Abstract
The taxonomy of the three species of the genus Secale is discussed followed by a description of their morphology, and account of their distribution, cytogenetics, and evolutionary aspects. The relationships of these species to one another and to other Triticineae, as well as processes that have led to the domestication of Secale cereale, are reviewed too.
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6.1 The Genus Secale—Taxonomic Survey
Secale L. is a small genus including one perennial and two annual species (Frederiksen and Petersen 1998; Table 6.1). The species are characterized by two hermaphroditic florets in each spikelet. Species with more florets in each spikelet, that were previously included in Secale, were later separated as Eremopyrum (Ledeb.) Jaub. and Spach (Frederiksen 1991a) or Dasypyrum (Coss. and Durieu) T. Durand (Frederiksen 1991b). The taxonomy of Secale has been complicated by the presence of many weedy, annual intermediates between the wild and the domesticated species, as well as by many wild perennial races. Roshevitz (1947) described 14 species in Secale, in addition to over 20 intra-specific taxa. He categorized several of the annual, weedy intermediates as separate species, namely, S. ancestrale (Zhuk.) Zhuk., S. dighoricum (Vav.) Roshev., S. segetale (Zhuk.) Roshev., S. afghanicum (Vav.) Roshev. and S. vavilovii Grossh. The similar cytology between these weedy taxa and its resemblance to that of domesticated Secale, with whom the weeds are inter-fertile, led Sencer (1975), Kobyljanskij (1983), Hammer et al. (1987), Evans (1995) and Frederiksen and Petersen (1998) to consider them subspecies of S. cereale, rather than independent species. This group of weeds is virtually confined to agricultural lands, currently widespread as cereal crops in northeastern Iran, Afghanistan and Transcaspian (Zohary 1971). In addition, there is a group of wild perennial races that are widely distributed from Morocco eastwards through the Mediterranean countries and the plateau region of central and eastern Turkey to northern Iraq and Iran. Roshevitz (1947) separated these races into several distinct species, e.g., S. ciliatoglume (Boiss.) Grossh., S. dalmaticum Vis., S. kuprijanovii Grossh., S. anatolicum Boiss, S. daralagesi Tum., and S. montanum Guss. Members of this group are morphologically highly similar, show high cytogenetic affinity to each other and are highly inter-fertile. They differ from the S. cereale complex by two major reciprocal translocations involving three pairs of chromosomes (Riley 1955). These races are most probably best described as subspecies of S. strictum (Sencer 1975; Kobyljanskij 1983; Hammer et al. 1987; Evans 1995; Frederiksen and Petersen 1998). Consequently, the number of Secale species was reduced, e.g., Schiemann (1948) recognized five species, Kobyljanskij (1983), and Hammer et al. (1987) recognized four species and Sencer (1975), Sencer and Hawkes (1980) and Frederiksen and Petersen (1997, 1998) recognized only three species in this genus, namely, S. strictum (C. Persl.) C. Presl. (Formerly S. montanum Guss.), S. sylvestre Host, and S. cereale L. (Table 6.1). Secale strictum includes all the wild perennial taxa that show high morphological resemblance and cytogenetic affinity to each other. S. sylvestre is a wild, annual species which is isolated geographically, ecologically, and reproductively from S. strictum, although the two-show cytogenetic affinity under experimental conditions. Rye, S. cereale, contains the annual wild, weedy and domesticated types (Sencer 1975; Sencer and Hawkes 1980; Frederiksen and Petersen 1998).
The general taxonomic relationships between the Secale species, determined based on morphological and cytological studies, were supported by studies of thin-layer chromatographic patterns of 41 fluorescent compounds in young leaves of 11 Secale taxa (Dedio et al. 1969). They showed that domesticated rye grouped together with weedy ryes, the perennial wild Secale taxa grouped together with each other, S. sylvestre had a distinct chromatogram of its own and S. vavilovii (currently included in S. cereale) was distinguished by the presence of four compounds not present in any other taxa. Sencer (1975), studying thin-layer chromatographic patterns of phenolic compounds in mature leaves of nine Secale taxa, also supported the general taxonomic relationships of the species by demonstrating high resemblance between S. cereale and S. afghanicum (currently included in S. cereale) and between S. anatolicum and S. vavilovii (both are currently included in S. cereale).
Frederiksen and Petersen (1998) performed a critical taxonomic review of the genus Secale, studying specimens primarily obtained from natural habitats. They claimed priority of the taxonomical name Secale strictum (C. Presl) C. Presl over S. montanum Guss. They also divided this species into two subspecies, subsp. strictum and ssp. africanum (Stapf) Hammer, that are separated geographically. Secale cereale was also treated as having two subspecies; the domesticated taxa, marked by their tough rachises, were placed in subsp. cereale and the wild or weedy taxa, that have either tough or varying degrees of fragile rachis, were placed in subsp. ancestrale Zhuk. (Table 6.1). S. sylvestre, although morphologically distinct from the wild, perennial, cross-pollinating S. strictum, has a similar karyotype to that of S. strictum (Sencer and Hawkes 1980; Evans 1995). Although it is geographically, ecologically and reproductively isolated from S. strictum, the two-show cytogenetic affinity under experimental conditions (Sencer and Hawkes 1980). The classification of the genus Secale suggested by Frederiksen and Petersen (1998) is currently accepted by many taxonomists and is used in this book.
