed, including 73 GAA bands and 48 pAs1 bands. Identification of the wheat chromosomes by FISH will be particularly useful in connection with the physical mapping of other DNA sequences to chromosomes, as well as for chromosome identification in general, as an alternative to C-banding.
10.4.2.8.4 Chromosomal Rearrangements in ssp. aestivum
Chromosomal rearrangements are abundant among accessions of allopolyploid wheats. Using the C-banding technique, Badaeva et al. (2007) detected chromosomal rearrangements in 70 of 208 accessions of tetraploid wheat, and 69 of 252 accessions of hexaploid wheat. Among all chromosomal aberrations identified in tetraploid and hexaploid wheats, single translocations were the most frequent type (39 types), followed by multiple rearrangements (9 types), pericentric inversions (9 types), and paracentric inversions (3 types). The breakpoints were located at or near the centromere in 60 rearranged chromosomes, while, in 52 cases, they were in interstitial chromosome regions. In the latter group, translocation breakpoints were often located at the border between constitutive heterochromatin (C-bands) and euchromatin or between two adjacent C-bands. According to Badaeva et al. (2007), some of these regions seem to be translocation “hotspots”. Their results, as well as data published by other authors, indicate that translocations most frequently involve B-subgenome chromosomes, followed by A- and D-subgenome chromosomes. Individual chromosomes also differ in the frequencies of translocations. Other translocations seem to occur independently and their broad distribution can result from selective advantages of rearranged genotypes in diverse environmental conditions. Badaeva et al. (2007) found significant geographic variation in the spectra and frequencies of translocation in wheat: the highest proportions of rearranged genotypes were found in Central Asia, the Middle East, Northern Africa, and France. A low proportion of aberrant genotypes was characteristic of tetraploid wheat from Transcaucasia and hexaploid wheat from Middle Asia and Eastern Europe.
In hexaploid wheat, evolutionary translocation involving chromosome arms 4AL (formerly 4BL), 5AL, and 7BS were proposed by Naranjo et al. (1987), following study of induced homologous chromosome pairing with the aid of differential chromosome staining. A similar translocation exists in rye, also involving chromosomes 4R, 5R and 7R (Naranjo et al. 1987). Since diploid wheat, T. monococcum, has a similar 4AmL/5AmL translocation (Miller et al. 1981), it was concluded that the translocation 4L/5L is an ancestral translocation involving many Triticineae species.
Genetic maps of wheat chromosome 4A, and the chromosomal locations of 70 sets of isozymes and molecular homoeologous loci, have been used to further define the structure of wheat chromosomes 4A, 5A and 7B (Liu et al. 1992). Evidence was provided showing that an interstitial segment on 4AL originated from 5AL. The construction of comparative genetic maps of chromosomes 4Am and 5Am of T. monococcum, and of chromosomes of homoeologous groups 4, 5 and 7 of ssp. aestivum has provided insight into the evolution of these chromosomes (Devos et al. 1995). As was shown by Naranjo et al. (1987), and Liu et al. (1992), wheat chromosome 4A is a translocated chromosome carrying segments derived from 4A, 5A, and 7B. This translocation existing in bread wheat, which can be explained by a 4AL/5AL translocation that already occurred at the diploid level, before the differentiation of T. urartu and T. monococcum, is an important chromosomal rearrangement incident (Luo et al. 2018). Three further rearrangements, a 4AL/7BS translocation, a pericentric inversion and a paracentric inversion, took place in the tetraploid progenitor of hexaploid wheat (Devos et al. 1995). The structurally rearranged chromosomes 4A, 5A, and 7B are an exception to other translocations. The first step in these rearrangements was fixation of a 4A/5A translocation in diploid ancestors of several Triticineae taxa. This translocation existed already in diploid wheat prior to the divergence of T. monococcum and T. urartu. The remaining rearrangements were fixed during the evolution of T. turgidum ssp. dicoccoides. These involved a pericentric inversion in 4A which converted the long arm into the short arm, a paracentric inversion in the 4AL arm, and a reciprocal translocation between 7BS and the rearranged 4AL arm. Translocations fixed during the evolution of T. turgidum ssp. dicoccoides differ from those fixed during the evolution of T. timopheevii ssp. armeniacum.
Although additional terminal translocations and inversions in the A, B, and D subgenomes may have been fixed during the evolution of the three subgenomes of T. aestivum, and escaped molecular detection, the order of loci in wheat homoeologous chromosomes is largely colinear.
10.4.2.8.5 Nucleolar-Organizing Regions (NORs) and rRNA Genes
Crosby (1957) studied the nucleolar activity of each of the 21 chromosomes of the complement of ssp. aestivum cv. Chinese Spring, by analyzing micronucleus formation at second meiotic anaphase and telophase of the lagged monosomic chromosomes. She found that four chromosomes can produce nucleoli in the pollen mother cells (PMCs): chromosome 1B produced nucleoli in 15% of its micronuclei, chromosome 6B in 20%, chromosome 1A in 13% and chromosome 5D in 7%. The normal nuclei in PMCs of disomic plants had an average 1.5 nucleoli per cell. Lines with four doses of chromosome 1B ((tetra 1B) and four doses of chromosome 6B each had an average of 3.0 nucleoli per PMC; tetra 1A and tetra 5D had 2.1 and 2.0 nucleoli per PMC, respectively. Thus, Crosby (1957) concluded that chromosomes 1B and 6B have strong nucleolar-organizing capacity, while chromosomes 1A and 5D have a weaker capacity. Crosby-Longwell and Svihla (1960) further studied the effect of increased and decreased doses of the chromosomes bearing NORs on nucleoli number in PMCs of bread wheat, and found that removal of pairs of strong nucleolar chromosomes induced latent nucleolar chromosomes to compensate for almost 100% of the nucleolar activity of the missing pair of strong nucleolar chromosomes.
Nucleolar organizer regions (NORs), which are located in the secondary constrictions of satellited chromosomes, have been shown to be the sites of multiple rRNA genes in eukaryotes (Birnstiel et al. 1971). In accordance, studies of Flavell and Smith (1974), Flavell and O’Dell (1976), Miller et al. (1980) showed that the major rRNA gene clusters in ssp. aestivum and ssp. spelta are located in chromosome 1B and 6B. Additional smaller sites were found on chromosomes 1A and 5D. This was confirmed by Hutchinson and Miller (1982), who showed four pairs of sites in some cells of ssp. spelta and ssp. aestivum. Using in situ hybridization of cloned ribosomal DNA, Hutchinson and Miller (1982), established the numbers of NORs in a range of subspecies of T. aestivum. In all subspecies, two pairs of sites occurred on chromosome arms with marked satellites. However, ssp. compactum and ssp. sphaerococcum showed an additional pair of minor sites located on a chromosome without an obvious satellite.
Following Crosby (1957), also Flavell and Smith (1974) and Flavell and O’Dell (1976) considered chromosomes 1B and 6B as possessing “strong” and the 1A and 5D as “weak” nucleolar organizers. NORs on 1B and 6B of the cultivar Chinese Spring possess approximately 90% of the total rRNA gene complement. Chromosome 6B possesses approximately 5500 (60%) rRNA genes, chromosome 1B possesses 2700 (30%) rRNA genes, whereas chromosomes 1A and 5D possess 950 (10%) rRNA genes of the total 9150 rRNA genes of the cv. Chinese Spring (Flavell and Smith 1974). Yet, different cultivars of bread wheat have different numbers of ribosomal RNA genes, as indicated by rRNA/DNA hybridizations (Flavell and Smith 1974; Mohan and Flavell 1974). For Example, in the cultivar Holdfast, chromosome 6B possess approximately only 2000 ribosomal RNA genes (Flavell and Smith 1974).
In plants, the rRNA cistrons (18S-5.8S-26S) are organized as families of repeated units in tandem arrays, at the NORs of chromosomes. Each repeating unit consists of one rRNA sequence including transcribed (18S-5.8S-26S) and non-transcribed spacer regions. The number of repeat units and the size of the spacer vary across plants. Also in hexaploid wheat the ribosomal RNA genes are organized in tandem arrays at the nucleolus organizers (Flavell 1989). By the use of various aneuploid lines and other genetic stocks, and by in situ hybridization using high specific activity 125I-rRNA, Appels et al. (1980) determined the location of the rRNA genes in wheat, rye and barley and studied the organization of the ribosomal RNA cistrons in these grasses. Their study confirmed the location of the 18S-5.8S-26S rRNA gene repeat units in ssp. aestivum (cv. Chinese Spring) on chromosomes 1B, 6B and 5D, and this repeating unit is approximately 9.5 kb long (Appels et al. 1980).
In situ hybridization in conjunction with deletion mapping (using chromosomal deficiencies described by Endo and Gill 1996) was employed to physically map the 18S.26S multigene rRNA gene family in ssp. aestivum cv. Chinese Spring (Mukai et al. 1991). These authors found a new locus in the long arm of chromosome 7D of Chinese Spring and Aegilops squarrosa, and also confirmed the location of the NOR locus at the telomeric end of the short arm of chromosome 1A. Moreover, they showed that the rDNA exists as condensed DNA (heterochromatic) at each end, while diffused rDNA was identified within the secondary constriction region of the NORs in 1B (Nor-B1), 6B (Nor-B2), and 5D (Nor- D3). On the basis of these observations, Mukai et al. (1991) supported the model of Hilliker and Appels (1989) which claimed that the usual state of rDNA is inactive (facultatively heterochromatic). A small fraction of rDNA at a specific location (usually in the middle of the NORs in wheat) exists as a diffuse region (active) in condensed metaphase chromosomes.
In ribosomal DNA, there are transcribed and non-transcribed spacers within and between gene clusters. The transcribed spacer contains both internal transcribed spacer (ITS) and external transcribed spacer (ETS) (Flavell 1980). The ITS is the spacer DNA situated between the small-subunit rRNA and the large-subunit rRNA genes in the polycistronic rRNA precursor transcript; ITS1 is located between 18S and 5.8S rRNA genes, while ITS2 is between 5.8S and 25S. Thus, each eukaryotic ribosomal cluster contains the 5′ ETS, the 18S rRNA gene, ITS1, the 5.8S rRNA gene, ITS2, the 25S rRNA gene, and finally the 3′ ETS. During rRNA maturation, ETSs and ITSs are excised (Flavell 1980) and rapidly degraded.
The non-transcribed spacer, termed the intergenic spacer (IGS) or non-transcribed spacer (NTS), separates the rRNA genes (and internal transcribed spacers) that are arranged in tandem repeats. Due to the non-coding nature of spacer DNA, its nucleotide sequence changes much more rapidly over time than nucleotide sequences coding for proteins that are subject to selective forces. Although spacer DNA might not have a function that depends on its nucleotide sequence, it may still have sequence-independent functions.
Although rRNA gene clusters were homogeneous within cultivars of ssp. aestivum and could be assigned to particular chromosomes, extensive polymorphism was observed for the spacer region in various cultivars (Appels and Dvorak 1982). May and Appels (1987) examined the length of the non-transcribed spacer separating rRNA genes in 25 ssp. aestivum cultivars, carrying up to 3000 such genes on chromosomes 1B and 6B. The data showed that there were three distinct alleles of the 1B locus, and at least five allelic variants of the 6B locus. Chromosome 5D had only one allelic variant. Whereas the major spacer variants of the 1B alleles apparently differed by the loss or gain of one or two of the 133 bp sub-repeat units within the spacer DNA, the 6B allelic variants showed major differences in their compositions and lengths. This may be related to the greater number of rRNA genes repeat units at this locus.
Genetic variation exists within a species for the number of the rRNA genes at a locus and also for the structure of the intergenic, regulatory DNA. This variation can affect the activity of a locus, relative to that of another in the same cell (Flavell 1989). The active loci are enriched with genes that are not methylated at specific CpG residues in the intergenic regulatory DNA. Flavell (1989) suggested a model that attempts to relate the structural variation between genes to the differential expression and nucleolar organization of the rRNA genes at different loci. The model is based on the affinity of proteins, at limited concentrations, to specific regulatory DNA sequences. These sequences are subject to change as a result of mechanisms that can spread mutations through a locus. The resulting variation, which may not be eliminated by selection, unless it is very deleterious and accounts for a large part of the total rDNA, may be one reason why plants maintain a large excess of ribosomal RNA genes.
Flavell and O’Dell (1979) investigated the genetic control of the various NORs in root tip cells of bread wheat by cytologically scoring the number of nucleoli per cell in (a) aneuploid derivatives of cv. Chinese Spring, each having a different dosage of a particular chromosome or chromosome arm, and (b) in substitution lines where nucleolus organizer chromosomes had been replaced by homologues possessing different NORs. They assumed that NOR activity correlates with nucleolus size and thus, with the intensity of a cytologically visible marker. The authors reported that the weak NORs on chromosomes 1A and 5D infrequently formed a visible nucleolus in the presence of the strong NORs on chromosomes 1B and 6B. When a major pair of NORs on chromosomes 1B or 6B was deleted, the smaller NORs formed a visible nucleolus more frequently. Similarly, when the major NORs were replaced by weak NORs, the smaller nucleolus organizers formed visible nucleoli more frequently. When a small nucleolus organizer was replaced by a strong NOR a larger nucleolus is formed. These and other findings led to the general conclusions that there is a correlation between the number of rRNA gene and nucleolus size, i.e., the relative size of the nucleolus formed depends principally upon the number of the total active rRNA genes in the cell. Varying the dosage of at least 13 non-nucleolus-organizer chromosomes also resulted in changes in the number of visible nucleoli per cell, implying that, in bread wheat, genetic control of the activity of individual nucleolus organizers is complex (Flavell and O’Dell 1979).
The number of nucleoli visualized at interphase by specific silver (Ag) staining, was also used to infer the activity of NORs. The silver staining procedure can be used to visualize gene activity at the ribosomal DNA sites with conventional light microscopy, since only NORs that are functionally active during the preceding interphase are stained by silver. Using this procedure, Lacadena et al. (1984) studied amphiplasty (suppression or dominance of NOR activity) in somatic metaphase cells of the synthetic allohexaploid triticale (tetraploid wheat-rye amphiploid) and found that while the NORs on 1B and 6B were active, rye NORs were suppressed. Cermeño et al. (1984) provided evidence for only four active NORs in hexaploid wheat, likely corresponding to the chromosome pairs 1B and 6B. However, some somatic metaphase cells also showed NOR activity on 1A and 5D. Their results clearly demonstrated the relative nucleolar activity of the four organizer chromosomes to be 6B > 1B > 5D > 1A in euploid, ditelosomic and nulli-tetrasomic plants of common wheat. Inclusion of a nucleolus organizer chromosome from Ae. umbellulata in the bread wheat genome, caused suppression of the wheat nucleolus organizers, while the Ae. umbellulata organizer remained active (Flavell and O’Dell 1979). Such suppression occurs in many interspecific plant hybrids and was described by Navashin (1928, 1931) as differential amphiplasty, i.e., dominance of one nucleolar organizer over another. Differential amphiplasty has been reported to exist in tetraploid and hexaploid wheats (Lacadena et al. 1984, and references therein).
Nucleolar differential amphiplasty is an epigenetic phenomenon that describes the formation of nucleoli, by chromosomes inherited from only one parent/progenitor of a genetic hybrid (Pikaard 2001). As only transcriptionally active rRNA genes give rise to nucleoli, the molecular basis for nucleolar dominance or amphiplasty is differential rRNA gene expression that might result from selective silencing of specific subsets of rRNA genes via changes in DNA methylation and histone posttranslational modifications (Pikaard 2001). Because rRNA genes are nearly identical in sequence, it has long been a mystery how rRNA genes destined for silencing can be discriminated from genes that remain active. However, recent genetic evidence indicates that selective rRNA gene silencing results from inactivation of entire NORs, and not through mechanisms that discriminate between individual rRNA genes (Pikaard 2001).
rRNA genes at different NOR loci in hexaploid wheat are expressed at different levels. Even in cv. Chinese Spring, the NOR on chromosome 1B is partially dominant to that on chromosome 6B, since the 1B locus is more active despite the smaller number of genes (Thompson and Flavell 1988). These authors have previously shown that these and other examples of nucleolar dominance in wheat are associated with undermethylation of cytosine residues in certain regions of the dominant rDNA. Thompson and Flavell (1988) showed that rRNA genes at dominant loci are organized in a chromatin conformation that renders them more sensitive to DNase I digestion than other rRNA genes.
Ribosomal RNA genes of T. aestivum, are known to be expressed at different levels and some loci exhibit full or partial dominance over others (Gustafson and Flavell 1996). Nucleolar dominance is best seen in hexaploid triticale where the wheat loci dominate over the rye NOR locus. A correlation appears to exist between the methylation of cytosine residues and the expression of a rRNA locus suggesting that a dominant locus would have a much-reduced methylation pattern over a recessive locus. The effect on rye NOR expression in tetraploid triticales containing various wheat and rye NOR loci was studied by Gustafson and Flavell (1996). The results showed that when both wheat chromosomes 1B and 6B were present, the rye NOR locus was methylated and suppressed. When either 1B or 6B were present, some minor rye activity was seen, and that a slightly higher degree of activity was observed in the absence of 1B versus 6B. When both 1B and 6B were absent, the rye locus was expressed as in rye. These data indicate that either one of the wheats rRNA gene loci suppress rye rRNA gene loci.