Roshevitz (1947) recognized S. vavilovii Grossh. as a valid species. S. vavilovii is an annual, self-pollinating taxon, with short culms, of limited geographical distribution; it grows in eastern Turkey and northern Iran. Its chromosome arrangement is identical to that of S. cereale and therefore, different from S. strictum and S. sylvestre by two reciprocal translocations involving three pairs of chromosomes (Stutz 1972). Although several studies recognized S. vavilovii as a valid species (e.g., Khush and Stebbins 1961; Kranz1961; Khush 1962, 1963a, b; Singh and Robbelen 1975, 1977; Vences et al. 1987; Hammer et al. 1987), Kobyljanskij (1983) included it as a subspecies in S. cereale. Similarly, following morphological analyses of many characteristics, Sencer (1975) and Frederiksen and Petersen (1998) also included it in S. cereale. It differs from S. cereale by its autogamous habit, but self-fertile strains are also known within both weedy and domesticated S. cereale (Jain 1960; Pérez de la Vega and Allard 1984; Voylokov et al. 1993; Meier et al. 1996).
Secale iranicum Kobyl. was described by Kobyljanskij (1975, 1983), based on material collected by H. Kuckuck in Hamadan, Iran. S. iranicum was initially identified by Kranz (1957) as S. vavilovii and, like S. vavilovii, it is a self-pollinating taxon. Morphological analyses based on several characters, as well as other evidence, led Frederiksen and Petersen (1998) to include it in S. cereale.
6.2 Secale Species
6.2.1 Introduction
The Secale species are perennials or annuals, with 25–120-cm-long culms and 6–15-cm-long spikes. The spikes are dense, laterally compressed, with solitary spikelets at each rachis node. In the wild species and in a number of the weedy types, spikes are brittle and disarticulate at maturity into spikelets with the rachis internode below each spikelet (wedge-type dispersal unit) or rarely, beneath the florets (floret-type dispersal unit); in the domesticated types and in most of the weedy types the spikes are not brittle. The number of spikelets per spike ranges from 15 to 25, with each spikelet containing two hermaphroditic florets and a third sterile, male or very rarely hermaphroditic floret. Rachises are fragile or tough, and rachis segments are densely covered with white hairs on the edges. The glumes are sub-equal, 8–18-mm-long, shorter than the adjacent lemmas, linear, 1-veined, keeled, and either awnless or taper to a straight, short awn (up to 35-mm-long). The lemmas are lanceolate, 10–19-mm-long, 5-veined, prominently keeled and terminate in a long, straight scabrous awn. The pales are nearly as long as the lemmas, are membranous, and 2-keeled. Anthers are 2.5–12-mm-long. The caryopsis is free.
The Secale species are cross-pollinating or self-pollinating. S. strictum subsp. africanum and S. sylvestre are self-compatible and have about 40% self-fertility, while most lines of S. cereale and S. strictum subsp. strictum are self-incompatible (Jain 1960; Kranz 1963; Kuckuck and Peters 1967; Stutz 1972). S. vavilovii and S. iranicum, which were included in S. cereale by Frederiksen and Petersen (1998), are autogamous (Kuckuck and Peters 1967) show about 50% self-fertility (Kranz 1963). In fact, Kranz (1963) observed many intermediate forms in S. vavilovii and S. iranicum, from allogamous through autogamous to cleistogamous. Assuming that the ancestor of the genus Secale was self-incompatible, then the transition from self-incompatible to self-compatible occurred independently several times in the genus, i.e., to S. sylvestre, to S. strictum subsp. africanum, and to S. cereale subsp. vavilovii.
A correlation between anther length and breeding habit exists in Secale species. Self-sterile, allogamous taxa feature long anthers (5–12 mm), whereas autogamous taxa have short anthers (2.5–5.0 mm) (Schiemann and Nürnberg-Krüger 1952; Nürnberg-Krüger 1960; Stutz 1957, 1972; Khush and Stebbins 1961; Khush 1963b; Kranz 1961, 1973; Kobyljanskij 1975, 1983; Hammer 1990). However, the actual degree of self-sterility has only been thoroughly studied in S. cereale (incl. S. vavilovii), which shows a continuous variation between self-sterility and self-fertility (Lundquist 1954, 1956, 1958a, b; Voylokov et al. 1993; Meier et al. 1996). The cross-pollinating taxa of Secale, i.e., the wild S. strictum subsp. strictum, the domesticated S. cereale subsp. cereale, and most of the weedy types of S. cereale subsp. ancestrale, exhibit broad morphological variation, both within and between populations.