Flavell et al. (1988) studied cytosine methylation in wheat rRNA genes at nucleolar organizers displaying different activities. They observed that the methylation pattern within a specific multigene locus is influenced by the number and type of rRNA genes in other rRNA gene loci in the cell. Dominant, very active loci had a higher proportion of rRNA genes with nonmethylated cytosine residues in comparison with recessive and inactive loci. The authors concluded that cytosine methylation in rRNA genes is regulated and that the methylation pattern correlates with the transcription potential of an rRNA gene. Suppression of rRNA genes, originating from one parent, is often due to cytosine methylation (Thompson and Flavell 1988; Gustafson and Flavell 1996; Houchins et al. 1997). Neves et al. (1995) showed that treatments during germination with the cytosine analogue 5-azacytidine, that causes cytosine demethylation, stably reactivated the expression of the suppressed rRNA genes of rye in triticale.
Wheat rRNA genes are methylated at CCGG sites that are present in the intergenic regions (Sardana et al. 1993). In all the genotypes of T. aestivum studied, the rRNA gene loci with larger intergenic regions between their genes, possessed a larger number of rRNA genes unmethylated at one or more CCGG sites in the intergenic regions as compared to loci with shorter intergenic regions. In four genotypes, rDNA loci with longer intergenic regions had larger secondary constrictions on metaphase chromosomes, a measure of relative locus activity, as compared to loci with shorter intergenic regions. The findings have been integrated into a model for the control of rDNA expression based on correlations between cytosine methylation patterns and the number of upstream 135 by repeats in intergenic regions (Sardana et al. 1993).
The reduction in the number of rye rRNA genes containing an unmethylated CCGG site in the promoter was associated in wheat x rye hybrids with the suppression of the rye nucleolus (Houchins et al. 1997). These results are consistent with a model in which promoter and upstream regulatory repeats of rRNA genes compete for limited concentrations of regulatory proteins, and genes that are methylated at key binding sites fail to engage these regulatory proteins and thus remain inactive.
Carvalho et al. (2010) studied the methylation patterns of the NOR regions in 18 Portuguese bread wheat lines, of which 10 presented six Ag-NORs per somatic metaphase and six nucleoli per interphase, and eight presented four Ag-NORs per metaphase and four nucleoli per interphase. Using Southern blot, with pTa71 as probe, which identified a complete rDNA unit of bread wheat, they noted that DNA digestions, performed by the restriction enzymes MspI and HpaII, resulted in different patterns, revealing the high level of cytosine methylation at their recognition sequences. The total percentage of NOR methylation indicated that wheat lines with a maximum of four Ag-NORs were more heavily methylated at the NOR region than lines with a maximum of six Ag-NORs.
Jointly with 25S and 5.8S rRNA, also 5S rRNA is an integral component of the large ribosomal subunits in plants. The genes coding for the 5S rRNA (5S DNA) of T. aestivum have been extensively studied (e.g., Gerlach and Dyer 1980; Appels et al. 1980; Scoles et al. 1988; Dvorak et al. 1989). This species contains several thousands of repeated 5S DNA units that are arranged in tandem arrays and are located at one or two loci in the A, B, and D subgenomes of T, aestivum (Appels et al. 1992). The 5S DNA multigene family in bread wheat cv. Chinese Spring consist of 10,000 copies of the 5S rRNA coding sequence per nucleus (Appels et al. 1980). Sequencing of entire repeating units in ssp. aestivum showed that there are two size classes of repeating units, 410 and 500 bp, in the 5S rRNA genes (Gerlach and Dyer 1980). Each of the size classes carry 5S rRNA genes (120 bp) coding for a small 120-bp molecule that forms part of the ribosome, and a variable spacer region (290 bp and 380 bp, respectively) (Baum and Bailey 2001). The spacer region changes much faster in evolution than the gene region (Fedoroff 1979; Scoles et al. 1988; Sastri et al. 1992) and consequently, each 5S DNA locus consists of tandem arrays of sequences containing blocks that are highly conserved (gene regions), alternating with blocks that are highly divergent (spacer regions) (Scoles et al. 1988; Baum and Appels 1992; Sastri et al. 1992). The units at a given locus are very similar in DNA sequence but marked differences have been observed between loci. Nucleotide sequences of the two clones showed that their 120-bp coding regions were very similar, while the spacers showed very low homology, indicating that their divergence must be relatively ancient.
In T. aestivum, the short (410 bp) units were found in the short arm of chromosomes 1B and 1D, while the repeated 500-bp units were in the short arm of chromosomes 5A and 5B (Dvorak et al. 1989). This suggests that, although the two subfamilies evolved in concert in the coding regions, homogenization between the spacers of different subfamilies, is limited or does not occur. This lack of homogenization of spacers between 5S DNA loci of different genomes in polyploid wheat, parallels a similar lack of spacer homogenization of the Nor loci between the B and D genomes of bread wheat (Lassner et al. 1987).
The number of 5S DNA repeats in T. aestivum is estimated to be 4700–5200 copies for the short sequence and almost 3100 copies for the long one (Appels et al.1992; Sastri et al. 1992). The copy number, however, may differ among cultivars (Röder et al. 1992). The 5S DNA repeats are located in bread wheat on the short arms of chromosomes of homoeologous groups 1 and 5 (Dvorak et al. 1989); those of the short-size class are located on group 1 chromosomes, while those of the long-size class are located on group 5 chromosomes (Appels et al. 1992). The physical location of these loci was assigned more precisely by deletion mapping and in situ hybridization (Mukai et al. 1990). The six loci of 5S DNA units located on chromosome arms 1AS, 5AS, 1BS, 5BS, 1DS, and 5DS were designated by Dvorak et al. (1989), according to the rules for wheat genetic nomenclature, 5SDna-A1, 5SDna-Bl, and 5SDna-Dl, on chromosome arms 1AS, lBS, and 1DS, respectively, and 5SDna-A2, 5SDna-B2, and 5SDNA-D2 on chromosome arms 5AS, 5BS, and 5DS, respectively.
In wheat, the major 5S RNA gene sites are close to the secondary constrictions where the 18S-5.8S-26S repeating units are found. The repeat unit of the 5S RNA genes was approximately 0.5 kb in wheat (Appels et al. 1980). Dvorak et al. (1989) determined the location of 5S rRNA genes (5S DNA) in bread wheat on chromosome arms 1BS, 1DS, 5AS, 5BS, and tentatively 5DS.
In chromosome arm 1BS, the 5S DNA probe hybridized in situ to the middle of the satellite (Appels et al. 1980). Chromosome 1B shows a C-band at that position. This suggests equivalence between the subterminal C-band in the satellite of chromosome 1 and the physical location of the 5S DNA. Deletion mapping of chromosome 5B placed all 5S DNA copies into the distal half of the short arm (Kota and Dvorak 1986). As in the short arm of chromosome lB, there is a subterminal C-band in this region. Hence, the subterminal C-bands of 1BS, 1DS, 5AS, and 5BS may be equivalent to the 5S DNA arrays (Dvorak et al. 1989).
These observations suggest that 5S DNA is located in a single locus in each chromosome arm. According to the rules for wheat genetic nomenclature and in adherence with the designations used for 5S DNA by Xin and Appels (1988), the loci on chromosome arms 1AS, lBS, and1DS were designated 5SDna-A1, 5SDna-Bl, and 5S Dna-Dl, respectively. The loci on chromosome arms 5AS, 5BS, and 5DS were designated 5SDna-A2, 5SDna-B2, and 5SDNA-D2, respectively. The existence of several species in which there is no linkage between the NORs and 5S DNA loci.