The Secale species are native to the Mediterranean region and western Asia. The genus distributes from central Europe and the western Mediterranean through the Balkans, Anatolia, the Levant, and the Caucasus to Central Asia. An isolated population also exists in South Africa.
6.2.2 Secale sylvestre Host
Secale sylvestre Host [Syn.: Triticum silvestre (Host) Asch. and Graebn.; Secale campestre Kit. ex Schult.; Triticum campestre (Kit.) Kit. ex Roem. and Schult.; Secale fragile M. Bieb.; S. cereale M. Bieb.; Triticum fragile (M. Bieb.) Link; Secale sylvestre var. fragile (M. Bieb.) Fritsch ex Nevski; S. glaucum d’Urv.; S. sylvestre var. glaucum (d’Urv.) Fritsch ex Nevski; S. sylvestre f. glaucum (d’Urv.) Roshev.: Secale spontaneum Fisch.] is an annual and self-pollinating species, possible with cleistogamous flowers. Culms are 25–50-cm-long, the rachis is highly fragile, and disarticulates at maturity into dispersal units, each consisting of a single spikelet and the rachis segment below it (wedge-type disarticulation). Glume awns are 15–35-mm-long, lemma awns are up to 65-mm-long, bristles are 0.5–0.7-mm-long on lemma keel, anthers are 2.5–3.5-mm-long.
Secale sylvestre is characterized by its long awns. Morphologically, S. sylvestre is well separated from the other two species of Secale. It also differs from S. cereale by three chromosomal translocations and from S. strictum by a single one. However, it is largely inter-fertile with both these species (Sencer and Hawkes 1980).
Secale sylvestre distributes in the area ranging from Hungary in the west, to the Altai mountains of Central Asia in the east. It is a psammophyte (a plant that thrives in sandy conditions) and grows near riversides, in river deltas and seashores, sand dunes, sandy pastures, steppes and semi-deserts (Roshevitz 1947).
6.2.3 Secale strictum (C. Presl) C. Presl
Secale strictum (C. Presl) C. Presl [Syn.: Triticum strictum C. Presl; S. montanum Guss.; T. cereale var. montanum (Guss.) Kuntze; S. cereale var. montanum (Guss.) Fiori in Fiori and Paol.; Frumentum Secale E. H. L. Krause; S. anatolicum Boiss.; S. cereale var. anatolicum (Boiss.) Regel; S. montanum var. anatolicum (Boiss.) Boiss.; T. cereale var. anatolicum (Regel) Kuntze; T. cereale ssp. montanum var. anatolicum (Boiss.) Asch. and Graebn.; S. montanum ssp. anatolicum (Boiss.) Tzvelev; S. strictum ssp. anatolicum (Boiss.) K. Hammer in Hammer, Skolimowska and Knüpffer; S. dalmaticum Vis.; T. cereale ssp. montanum var. dalmaticum (Vis.) Asch. and Graebn.; S. montanum var. dalmaticum (Vis.) E. Schiem.; S. strictum ssp. strictum K. Hammer in Hammer, Skolimowska and Knüpffer; S. serbicum PanÈic ex Griseb.; S. kuprijanovii Grossh.; S. montanum Guss. ssp. kuprijanovii (Grossh.) Tzvelev; S. strictum ssp. kuprijanovii (Grossh.) K. Hammer in Hammer, Skolimowska and Knüpffer; S. kuprijanovii ssp. ciscaucasica A. P. Ivanov and Yakovlev; S. kuprijanovii ssp. transcaucasica A. P. Ivanov and Yakovlev; S. chaldicum Fed.; S. montanum ssp. chaldicum (Fed.) Tzvelev; S. kuprijanovii var. chaldicum (Fed.) Sinskaya and Bork.; S. cereale var. perennans Dekapr. in Grossh.: S. daralagesi Tumanian; S. rhodopaeum Delip.; S. anatolicum Delip.; S. perenne Hortor in Fisch. and C. A. Mey.]. According to Frederiksen and Petersen (1998), Secale strictum contains two subspecies, ssp. strictum and ssp. africanum (Stapf) K. Hammer.
6.2.3.1 Ssp. strictum
The plants are perennial and allogamous, with 40–100-cm-high culms that are glaucous, tufted, and glabrous below the spikes. Spikes are 6–14-cm-long (excl. awns), the rachis is densely hairy along the margins, and fragile, and disarticulating with rachis internode below spikelets (wedge-type dispersal units). Spikelets are 2-flowered, glumes are keeled and 15–23-mm-long (incl. awns that are 0–6-mm-long), lemma are 15–24-mm-long (excl. awns), with a strongly developed keel, which features strongly developed bristles, and end in a scabrous awn that is 4–50-mm-long, and with 5–12-mm-long anthers.