10.4.2.8.6 Genome Size
The 1C DNA content in the subspecies of T. aestivum ranges from 17.67 pg in ssp. aestivum to 18.92 pg in ssp. tibetanum (Eilam et al. 2008). A similar estimate was provided by Bennett (1972), who reported on 18 pg 1C DNA in ssp. aestivum, and a somewhat lower estimate by Arumuganathan and Earle (1991), who reported on 16.5 pg in this subspecies. Two cultivars (4 plants) of ssp. spelta had a mean of 17.72 ± 0.039 pg, 12 cultivars (19 plants) of ssp. aestivum had 17.67 ± 0.311 pg, one cultivar (2 plants) of ssp. compactum had 17.78 pg, two cultivars (4 plants) of ssp. sphaerococcum had 17.99 ± 0.244 pg, and one line (2 plants) of ssp. tibetanum had 18.92 pg 1C DNA. The amount of DNA in the four domesticated subspecies of T. aestivum did not differ significantly, whereas ssp. tibetanum had a significantly higher DNA content than ssp. aestivum and ssp. spelta (but only one line was analyzed in ssp. tibetanum) (Eilam et al. 2008). The DNA content of T. aestivum did not differ from that of the other hexaploid wheat, T. zhukovskyi (Eilam et al. 2008). Nishikawa and Furuta (1968) found no significant differences in DNA content among American and Japanese cultivars of ssp. aestivum. Likewise, Nishikawa and Furuta (1969), Furuta et al. (1974), Eilam et al. (2008) reported no differences in DNA content neither between synthesized hexaploid wheat and cultivars of this subspecies, nor between the various subspecies of T. aestivum. The synthesized hexaploids have nuclear DNA content equal to the sum of the DNA contents of their respective parents (Nishikawa and Furuta 1969; Furuta et al. 1974). Similarly, Rees (1963), Rees and Walters (1965), Pegington and Rees (1970) found no evidence of appreciable change in nuclear DNA subsequent hybridization and allopolyploidy that gave rise to the hexaploid wheats. Yet, Pegington and Rees (1970) found that chromosomes in T. aestivum are shorter than in its tetraploid and diploid ancestors, which they claim is not reflection of a diminution in the chromosome material but, rather, of its reorganization. In contrast, Pai et al. (1961) reported that a considerable degree of elimination of chromosomal material took place in hexaploid wheats subsequent their origin, and Upadhya and Swaminathan (1963a) reported that in two studied cultivars of ssp. aestivum, there is less DNA than the expected amount from the sum of its two putative parents. Pai et al. (1961), Upadhya and Swaminathan (1963a) suggested that this reduction in DNA content might have been an important factor in the conversion of allopolyploid wheats into functional diploids. The combination of the multivalent gene suppressor system, the Ph1 gene, and DNA elimination, appears to have led to a synthesis of the advantageous features of allopolyploidy in wheats. Eilam et al. (2008) also found that the 1C DNA content of T. aestivum is significantly smaller than the expected additive amount of 1C DNA of its two putative parents, namely, 12.84 ± 0.175 pg in T. turgidum ssp. durum, one of the putative donors of the B and A subgenomes, and 5.17 ± 0.087 pg of Ae. tauschii, the donor of the D subgenome (Eilam et al. 2007, 2008).
Furuta et al. (1984) determined the DNA content of the three subgenomes of hexaploid wheat by summing the DNA contents of the seven individual chromosomes of each subgenome. They found that the DNA content of the B subgenome was significantly higher than those of the A and D subgenomes. In addition, DNA content of individual chromosomes varied from chromosome to chromosome in the studied lines. Lee et al. (1997) estimated the DNA content of individual chromosomes at the G1 stage using flow cytometry, by subtracting the readings of a monosomic line from those of euploid T. aestivum. The haploid 2C DNA content of individual wheat chromosomes at the G1 stage range from about 0.58 pg in single-chromosome 1D, to approximately 1.12 pg in single-chromosome 3A. The A subgenome (haploid 2C content = 6.15 pg) seems to contain more DNA than the B (haploid 2C = 6.09 pg) and D (haploid 2C = 5.05 pg) subgenomes. Analysis of variance showed significant differences (α = 0.01) in DNA content both among homoeologous groups and among genomes. Yet, their estimates of interphase wheat chromosomes DNA content in monosomic lines correlated poorly with the chromosome sizes at metaphase (r = 0.622, p ≤ 0.01).
10.4.2.8.7 Chromosome Arrangement in the Nucleus of T. aestivum
Arrangement of chromosomes in the eukaryotic nucleus and its impact on various aspects of chromosomal behavior and function, have been a focal point of interest in cytological research for over a century (for review see Avivi and Feldman 1980; Comings 1980; Hilliker and Appels 1989). Arrangement of chromosomes has two main elements: (i) arrangement of chromosomes with respect to nuclear polarity and to various nuclear components (e.g., Rabl orientation, attachment of centromeres to the spindle fibers, involvement of centromeres in the formation of the nuclear membrane, and attachment of centromeres and telomeres to the nuclear membrane), and (ii) arrangement of chromosomes with respect to one another (Comings 1968; Feldman and Avivi 1973a, b; Vogel and Schroeder 1974; Mosolov 1974; Horn and Waldman 1978; Avivi et al. 1982a, b). While there is consensus regarding the concept of polarized chromosomal arrangements in the interphase nucleus, there is still some controversy concerning the spatial relationships of chromosomes with respect to one another. This controversy stems from difficulties in performing direct observations of interphase chromosomal arrangements and from the fact that mitotic metaphase chromosomal distribution, i.e., arrangement of chromosomes on the metaphase plate by means of the spindle fibers, may be distinct from that of interphase. In most cases, therefore, interphase chromosomal arrangement is inferred from chromosomal positions at metaphase of physically or chemically treated cells. In such cells, the spindle system did not develop and, presumably, the chromosomes did not move much after the disintegration of the nuclear membrane; therefore, they are assumed to retain, more or less, their interphase location.
In diploid organisms the arrangement of chromosomes with respect to one another in the interphase nucleus comprises two kinds of spatial relationships: (a) those between homologous chromosomes, and (b) those between non-homologous chromosomes. In interspecific hybrids and in allopolyploids, spatial relationships also exist between homoeologous (partially homologous) chromosomes and non-homoeologous chromosomes of different subgenomes (Avivi and Feldman 1980).
Bread wheat, T. aestivum ssp. aestivum, is quite suitable for studies of such spatial relationships. First, as bread wheat is a hexaploid with three homoeologous subgenomes, A, B, and D, and six genetically related chromosomes in each of the seven homoeologous groups, it can be used to examine the relationships between chromosomes of the same or of different subgenomes. Second, the availability in bread wheat cv. Chinese Spring complete series of telocentric chromosomes (Sears 1954; Sears and Sears 1979), facilitates production of plants with different types of telocentric pairs, easily recognizable in mitosis and meiosis. Third, the deduction that chromosome arm 5BL affects spatial relationships between chromosomes (Feldman 1966c; Feldman and Avivi 1973b, 1984), allows studies of the genetic control and subcellular and molecular mechanisms involved in chromosomal arrangement.
When studying spatial relationships in hexaploid wheat, chromosomes can be grouped into telocentric pairs, whose members are either genetically related or unrelated. In allohexaploid wheat, related chromosomes can be either of the same subgenome (homologues) or of different subgenomes (homoeologues). Unrelated combinations of two chromosomes (non-homologues and non-homoeologues) can be divided into combinations whose members belong to the same subgenome and those whose members belong to different subgenomes.
The approximate two decades of study of chromosomal arrangement in the somatic and meiotic nucleus of bread wheat (Feldman et al. 1966; Feldman and Avivi 1973a, 1973b, 1984; Avivi et al. 1982a, b; Yacobi et al. 1985) have provided much information on spatial relationships between different types of chromosomes and on the genetic control of these relationships. These studies indicate that in root-tip and premeiotic cells and in first meiotic prophase and metaphase, chromosomes are distributed nonrandomly with respect to each other and occupy definite positions in the nucleus.
10.4.2.8.7.1 Spatial Relationships Between Chromosomes of the Different Subgenomes
Feldman and Avivi (1973b), Avivi et al. (1982b), measuring distances between different telocentric pairs in root-tip cells of bread wheat cv. Chinese Spring, found that the chromosomes of each of the three subgenomes are arranged at larger distances from each other than chromosomes of the same subgenome do. This might imply that each subgenome occupies a distinct region in the allohexaploid nucleus.
Spatial separation of parental genomes in somatic and meiotic metaphases of various plant hybrids has been reported by several researchers (Finch et al. 1981; Schwarzacher et al. 1989, 1992; Linde-Laursen and Jensen 1991). Others have made such observations in allopolyploid Milium montianum (Bennett and Bennett 1992) and allotetraploid cotton (Han et al. 2015). In allopolyploid plants, there appears to be subgenome separation of interphase chromosomes, with chromosomes of each subgenome tending to cluster together (Hilliker and Appels 1989). A similar genome separation phenomenon was found in synthesized tetraploid cotton (genome AAGG) (Han et al. 2015), indicating that genome separation established immediately after tetraploid cotton formation. Given the evidence of parental genome separation in other plants, Han et al. (2015) speculated that genome separation might be a normal phenomenon in diploid and allopolyploid species. Concia et al. (2020) analyzed the whole genome interaction matrix in allohexaploid wheat and revealed three hierarchical layers of chromosome interactions, from strongest to lowest: (i) within chromosomes, (ii) between chromosomes of the same subgenome, and (iii) between chromosomes of different subgenomes. This organization indicates a non-random spatial distribution of the three subgenomes that could mirror the presence of functional “subgenome territories.”
Concia et al. (2020) confirmed the presence of subgenome-specific territories using genomic in situ hybridization (GISH) in root meristematic cells. Similar to Avivi et al. (1982b), Concia et al. (2020) observed that the A and B subgenomes interact more frequently than do A and D or B and D. To determine whether other polyploid plants share the same large-scale nuclear organization, Concia et al. (2020) analyzed 14-day-old rapeseed seedlings (Brassica napus), and again revealed a three-layer hierarchy of chromosomal interactions identical to those in wheat, suggesting that this organization might be a general feature of allopolyploid plants.