Ssp. strictum contains two varieties, var. strictum and var. c iliatoglume (Boiss.) Frederiksen and Petersen comb. nov. (Frederiksen and Petersen 1998). Var. strictum is morphologically very variable, comprising a group of perennial cross-pollinated taxa, such as S. dalmaticum Vis., S. anatolicum Boiss., and S. kupriyanovii Grossh.
Var. ciliatoglume [Syn.: Secale montanum var. ciliatoglume Boiss.; S. ciliatoglume (Boiss.) Grossh.; Triticum cereale ssp. montanum var. ciliatoglume (Boiss.) Asch. and Graebn.; S. anatolicum var. ciliatoglume (Boiss.) A. P. Ivanov and Yakovlev; S. strictum ssp. ciliatoglume (Boiss.) K. Hammer in Hammer, Skolimowska and Knüpffer], differs from var. strictum by its dense layer of hairs over the internodes, leaf sheaths, and blades. Var. ciliatoglume also differs from var. strictum by three restriction site mutations in the plastid DNA (Petersen and Doebley 1993).
Var. strictum is an Irano-Turanian and Mediterranean element, extending from the western Mediterranean to the Caspian Sea, namely, Morocco southeast Spain, Sicily, south Balkans, Greece, Syria, Lebanon, Mt. Hermon and Golan Heights, central and eastern Turkey, southern Armenia, Caucasus, northern Iraq, and northwestern Iran. Var. strictum is native to elevated plateaus and mountain systems and mainly grows in primary habitats (meadows, rangelands, open oak-park forests, shrub formations) on calcareous slopes, on rocky mountain slopes, in dry mountain areas, in the sub-alpine and alpine regions of the mountains, and as a weed in segetal habitats, such as along roadsides or the edges of cultivated fields (Roshevitz 1947; Sencer and Hawkes 1980). Var. ciliatoglume is restricted to eastern Turkey, southern Armenia, north-western Iran and northern Iraq. It grows on dry, stony or sandy mountain slopes.
6.2.3.2 Secale strictum ssp. africanum (Stapf) K. Hammer
Secale strictum ssp. africanum (Stapf) K. Hammer [Syn.: S. africanum Stapf; S. montanum ssp. africanum (Stapf) Kobyl.] is perennial and self-pollinating, with culms up to 100-cm-high. Its spike is 80–120-mm-long, linear, very dense and laterally compressed, its rachis has short hairs and disarticulates at maturity, the spikelets are solitary, 10–15-mm-long, and laterally compressed. Its two unequal glumes are shorter than the lemmas, and awned; lemmas are 5-nerved, and keeled, with an awn up to 20-mm-long, with less developed bristles on the keel (only about 0.3-mm-long). Anthers are approximately 5-mm-long.
Ssp. africanum is a single taxon found only in South Africa. This subspecies inhabits natural vegetation on stony ground among shrubs, but only in a very small area of the country; even in this area it appears to be rare (Schiemann and Schweickerdt 1950). In fact, ssp. africanum is only known from a single locality in the Sutherland District of the Western Province of South Africa. This disjuncted location, at a long distance from the distribution of other Secale taxa, is peculiar and has been explained by either human activities or as the remain of an originally much larger continuous distribution area (Schiemann and Schweickerdt 1950; Khush 1962). Alternatively, grains (or spikelets) of this subspecies might have been brought from the Mediterranean-central Asiatic region to South Africa by migrating birds, either through droppings that contain undigested grains or through spikelets that were attached to their feathers. The enigma has not yet been satisfactorily solved.
6.2.4 Secale cereale L.
Secale cereale L. [Syn.: Triticum cereale (L.) Salisb., T. Secale Link, Triticum cereale ssp. eu-cereale Asch. & Graebn., Frumentum secale var. cereale E. H. L. Krause] contains the domesticated varieties and a group of weedy, semi-wild forms. All are annual, self-incompatible or sporadically self-compatible, chromosomally homologous, and fully inter-fertile with one another. The species was divided into two subspecies, ssp. cereale, containing all the domesticated forms, and ssp. ancestrale, containing all the weedy and semi-wild forms (Frederiksen and Petersen 1998).
6.2.4.1 Ssp. cereale
Secale cereale L. subsp. cereale [Syn.: S. cereale ssp. indo-europaeum Antropov and Antropova in Roshev., S. cereale var. eligulatum Vavilov in Majssurjan, S. cereale var. compositum Lilj., S. cereale var. vulgare Kom., Triticum cereale ssp. eucereale Asch. & Graebn., S. trijlorum P. Beauv., S. cereale var. trijlorum (P. Beauv.) Peterm.] is an annual, mostly allogamous (occasionally autogamous) plant, with a tough (occasionally brittle) rachis, and with characteristic large and plump grains (Fig. 5.4b). It is grown as a cereal in most temperate regions, tolerating cold climates and poor soils. Ssp. cereale is mainly cultivated in Europe (Germany, Poland, Russia, Belarus Ukraine, Denmark and Spain), China, Turkey, Caucasus, Central Asia, North and South America (mainly Canada), and Australia (Table 6.2). It is also cultivated in high elevations in the tropics and subtropics, i.e., in the highlands of East Africa. Rye is also grown in Morocco, Algeria, Egypt and South Africa.