Concia et al. (2020) showed, using two genome-wide complementary techniques, GISH and Hi-C, that the chromatin of hexaploid wheat is not uniformly distributed across the nucleus but, rather, occupies subgenome-specific nuclear compartments. This finding is consistent with previous cytological observations (Feldman and Avivi 1973b; Avivi et al. 1982a, 1982b), indicating that chromosomes of the same subgenome tend to be physically closer to each other than chromosomes of different subgenomes. Consequently, Concia et al. (2020) proposed that subgenome territories are the primary level of chromatin spatial organization in bread wheat. The establishment of subgenome territories may be a mechanism that favors the pairing of homologues versus homoeologues by creating territorial “boundaries” between the different subgenomes, i.e., either homoeologues or non-homologues (Concia et al. (2020).
Similar finding showing that the three subgenomes of bread wheat are located in three different territories in the interphase nucleus were presented by Li et al. (2000) and Jia et al. (2021). Using genomic in situ hybridization (GISH), Li et al. (2000) found that the three subgenomes of hexaploid wheat tend to localize to specific nuclear territories. Jia et al. (2021) investigated the mechanism affecting higher-order structure on both chromosome and subgenome levels in common wheat. Their data rsupports the existence of subgenome-specific territories and reveals the impact of the genetic sequence context on the higher-order chromatin structure and subgenome stability in hexaploid wheat.
10.4.2.8.7.2 Spatial Relationships Between Homologous and Homoeologous Chromosomes
In normal dosage, the long arm of chromosome 5B (5BL) of ssp. aestivum cv. Chinese Spring prevents pairing of homoeologues while allowing homologues to pair regularly at meiosis. In the absence of 5BL as in nullisomic 5B or in the ph1b mutant line, which is deficient for the Ph1 gene, the suppressor of homoeologous pairing on 5BL, some homoeologous pairing superimposed on the homologous pairs can be observed (Sears 1976b). Six doses of 5BL caused partial asynapsis of homologous chromosomes at meiosis, and at the same time, some pairing of homoeologous chromosomes and interlocking of bivalents (Feldman 1966c). To explain this paradoxical effect of six doses of 5BL, it was assumed (Feldman 1966c, 1968) that this chromosome arm carries a gene, most probably Ph1, that neither interferes with the pairing process itself nor with those of recombination, but, rather, disrupts a premeiotic event which is a prerequisite for regular meiotic pairing. It was hypothesized that six doses of 5BL alter the arrangement of homologues and homoeologues in the premeiotic nucleus of bread wheat. According to this assumption, in plants lacking 5BL, the homoeologues as well as homologues lie close to each other, resulting in some homoeologous pairing, which is superimposed on the homologous pairs, and also in few interlocking of two or, more rarely, three bivalents. Two doses of 5BL, as in disomic 5B or mono-isosomic 5BL, while scarcely affecting the homologous chromosomes, maintain the homoeologues apart, thus, leading to exclusive homologous pairing without interlocking of bivalents. Six doses of 5BL (as in tri-isosomic 5BL) fully suppress premeiotic arrangement, leading to a random distribution of chromosomes, in which the homologues may presumably be separated by a distance of as much as several microns. The meiotic attraction forces which usually cause pairing of very closely oriented homologues are not sufficient to bring about pairing of such distantly separated homologues, and, as a result, many homologous chromosomes fail to pair. Since homoeologous chromosomes may, by chance, lie close to each other, homoeologous pairing can take place. Although multivalent associations were rare at first metaphase of tri-isosomic 5BL, due to the general reduction of pairing, heteromorphic rod bivalents occur, presumably also the result of homoeologous pairing. Finally, the wide occurrence of interlocking bivalents, in spite of the reduction in the total number of bivalents, shows clearly that some of the pairing is between widely separated partners.
The gene on 5BL is not a specific suppressor of homoeologous pairing, since in extra doses, it also affects the pairing of homologous chromosomes (Feldman 1966c; Wang 1990). In disomic 5B plants, the normal two doses of the 5BL gene are presumably counteracted by the presence of the homoeoallelic pairing promoters on chromosomal arms 5AL and 5DL and, therefore, only homoeologous pairing is suppressed, whereas in tri-isosomic 5BL plants, the extra dose of this gene also suppresses homologous pairing. Indeed, it was found (Feldman, 1966c, 1968) that the long arms of 5A and 5D carry gene(s) that promote pairing. There are several other pairing genes that may also be involved in the control of premeiotic association between bread wheat chromosomes. These include weak suppressors on 3DS (Mello-Sampayo 1972), on 3AS (Driscoll 1973), on 2DL and possibly also on 2AL and 2BL (Ceoloni et al. 1986), and promoters on the short arms of chromosomes of group 5 (Feldman 1966c; Feldman and Mello-Sampayo 1967; Riley et al. 1966; Dvorak 1976), on the long arms of chromosomes of group 3 (Driscoll 1973), and on the short arms of chromosomes of group 2 (Ceoloni et al. 1986). Hence, the control of pairing in bread wheat stems from a balance between several suppressors and promoters.
Further evidence indicating that extra doses of 5BL interfere with premeiotic chromosomal arrangement came from their effect on pairing of isochromosomes in plants bearing tri-isosomic 5BL. Such bread wheat plants carry three isochromosomes 5BL, each with two homologous 5BL arms, which may undergo inter-chromosomal pairing between 5BL arms of different isochromosomes or intra-chromosomal pairing involving arms of the same isochromosome. While six doses of 5BL reduced the inter-chromosomal pairing between the three 5BL isochromosomes down to a frequency similar to that of conventional homologous chromosomes (to about 50% of the normal pairing), the degree of intra-chromosomal pairing of these isochromosomes was not affected at all. Hence, when the homologous arms are connected by a common centromere and cannot be spatially separated, their pairing is not suppressed by six doses of 5BL.
The effect of Ph1 on intra- and inter-chromosomal pairing was compared to the effect of the Syn-B1 gene (Vega and Feldman 1998) located on the long arm of chromosome 3B (3BL), whose activity is responsible for normal synapsis and chiasma formation (Sears 1954; Kempanna and Riley 1962; Kato and Yamagata 1982, 1983). In contrast to the effect of Ph1, intra-chromosome pairing was strongly reduced in the absence of the synaptic gene Syn-B1 (Vega and Feldman 1998).
Absence of 5BL also induces bivalent interlocking, but to a lesser extent than six doses. However, in zero dose of 5BL, interlocking configurations are composed of only two or three bivalents, as predicted for interlocking involving only homoeologous bivalents. In the presence of two doses of 5BL, no interlocking bivalents are formed. On the other hand, in plants with four and six doses of 5BL, more than three bivalents (up to seven) form interlocking configurations, indicating that in extra dose of 5BL, non-homologous bivalents, presumably from the same subgenome, may interlock with each other (Yacobi et al. 1982; Yacobi and Feldman 1983). Chromosomal arm 5BS affects interlocking in an opposite manner than 5BL; namely, two and four doses of 5BS markedly reduce interlocking frequency (Yacobi et al. 1982).
Although this arrangement of close association of homologues and distant positioning of homoeologues could conceivably be limited to the stage immediately preceding meiosis, a number of investigators (e.g., Kitani 1963) have maintained that homologues are associated throughout the life of the plant. The study of Feldman et al. (1966), Feldman and Avivi (1973a, b, 1984), Avivi et al. (1982a, b) was carried out to see whether chromosomes in bread wheat are arranged non-randomly also in root-tip cells.
For the study chromosomal arrangement in root tip cells of bread wheat, telocentric chromosome pairs of homologues, homoeologues, or of non-homologues of the same subgenome, and non-homoeologues of different subgenomes, were used as marked pairs. The telocentric chromosomes are easily distinguished from the normal two-arm chromosomes of bread wheat. Measures of distances between different types of telocentric pairs, showed that in root tip cells of bread wheat, chromosomes are distributed non-randomly with respect to one another (Feldman et al. 1966; Feldman and Avivi 1973a, b, 1984; Avivi et al. 1982a, b). Within each of the three subgenomes composing the bread wheat nucleus, homologous chromosomes exhibited a so-called somatic association, being located closer to each other than any other pair of non-homologues (Feldman et al. 1966). Approximately equal degrees of association were observed between the two telocentrics for opposite arms of the same chromosome and between homologous telocentrics, suggesting that the centromere is at least partly responsible for somatic association (Feldman et al. 1966; Mello-Sampayo 1968, 1973). On the other hand, chromosomes of the different subgenomes, either homoeologues or non-homoeologues, were spatially separated, indicating that each subgenome occupies a different territory in the interphase nucleus (Feldman and Avivi 1973b; Avivi et al 1982b). Similarly, Yacobi et al. (1985) determined distances between marked pairs of bivalents at first meiotic metaphase of bread wheat by tallying the number of bivalents intervening between two marked bivalents. Within each subgenome, the association of telocentric bivalents representing the two different arms of one chromosome was much more intimate than that of genetically unrelated bivalents. The data from meiotic cells indicate that a similar pattern of chromosomal arrangement exists in both meiotic and somatic cells. Moreover, the arrangement of chromosomes in cold-treated cells, in which mitotic spindle formation is inhibited, is maintained on the functioning spindle at meiotic metaphase.