It probably originated in northeastern Turkey as the weedy derivative of wild S. strictum, infesting wheat and barley fields, and eventually taken into cultivation when agriculture spread northwards and eastwards into colder climates (see Sect. 5.6 on rye domestication). Currently, subsp. cereale is grown as a grain crop and in many areas as forage. Rye is an important food plant, especially in north and east Europe. It includes a great number of varieties.
6.2.4.2 Ssp. ancestrale Zhuk.
This subspecies includes S. ancestrale (Zhuk.) Zhuk.; S. cereale ssp. afghanicum (Vavilov) K. Hammer in Hammer Skolimowska and Knüpffer.; S. afghanicum (Vavilov) Roshev.; S. segetale ssp. segetale var. afghanicum (Vavilov) Tzvelev; S. segetale ssp. afghanicum (Vavilov) Bondar. ex O. Korovina; S. cereale ssp. dighoricum Vavilov; S. dighoricum (Vavilov) Roshev.; S. segetale ssp. dighoricum (Vavilov) Tzvelev; S. segetale (Zhuk.) Roshev.; S. cereale ssp. segetale Zhuk.; S. kasakorum Roshev.; S. cereale ssp. vavilovii (Grossh.) Kobyl.
Ssp. ancestrale is an annual weedy or semi-wild taxon always found as weeds in cultivated fields and field borders in Anatolia, the Caucasus and Central Asia (Vavilov 1926; Zhukovsky 1933; Roshevitz, 1947; Sencer 1975). It contains forms with different degrees of spike brittleness, including non-brittle, partly brittle (usually the upper part of the spike) and fully brittle. The forms with non-brittle spikes are weeds that infest wheat and barley fields in southwestern Asia, Caucasia and Transcaucasia and in southeastern Europe. Weeds with partly brittle spikes are common in Armenia, northeastern Iran, Afghanistan and central Asia. Usually, the upper part of the mature spike disarticulates upon maturity, while the lower part remains intact and is harvested together with the wheat or the barley crop. Forms of subsp. ancestrale with fully brittle spikes are relatively rare and have been found in western Turkey and in western Iran. S. cereale ssp. ancestrale infests cultivated fields as well as secondary habitats, such as edges of cultivation and roadsides.
6.3 Cytology, Cytogenetics and Evolution
All three Secale species are diploids, with 2n = 2x = 14 (Sakamura 1918; Stolze 1925; Aase and Powers 1926; Thompson 1926; Emme 1927; Lewitsky 1929, 1931; Jain 1960; Bowden 1966; Love 1984; Petersen 1991a, b); their genome has been designated R (Love 1984; Wang et al. 1995). B-chromosomes occur in a low frequency in S. cereale and in a few populations of S. strictum subsp. strictum (Emme 1928; Darlington 1933; Hasegawa 1934; Popoff 1939; Müntzing 1944, 1950; Kranz 1963; Jones and Rees 1982; Niwa et al. 1990). Several synthetic autotetraploid lines of the domesticated subspecies S. cereale ssp. cereale, also exist. The karyotype of all Secale species is symmetric; three chromosome pairs are metacentric and four are sub-metacentric, of which one pair, chromosome 1R, carries a satellite (Bennett et al. 1977; Fig. 5.4c).
With the exception of the SAT-chromosome, the similar arm ratios and relative length of Secale chromosomes render it difficult to distinguish between chromosomes using conventional cytological methods. Yet, the presence of massive blocks of sub-telomeric heterochromatin characteristic to Secale chromosomes (Lima-de-Faria 1953; Vosa 1974; Gill and Kimber 1974; Singh and Röbbelen 1975), has enabled recognition of individual Secale chromosomes via C-banding techniques (Vosa 1974; Gill and Kimber 1974; Singh and Röbbelen 1975; Fig. 5.4c). Giemsa banding of domesticated Secale cereale chromosomes, not only enables identification of individual chromosome, but also shows large telomeric heterochromatic bands in most of the telomeres and a number of weaker bands in centromeric and interstitial positions (Vosa 1974; Gill and Kimber 1974; Singh and Röbbelen 1975). In fact, all S. cereale chromosomes possess thin centromeric bands and a number of bands adjacent to the secondary constriction on chromosome 1R (Vosa (1974). As an allogamous species, Secale cereale exhibits great variability in Giemsa banding patterns (Singh and Röbbelen 1975; Giraldez et al. 1979). The few specimens of S. strictum ssp. strictum that have been studied, also exhibit large telomeric heterochromatic bands (Singh and Röbbelen 1975; Cuadrado and Jouve 1995). In contrast, S. sylvestre bears small telomeric bands (Singh and Röbbelen 1975).
The constitutive heterochromatin in somatic chromosomes, detected by C-banding, has been shown by Gill and Kimber (1974) to be equivalent to the classical heterochromatic structures observed by Lima-de-Faria (1953) in pachytene chromosomes of S. cereale. The pattern and relative size of the terminal C-bands, pattern of minor interstitial bands and arm ratios enable individual chromosome identification. Since common wheat, Triticum aestivum, chromosomes do not have the dense band in the terminal position on the short arms, Gill and Kimber (1974) used the distinct traits of Secale chromosomes to identify the seven disomic additions of Imperial rye chromosomes to common wheat. On the basis of their homoeology with wheat chromosomes, Gill and Kimber (1974) arranged the seven rye chromosomes in the homoeologous groups of wheat chromosomes and designated them 1R to 7R. Imperial rye chromosomes are considered to be the standard for karyotype arrangement of S. cereale (Sybenga 1983).
The Secale genome differs from that of wheat in both size and structure (Gill and Friebe 2009). Its size of approximately 9 pg 1C DNA is 33% larger than the genome of diploid wheat (~6 pg 1C DNA), and is among the larger genomes of the Triticeae (Table 6.3). 1C DNA content ranges from 7.21 pg in S. sylvestre to 7.4 pg in S. strictum subsp. africanum, 8.28–8.65 pg in S. cereale ssp. cereale and 8.20–9.45 pg in S. strictum subsp. strictum (Table 6.3). Intraspecific and interspecific variations in DNA content among Secale genomes are mainly due to different amounts of sub-telomeric heterochromatin (Bennett et al. 1977). In fact, Bennett et al. (1977) measured the length of sub-telomeric C-bands and found that the proportion of sub-telomeric heterochromatin in the genome ranged from about 6% in S. Silvestre and S. strictum ssp. africanum to about 9% in S. strictum ssp. strictum and to 12.24% in S. cereale subsp. cereale (Table 6.3). Thus, one of the major evolutionary changes in chromosome structure in Secale has involved the addition of heterochromatin close to the telomeres (Bennett et al. 1977). Bedbrook et al. (1980) succeeded in cloning six families of non-homologous repeat heterochromatin-specific DNA sequences of S. cereale ssp. cereale. The six sequences are predominantly located within the blocks of constitutive sub-telomeric heterochromatin that can be observed on all seven ssp. cereale chromosome pairs by Giemsa staining. Four of these sequence unrelated families, having repeating units of 120, 480, 610, and 630 bp, account for most, if not all, of the difference in sub-telomeric heterochromatin DNA content between the three Secale species (Bedbrook et al. 1980; Table 6.3). The four repeats are present in high copy numbers in S. cereale DNA and in somewhat smaller amounts in S. strictum ssp. strictum whereas only one repeat is detectable in S. sylvestre DNA and two repeats in S. strictum ssp. africanum (Table 6.3). The four families of ssp. cereale-specific sequences, accounting for most of the sub-telomeric heterochromatin, are arranged in tandem arrays, are complex and contain simple sub-repeats interspersed with an unrelated sequence without sub-repeats. Bedbrook et al. (1980) suggested that each of the ssp. cereale-specific repeats evolved by the insertion of DNA elements into an array of simple repeats, followed by amplification of the portion of the array containing the inserted sequence.
The structure, copy number and chromosomal location of arrays of the four families of highly repeated sequences have been investigated in Secale species (Jones and Flavell 1982a, b). Each species was found to be unique in its complement and/or chromosomal distribution of the sequence families. For example, S. strictum subsp. strictum and S. cereale ssp. cereale accessions show the same complement of repeated sequences, but differ substantially in the number of repeats they contain of the 480-bp, 610-bp, and 630-bp sequences (Table 6.3). The structure of the 480-bp repeating unit also varies across accessions of ssp. strictum. In this outbreeding subspecies, hetero-morphisms are frequent, and are particularly conspicuous in hybridization analyses detecting the 480-bp sequence.
The relationship between the chromosomal location of heterochromatin C-bands and of the four non-homologous repeat sequence families, constituting 12% or more of total ssp. cereale DNA, has been investigated by in situ hybridization in ssp. cereale chromosomes (Jones and Flavell 1982a, b). Only centromeric and nucleolar organizer region-associated C-bands failed to hybridize with at least one of the sequences, whereas many sub-telomeric blocks of heterochromatin contained all four repeat sequence families.