The close association between homologous chromosomes in root-tip cells of bread wheat aligns well with data of Schulz-Schaeffer and Haun (1961), Singh and Joshi (1972), Singh et al. (1976) obtained in hexaploid wheat. Specific chromosome order within a set was found in a large number of plant species (reviewed in Avivi and Feldman 1980). On the other hand, Darvey and Driscoll (1972), Dvorak and Knott (1973) found no evidence that homologous chromosomes are closer to one another than are non-homologues in root tip cells of bread wheat. As Avivi et al. (1982a) demonstrated, experimental errors could account for this failure to detect somatic association.
Studies of C-banded first meiotic metaphase in plants with four doses of 5BL have shown that most of the unpaired chromosomes, as well as the interlocked bivalents, belong to the B subgenome (Lukaszewski and Feldman, unpublished). Likewise, evidence exists for a greater effect of the Phl gene, which is located on 5BL (Okamoto 1957a), on the pairing of B-subgenome chromosomes than on the A- and D-subgenome chromosomes in wheat-rye hybrids (Naranjo et al. 1987). This finding supports the notion that the hexaploid wheat nucleus still maintains some individual ancestral genomic organization, which, in turn, is recognized by Phl.
10.4.2.9 Crosses with Other Species of the Wheat Group
A large number of T. aestivum accessions exhibit one, or, more rarely, two, reciprocal translocations, some of which are of different types (Badaeva et al. 2007, and reference therein). Some of these translocations may have occurred at the tetraploid level, while most translocations and obviously, those involving chromosomes of the D subgenome, occurred after the formation of the allohexaploid. The B-subgenome chromosomes are most frequently involved in translocations, followed by the A- and D-subgenome chromosomes (Badaeva et al. 2007). Individual chromosomes also differ in the frequencies of translocations. Several types of pericentric inversions, and paracentric inversions have also been detected in different accessions (Badaeva et al. 2007). The occurrence of such rearrangements and presumably also some cryptic structural hybridity, undetectable by cytological studies, may have led to some pairing failure at meiosis. In fact, the frequency of meiotic cells with univalents was 4.0–4.4% in pure strains of several subspecies of T. aestivum, namely, ssp. aestivum, ssp. compactum, and ssp. spelta (Thompson and Robertson 1930), and some inter-varietal hybrids of ssp. aestivum had two or more univalents in few cells and rare trivalents and quadrivalents (Hollingshead 1932).
Most F1 hybrids between the various subspecies of T. aestivum displayed complete or almost complete chromosomal pairing at first meiotic metaphase, indicating full homology between their genomes. Yet, the F1 hybrids between ssp. spelta and ssp. macha showed some pairing failure at first meiotic metaphase (bivalents exhibited reduced chiasmata) and a bridge + an acentric fragment, frequently formed at first anaphase, indicating the occurrence of a paracentric inversion (Chin and Chwang 1944). At meiosis of ssp. aestivum x ssp. macha, a multivalent (either a quadrivalent or a trivalent plus univalent) was observed in many meiocytes (Chin and Chwang 1944).
Chapman et al. (1976), Dvorak (1976) presented evidence implying that the A subgenome of ssp. aestivum derived from the genome of T. urartu. Chapman et al. (1976) compared the pairing behavior of the ssp. aestivum x T. urartu hybrids with earlier results obtained from hybrids between ssp. aestivum and T. monococcum ssp. aegilopoides var. boeoticum (Chapman and Riley 1966) and concluded that pairing affinities of the chromosomes of T. urartu or T. monococcum ssp. boeoticum with the chromosomes of ssp. aestivum are essentially similar but the lhybrid ssp. aestivum x T. monococcum exhibited a higher frequency of trivalents (Chapman et al. 1976). Dvorak (1976) while investigating the relationships between the A and B subgenomes of ssp. aestivum and the genome of T. urartu, reported that the F1 hybrids showed relatively high chromosome pairing with an average of 5.4 bivalents, and 0.05 trivalents per cell. The low frequency of trivalents suggests that the majority of ssp. aestivum A subgenome chromosomes do not differ structurally from the chromosomess of T. urartu. Dhaliwal (1977c) observed in the F1 hybrid between ssp. aestivum, and diploid wheat, T. urartu 5.94 bivalents (of which 1.58 were rod and 4.36 ring). This high level of pairing, in the presence of the Ph1 gene of hexaploid wheat, indicates great, but not complete homology, between the A subgenome of ssp. aestivum and the genome of T. urartu.
Chapman et al. 1976) analyzed fourteen distinct F1 hybrids between di-telocentric lines of A and B subgenomes of ssp. aestivum cv. Chinese Spring and the wild diploid wheat T. monococcum ssp. aegilopoides var. thaoudar, and observed 3.06–5.30 (range from 1 to 7) bivalents and 0.02–0.34 (range from 0 to 2) trivalents. The trivalents occurring in these hybrids represent interchanges mainly between A subgenome chromosomes of ssp. aestivum and the A chromosomes of var. thaoudar. The meiotic pairing behavior at first meiotic metaphase of the hybrid ssp. aestivum cv. Courtot × T. monococcum ssp. monococcum has been studied by means of the C-banding technique, to ascertain the homology between the chromosomes in the A subgenome of the hexaploid and those in the genome of the diploid (González et al. 1993). The technique allowed the A and B subgenome chromosomes and the 2D, 3D and 5D chromosomes to be identified. Average chromosomal pairing was 3.99 (1–7) bivalents (of which 3.11 (1–6) were rod and 1.05 (0–3) ring), and 0.14 (0–2) trivalents. A similarly low level of pairing in this hybrid combination was reported by Miller and Reader (1980), while Melburn and Thompson (1927) found higher pairing (average of 5.0 bivalents). The T. monococcum 4A chromosome did not pair with any of the ssp. aestivum chromosomes. Two reciprocal translocations 2B/2D and 2A/3D have been identified in ssp. aestivum cv. Courtot. Evidently, these translocations occurred at the hexaploid level.
Data of chromosome pairing in F1 hybrids between ssp. aestivum diploid specie of Aegilops are presented in Table 9.10. The hybrids ssp. aestivum and Ae. speltoides show different results depending on the genotype of the latter. Kimber and Athwal (1972) produced F1 hybrids between ssp. aestivum cv. Chinese Spring and a high-intermediate- and low-pairing types of Ae. speltoides. At first meiotic metaphase of these hybrids, they observed much higher pairing when the high-pairing type was used than when the intermediate pairing type was used, and much reduced pairing when the low-pairing type was used (Table 9.10). These results show that none of the subgenomes of ssp. aestivum are homologous to the genome of Ae. speltoides (Kimber and Athwal 1972).
Hybrids between ssp. aestivum and the other species of Aegilops section Sitopsis, namely, Ae. sharonensis, Ae, bicornis, Ae. longissima, and Ae. searsii, had very little pairing (observed average pairing was 1.50–1.78 bivalents, and 0.02- 0.08 trivalents; Table 9.10), showing that either very little homology exists between the chromosomes of these species or that these diploids contain a Ph-like gene that suppresses pairing of homoeologous chromosomes (Feldman 1978). On the other hand, a hybrid between ssp. aestivum and an intermediate pairing type of Ae. longissima showed more pairing than the hybrids with standard lines of Ae. longissima (Feldman 1978).
The meiotic behavior of ssp. aestivum x Ae. speltoides, ssp. aestivum x Ae. sharonensis and ssp. aestivum x Ae. longissima has been analyzed by the C-banding technique (Fernández-Calvín and Orellana 1994). These authors reported that in all the hybrids analyzed the mean number of bound arms per cell for the A-D type was significantly higher than the mean number of associations between the B subgenome and the S/Ssh/Sl genomes of the aegilops species. Usually, the relative contribution of each type of pairing is maintained among hybrids with different Aegilops species. These results indicate that the genomes of Ae. speltoides, Ae. sharonensis and Ae. longissima show a similar affinity with the genomes of hexaploid wheat; therefore, none of these species can be considered to be a distinct donor of the B subgenome of hexaploid wheat.