The repeat sequences are mostly ssp. cereale-specific and serve as convenient markers for ssp. cereale chromatin in wheat-rye hybrids (Appels 1982; Lapitan et al. 1986). Upon study of the distribution of families of repeats in triticale and in Secale-addition lines to bread wheat, Jones and Flavell (1982a) found that some of the families of repeats, present in rye but not in wheat sub-telomeric heterochromatin, were selected against in the wheat genetic background.
Using FISH, Hutchinson et al. (1981) studied the relationship between sub-telomeric C-bands and the four families of repeat sequences. They used the DNA probes, produced by Bedbrook et al. (1980) and Jones and Flavell (1982a) that represent the repeat sequences, namely, pSc119.2 representing the120 bp repeat, pSc74 the 350–480 bp repeat, and pSc34 the 630 bp repeat. Similar to Jones and Flavell (1982b), also Hutchinson et al. (1981) found that these repeats account for most, if not all, of the differences in sub-telomeric heterochromatic DNA quantities between the Secale species. The proportion of DNA in the genome represented by these sequence families in different species of Secale is different (Hutchinson et al. 1981). The 120-bp family is equally abundant in all Secale species and is the only repeat family found in S. sylvestre, in which a correlation has also been observed between low C-heterochromatin content and the absence of the other three repeat sequences (Hutchinson et al. 1981; Jones and Flavell 1982b). The relative high DNA amount and the higher proportion of heterochromatin in ssp. cereale and ssp. strictum, is the result of accumulation of several repeat families that constitute the major components of sub-telomeric heterochromatin and are absent in S. sylvestre (Table 6.3).
In accord with the above, Cuadrado and Jouve (1997) used FISH with the probes pSc119.2, pSc74, and pSc34 to study the quantity and distribution of the highly repeated sub-telomeric DNA sequences that are located in the sub-telomeric heterochromatin. In accord with the above, they showed that S. sylvestre had considerably fewer repeat DNA sequences in the sub-telomeric heterochromatin than the other two species and proposed that it was due to its autogamous nature.
The fairly constant C-banding pattern of all seven chromosomes in various samples of S. strictum ssp. strictum were reported by Gustafson et al. (1976). The chromosomes of this subspecies are easily identifiable and can be distinguished from the seven S. cereale chromosome pairs by their distinct C-banding pattern (Gustafson et al. 1976). FISH analysis of the karyotype of ssp. strictum was performed using the probes pSC119.2, pSc74, and pSc34, enabling the identification of each ssp. strictum chromosome (Cuadrado and Jouve 1995). Moreover, this labeling allowed the comparison of the karyotype of ssp. strictum to that of ssp. cereale since labeling of a combination of two different repetitive DNA sequences enabled identification of all chromosomes of both species (Cuadrado and Jouve 1995). Using this approach, it was found that the physical locations of the repetitive 120-, 480-, and 610-bp repeats are rather similar in the chromosomes of ssp. strictum and ssp. cereale and that the main qualitative difference lies in the rarity of a combination of the 610-bp and 480-bp repeats in the same telomeres in ssp. strictum, in contrast to ssp. cereale (Cuadrado and Jouve 1995). This finding is in accord with that of Jones and Flavell (1982b), who reported that both species have the same complement of repetitive DNA sequences, but differed significantly in the amount of telomeric 610-bp repetitive sequences and in the pattern of distribution of the 480-bp repetitive sequences along the chromosomes. Differences in the distribution of hybridization sites of the 120-bp family (pSc119.2) probe in both subspecies were limited to chromosome arms 2RS, 2RL and 7RL. The 610-bp repetitive sequence probe hybridized exclusively to the sub-telomeric regions predominantly of chromosome arms 1RS, 1RL, 4RS, 5RS, 6RS and 7RS, and was almost always absent in the most prominent heterochromatic blocks of sub-telomeric 2RS, 2RL and 7RL in ssp. strictum. Jones and Flavell (1982b) reported a major difference in the hybridization responses of ssp. strictum and ssp. cereale to the pSc34 (610 bp) probe, with hybridization being clearly more intense in ssp. cereale. Finally, use of the pSc74 probe, demonstrated the presence of the 480-bp sequence in almost all arms (Cuadrado and Jouve 1995). Interestingly, interstitial hybridization sites were found in the short arm of 6R in ssp. strictum and in the long arm of the same chromosome in S. cereale (Jones and Flavell 1982a; Lapitan et al. 1988; Mukai et al. 1992; Cuadrado and Jouve 1994).
González-García et al. (2006) used FISH to compare the morphology of the sub-telomeric heterochromatin during the transition from zygotene to second meiotic telophase in meiocytes of Secale cereale ssp. cereale. At zygotene, pachytene and diplotene, the sub-telomeric heterochromatin formed clumps, often featuring two or more bivalent ends, strongly suggesting ectopic recombination. The high variability between homologous chromosomes and the frequent nonhomologous bindings of sub-telomeric heterochromatin, strongly suggest that rye sub-telomeric heterochromatin is in a dynamic state and that its position along the chromosome changes frequently during meiosis (González-García et al. 2006).