Using the C-banding technique, Maestra and Naranjo (1998) studied homoeologous pairing at first meiotic metaphase in the Ph1, ph1b, and ph2b hybrids of ssp. aestivum and a high-pairing type of Ae. speltoides. All arms of the seven chromosomes of the speltoides genome showed normal homoeologous pairing, which implies that no apparent chromosome rearrangements occurred in the evolution of Ae. speltoides relative to that of bread wheat. A pattern of preferential A-D and B-S pairing confirmed that the S genome is closely related to the B subgenome of wheat. Although this pairing pattern was also reported in hybrids of wheat with Ae. longissima and Ae. sharonensis (Fernández-Calvín and Orellana 1994), somewhat more intimate pairing was observed between some chromosomes of the B subgenome and those of Ae. speltoides. These results are in agreement with the hypothesis that the B subgenome of wheat is derived from a species closely related to Ae. speltoides. Chromosomal pairing in the F1 hybrid ssp. aestivum x Ae. tauschii (genome BADD) and in the reciprocal hybrid, was studied by (Kimber and Riley 1963; Table 9.10). This high level of pairing observed in these hybrids shows clearly that ssp. aestivum possess one subgenome (D) homologous to the genome of Ae. tauschii. Hybrids between ssp. aestivum and other diploid species of Aegilops, namely, caudata, comosa, and umbellulata, had little pairing (Table 9.10) Hence, the genomes of these diploid species have no homology to any of the three subgenomes of hexaploid wheat.
Crosses between ssp. aestivum x and tetraploid wheat, T. turgidum ssp. durum (Table 10.8), produced a pentaploid F1 hybrid (genome BADBA) that had at meiosis, close to 14 bivalents that resulted from pairing between the A and B subgenomes of ssp. aestivum each with its homologous subgenome of ssp. durum (Table 10.8). Likewise, the F1 hybrid ssp. macha x ssp. durum had 12.0 bivalents, and a quadrivalent (Kihara 1949). This high level of pairing corroborates the conclusion of Kihara (1924), who showed that two subgenomes of hexaploid wheat (B and A) are fully homologous with the two subgenomes of T. turgidum. On the other hand, the pentaploid F1 hybrid between ssp. aestivum and T. timopheevii ssp. armeniacum (hybrid genome BADGA) had had reduced pairing (Table 10.8), showing that the G and B subgenomes of these two taxa are homoeologous rather than homologous.
Chromosomal pairing in F1 hybrids between ssp. aestivum and the second hexaploid wheat species, T. zhukovskyi (hybrid genome BADGAAm) (Table 10.8) implied that while the A subgenomes of these species are homologous, the Am subgenome is very closely related A, and B, G, and D subgenomes are homoeologous.
Data on meiotic chromosome pairing between ssp. aestivum and allotetraploid Aegilops species are presented in Table 10.10. The pentaploid hybrid between ssp. aestivum and Ae. ventricosa (genome BADDN) had 5.02 bivalents (of which 2.94 were rod, and 2.08 ring), and 0.13 trivalents and the reciprocal hybrid had 3.35 rod, 0.92 ring and 4.27 total bivalents, and 0.19 trivalents (Kimber and Zhao 1983). This level of chromosomal pairing shows that the D subgenome of hexaploid wheat is homoeologous rather than homologous to the D subgenome of Ae. ventricosa. The pentaploid hybrid ssp. aestivum x Ae. cylindrica (hybrid genome BADDC) had 6.74 bivalents, 0.18 trivalents, and 0.02 quadrivalents (Riley 1966), 2.16 rod, 4.66 ring and 6.82 total bivalents and 0.08 trivalents (Kimber and Zhao 1983). Evidently, and as was shown previously by Sears (1944b), the D subgenome of Ae. cylindrica is homologous to the D subgenome of hexaploid wheat. In contrast, the pentaploid F1 hybrids between ssp. aestivum and Ae. peregrina (hybrid genome BADSvU), Ae geniculata (hybrid genome BADMoU) and Ae. triuncialis (hybrid genome BADUC) had much reduced pairing (Table 10.6). The reduced pairing in these hybrids implies that the subgenomes of these allotetraploid species are only distantly homoeologous to those of hexaploid wheat.
Chromosome pairing was studied in in F1 hexaploid hybrids between ssp. aestivum and allohexaploid species of Aegilops, Ae. juvenalis (genome hybrid BADDcXcU), Ae. vavilovii (hybrid genome BADDcXcSs), and hexaploid Ae. crassa (hybrid genome BADDcXcD) (Table 10.6). Ssp. aestivum x Ae. juvenalis and ssp. aestivum x Ae vavilovii had a number of paired chromosomes between the D subgenome of hexaploid wheat and the D subgenomes of these Aegilops allohexaploids showing that they are homoeologous rather than homologous. Presumably, the D subgenomes of Aegilops underwent some changes on the polyploid level and became modified subgenomes. On the other hand, the hybrid 6x Ae. crassa x ssp. aestivum had a higher pairing indicating homology between the D subgenome of ssp. aestivum and the unmodified subgenome D of Ae. crassa.
10.4.3 T. zhukovskyi Menabde & Ericz. (Genome GGAAAmAm)
10.4.3.1 Description of Species
Triticum zhukovskyi, known as zhukovsky’s wheat, [Syn.: T. timococcum Kostov.; T. timopheevii ssp. zhukovskyi (Men. et Ericz.) L. B. Cai: T. timopheevii var. zhukovskyi (Men. et Ericz.) Morris et Sears; T. turgidum var. zhukovskyi (Men. & Er.) Bowden; Gigachilon zhukovskyi (Menabde & Erizin) Á. Löve] is an annual, predominantly autogamous, 90–130-cm-tall (excluding spikes), pubescent plant. Culms are erect and hollow throughout. The spike is indeterminate, strongly bilaterally compressed, two-rowed, 9–14-cm-long (excluding awns), ovoid or lanceolate, tapered towards the base and tip, hairy and awned. The rachis is semi-fragile and subsequently, the spike either remains intact on the culm or, during threshing, easily disarticulates at maturity into single spikelets with the rachis segment below it. The rachis internodes are covered with dense, white hairs and the spikelets are compressed and ovoid or lanceolate, with the top spikelet being fertile and generally in the same plane as those below. There are 10–15 spikelets per spike, and the 2–3 basal spikelets are rudimentary. The fertile spikelet is 10–12-mm-long and has 3 florets, the upper one usually being sterile. The glumes are similar to one another, 9–12-mm-long, very hairy, with 2 keels and 5–9 veins, and with two teeth on the upper margin, one larger and pointed and separated from the other by an acute angle. Lemma are elliptic, hairy, 9–12-mm-long, without keels, with 9–11 veins, and with a central vein, prolonged as a narrow 60–100-mm-long white or black awn. In addition to the awn, the lemma has a lateral tooth. At maturity, the palea is membranous and split along the keel. Usually, there are two grains per spikelet. The caryopsis is free but laterally compressed (hulled), hairy at the apex, long and red in color.
T. zhukovskyi was discovered recently, in 1957, in Western Georgia, by Menabde and Ericzjan (Jakubziner 1959). It only exists as a domesticated form and has never been cultivated alone. Zhukovsky’s wheat is continually found in cultivated fields in West Georgia, containing, in addition to T. zhukovskyi, a mixture of diploid T. monococcum var. hornemanni and tetraploid T. timopheevii, a mixture called the Zanduri wheat (Jakubziner 1959; Dorofeev 1966). T. zhukovskyi has been a minor component of the endemic Zanduri wheat complex and is currently grown in extremely limited amounts in Western Georgia. The three components of the Zanduri complex are genetically effectively isolated by different ploidy levels (Mac Key 1966). T. zhukovskyi constitutes a minor part of the Zanduri complex which currently, is mainly consumed as porridge (Mac Key 1975).
T. zhukovskyi resembles T. timopheevii in its ear morphology and growth characteristics, but its spike is somewhat larger than that of T. timopheevii (Jakubziner 1959). Likewise, Upadhya and Swaminathan (1963b) pointed out that T. zhukovskyi resembles T. timopheevii in most plant characters and particularly in their hairs, which, in both species, are long, thin and unicellular. However, it has enlarged cells as compared to T. timopheevii. T. zhukovskyi and T. timopheevii have similar disease immunity (Jakubziner 1959) and seedlings of T. zhukovskyi are highly resistant to manty races of leaf rust and stem rust (Upadhya and Swaminathan 1963b). When sown in the fall, its development lags several days behind T. timopheevii. T. zhukovskyi has a spring habit and exhibits very limited variation.
10.4.3.2 Cytology, Cytogenetics and Evolution
Its morphology and its constant association with T. timopheevii and T. monococcum suggest that T. zhukovskyi is a hexaploid species (2n = 6x = 42) that derived from a spontaneous hybridization between a domesticated subspecies of tetraploid T. timopheevii and a domesticated subspecies of diploid T. monococcum (presumably var. hornemanni which is a component of the Zanduri complex). Menabde and Ericzjan noted that the crossing between T. timopheevii and T. zhukovskyi occurs readily, but the F1 hybrid displays low fertility. If T. zhukovskyi originated from hybridization of the other two components of the Zanduri mixture, then, it is obviously of a more recent origin than its two domesticated parents.
Bowden (1959) was the first to suggest that T. zhukovskyi originated as a Allohexaploid from the cross of T. timopheevii and consequently, designated its genome AAAAGG i, implying the sum of the genomes of T. timopheevii (genome GGAA) and of T. monococcum (AmAm), the other two components of the Zanduri mixture. The idea that T. zhukovskyi is a natural polyploid derived from hybridization of T. timopheevii and T. monococcum was confirmed cytogenetically by Upadhya and Swaminathan (1963a, b). Upadhya and Swaminathan (1963) pointed out that T. zhukovskyi is the firbst hexaploid wheat to have a genomic constitution other than AABBDD. Thus, the allopolyploid species of the genus Triticum constitute two evolutionary lineages; the BBAA and BBAADD comprise one lineage and GGAA and GGAAAmAm the second lineage.
Kimber and Sears (1983, 1987), following Bowden (1959), designated the genome of T. zhukovskyi AAAAGG, assuming that the genomes of T. urartu and T. monococcum are very closely related. However, Dvorak et al. (1993), studying variation in 16 repeated nucleotide sequences, showed that T. zhukovskyi contains one A subgenome, that was contributed by T. urartu, and another related subgenome, contributed by T. monococcum, thereby verifying that T. zhukovskyi originated from hybridization of T. timopheevii with T. monococcum. Dvorak et al. (1993), in view of the differences in the profiles of repeated nucleotide sequences and the reproductive isolation by hybrid sterility between T. urartu and T. monococcum (Johnson and Dhaliwal 1976), considered their genomes modified relative to each other. Consequently, they proposed to designate the genome of T. urartu AA and that of T. monococcum AmAm. Thus, the genome formula of T. zhukovskyi is AAAmAmGG (Dvorak et al. 1993). Since the female parent in the formation of T. zhukovskyi was T. timopheevii, its genome should be designated GGAAAmAm. In addition, the repeated nucleotide sequence profiles in the A and Am subgenomes of T. zhukovskyi showed reduced correspondence with those in the genomes of both ancestral species, T. urartu and T. monococcum. According to Dvorak et al. (1993), this differentiation is attributed to heterogenetic chromosome pairing and segregation among chromosomes of the two A genomes in T. zhukovskyi. This agrees with the formation of some multivalents at meiosis of T. zhukovskyi, indicating that T. zhukovskyi has four A related subgenomes (Upadhya and Swaminathan 1963b).
The karyotypes of T. zhukovskyi, T. timopheevii ssp. timopheevii and T. monococcum ssp. monococcum var. hornemanni, were studied by Upadhya and Swaminathan (1963b). They found that all the chromosomes of T. zhukovskyi possess median or sub-median centromeres. The species contains three pairs of satellited chromosomes, two of which bear large satellites and one with small satellites. The two chromosome pairs with the large satellites resemble the two pairs present in T. timopheevii, whereas the other pair is similar in arm ratio to the pair found in T. monococcum var. hornemanni.
Electrophoretic seed protein patterns confirmed the origin of T. zhukovskyi as a product of hybridization between T. timopheevii and T. monococcum (Johnson 1968). The electrophoretic pattern of T. zhukovskyi proteins is similar to the pattern of T. timopheevii, specifically to that of ssp. timopheevii, but also contains bands of domesticated T. monococcum. Immunoelectrophoretic findings (Aniol 1973) also supported the conclusion that T. zhukovskyi originated from chromosome doubling of a hybrid between T. timopheevii and T. monococcum. Using a set of molecular cytogenetic landmarks, based on eleven DNA probes, that identified the chromosomes of T. timopheevii, Badaeva et al. (2016) demonstrated the existence of the timopheevii genome in T. zhukovskyi. This further corroborated the conclusion of Upadhya and Swaminathan (1963b) and others, that the latter contains the genome of the former, and presumably resulted from hybridization of T. timopheevii with T. monococcum. However, Badaeva et al. (2016) observed that the formation of T. zhukovskyi was accompanied by structural changes involving mostly A subgenome chromosomes, presumably, due to inter-subgenomic chromosomal pairing between the two closely related A- and Am subgenomes in T. zhukovskyi.
Sallares and Brown (1999), using the sequence of the intergenic spacer regions of the NOR loci in diploid and polyploid species of wheat, showed that while T. timopheevii contains the spacer originating from T. urartu, T. zhukovskyi contains the spacer of both T. urartu and T. monococcum. This observation confirmed that one of the A subgenomes of T. zhukovskyi originated from T. urartu and the other from T. monococcum. On the other hand, Adonina et al. (2015), using the pTm30 probe cloned from Triticum monococcum genome and containing (GAA)56 microsatellite sequence, found that (GAA)n sites observed in T. monococcum are undetectable in the Am genome of T. zhukovskyi. They concluded that this site may have been eliminated during the process of allopolyploidization.
Using T. timopheevi as female and T. monococcum as male, synthetic amphiploids (genome GGAAAmAm) were produced, by several teams (Kostoff (1937b), Bell et al. (1955), Watanabe et al. 1956; Dhaliwal and Johnson 1976; Upadhya and Swaminathan 1963b; Cao et al. 2000a) and, in all cases, the morphological characteristics of the amphiploid closely resembled that of T. zhukovskyi. This further supports the conclusion that this species originated from a natural cross between T. timopheevii and T. monococcum, followed by chromosome doubling. However, the amphiploid is reported to be partially sterile.
Thus, the 14 timopheevii pairs (genome GGAA) plus the 7 pairs of T. monococcum (genome AmAm), constitute the 21 pairs of hexaploid T. zhukovskyi. The cytoplasm of T. timopheevii and of T. zhukovskyi derived from the donor of the G genome (Ogihara and Tsunewaki 1988; Wang et al. 1997; Gornicki et al. 2014), implying that T. timopheevii was the female parent. T. zhukovskyi is an auto-allo-hexaploid (genome GGAAAmAm), carrying two closely related subgenomes, A and Am. Consequently, a maximum of 4 multivalents per cell was found at meiosis in T. zhukovskyi, the average being 1.35 per cell (Upadhya and Swaminathan 1963b). Wang et al. (1997) reported that while the average genetic distance between the A genome of emmer wheat and that of hexaploid wheat was 0.016, the average distance between T. timopheevii and T. zhukovskyi was only 0.004, suggesting that T. zhukovskyi arose quite recently.
Eilam et al. (2008) found the 1C DNA content of one line of T. zhukovskyi to be 17.74 pg. The 1C DNA content of T. zhukovskyi is less than 18.35 pg, the expected additive amount of 1C DNA of its two-parental species, namely 11.87 pg of domesticated T. timopheevii, and 6.48 pg of domesticated T. monococcum, (Eilam et al. 2007). Interestingly, Upadhya and Swaminathan (1963b) found that total chromatin length in µ in T. zhukovskyi is 461.52 ± 12.68 (smaller than the expected additive amount of its two parents: T. timopheevii 329.47 and T. monococcum var. hornemanni 146.23, together 475.70).
On the basis of chromosome pairing in 41- and 42-chromosome hybrids between ssp. aestivum cv. Chinese Spring monosomic for chromosome 5B and T. zhukovskyi, Upadhya and Swaminathan (1965) suggested that T. zhukovskyi does not contain the Ph1 gene, that suppresses pairing of homoeologous chromosomes. Since T. zhukovskyi arose from the cross of T. timopheevii and T. monococcum, they assumed that T. timopheevii also lacks Ph1. Joshi et al. (1970) presented pairing data indicating that the potency of Ph1 in T. timopheevii is somewhat weaker than in ssp. aestivum. On the other hand, Feldman (1966a), Sallee and Kimber (1976) presented evidence implying that T. timopheevii contains a ph1 as effective as that of ssp. aestivum. Thus, different cultivars of T. timopheevii may contain Ph1 with different potencies, as was found by Ozkan and Feldman (2001).
10.4.3.3 Crosses with Other Species of the Wheat Group
Few hybrids were produced involving T. zhukovskyi and other species of the wheat group. Actually, only two such hybrids were reported. The F1 hybrid T. zhukovskyi and T. aestivum ssp. spelta, had an average of 15.12 univalents, 10.70 bivalents, 1.39 trivalents and 0.33 quadrivalents per cell (Upadhya and Swaminathan 1963b). The F1 hybrid T. zhukovskyi and T. aestivum ssp. aestivum had an average frequency of 12.27 univalents, 9.00 bivalents of which 5.53 were rod and 3.47 ring, 3.13 trivalents, 0.49 quadrivalents, 0.07 pentavalents, and 0.07 hexavalents (Shands and Kimber 1973). The partial failure of chromosome pairing in these two hybrids is similar to that usually found in hybrids between the G subgenome of T. timopheevi and the B subgenome of T. turgidum and T. aestivum o (Upadhya and Swaminathan 1963b). The multivalents, mainly trivalents and quadrivalents, are presumably the result of pairing between chromosomes of the A subgenome of the two specie and and Am subgenome of T. zhukovskyi.
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Feldman, M., Levy, A.A. (2023). Triticum L.. In: Wheat Evolution and Domestication. Springer, Cham. https://doi.org/10.1007/978-3-031-30175-9_10
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