Little is known about the mechanism driving the dynamics of telomeric chromatin. Insertions of DNA sequences into an array of single repeats, followed by saltatory amplification and the occurrence of other chromosomal rearrangements, may have played an important role in the process. These could result from saltatory amplification events at telomeres that were initially responsible for each large increase in DNA quantity. Subsequently, unequal crossing-over between homologues may have played an important secondary role, by extending the range of variation in the amount of heterochromatin at a given telomere, while crossing-over between non-homologues may have driven an increase in the DNA quantity at one telomere to be distributed between chromosomes (Bennett et al. 1977). In accord with this, Evtushenko et al. (2016) found that the evolution of sub-telomeric heterochromatin appears to have involved a significant contribution of illegitimate recombination. They suggested that the large blocks of sub-telomeric heterochromatin arose from the combined activity of transposable elements (TEs) and the expansion of the tandem repeats, likely as a result of a highly complex network of recombination mechanisms. The abundance of TEs and repeats associated with heterochromatin in sub-telomeric regions raises questions as to their potential role in telomere activity. It is unlikely that this heterochromatin can substitute for telomeres as in Drosophila (Pardue and DeBaryshe 2003), because plants have both the telomerase and the array of simple telomeric repeats necessary for telomere maintenance. However, it is possible that the heterochromatin packaging and dynamics at the chromosome ends affects telomeric functions and chromosome behavior in cereals, as it does in other species (Schoeftner and Blasco 2009).
The occurrence and distribution of the sub-telomeric tandem arrays in the different Secale species suggest that S. sylvestre may be of ancient origin, while S. strictum and S. cereale may have a more recent origin (Jones and Flavell 1982b). The fact that the 120-bp repeat is the only repeat family that exists in S. sylvestre, may indicate that this repeat was the first to be amplified in the evolution of the genus Secale (Zeller and Cermeño 1991). On the other hand, if S. strictum ssp. strictum is more ancient than S. sylvestre, then repeat sequences may have also been lost during evolution of the species.
Murai et al. (1989) used several restriction endonucleases to study chloroplast DNA variation in all the species of Secale. The chloroplast genome size was estimated to be 136 kbp, which is very close to its size in Triticum and Aegilops, and produced identical patterns with all the restriction enzymes applied in S. strictum ssp. strictum and S. cereale ssp. cereale, but not in S. sylvestre. The restriction fragment patterns of S. sylvestre showed up to two differences from those of the other Secale taxa, suggesting early separation of S. sylvestre from the rest of the species.
There is a general agreement that the Triticeae tribe is monophyletic and therefore, assumed to be derived from a common ancestor (Watson et al. 1985; Kellogg 1989; Soreng et al. 1990; Hsiao et al. 1995a). Thus, genetic similarities, i.e., synteny (the conservation of order of loci on homoeologous chromosomes), might be expected between the homoeologous chromosomes of the various Triticeae species and those of the common wheat cultivar Chinese Spring, whose seven homoeologous chromosome groups serve as a standard (Sears 1954, 1966). The homoeology of the chromosomes of a given Triticeae species is determined by the degree to which a pair of chromosomes that is added to a nullisomic line of common wheat compensates for the missing wheat chromosome pair for vigor and fertility. Accordingly, the nomenclature of the chromosomes of the Secale species is based on the homoeologous system of the Triticeae. Good genetic compensation by Secale chromosomes to common wheat chromosomes has been indicated by the ability of the former to satisfactorily compensate for the missing bread wheat chromosomes when substituted into wheat. Over the years, individual chromosomes of both, domesticated rye, Secale cereale ssp. cereale, and wild type, S. strictum ssp. strictum, have been added to bread wheat, and substituted of wheat chromosomes (Miller 1984). Evidence from the compensating effect of Secale chromosomes in the absence of their common wheat homoeologues in wheat-Secale (S. cereale and S. strictum) addition and substitution lines implied homoeology relationships between Secale and bread wheat chromosomes (Zeller and Hsam 1983; Miller 1984). In fact, Gill and Kimber (1974), Zeller and Hsam (1983), and Miller (1984) designated the seven pairs of rye chromosomes 1R-7R relating to the seven homoeologous groups of common wheat.
Supporting evidence of the homoeology between Secale and wheat chromosomes can be obtained by comparing the chromosomal location of genes and of various biochemical and molecular markers. Studies of gene localization in wheat-Secale (S. cereale and S. strictum) addition and substitution lines, have contributed considerably to the knowhow on the position and order of genes in chromosomes of Secale relative to wheat. Devos et al. (1993) constructed an RFLP-based genetic map of S. cereale ssp. cereale that provided evidence that the genetic synteny between Secale and wheat chromosomes has been affected by chromosomal rearrangements that occurred during the evolution of the various Secale genomes. Their work revealed multiple evolutionary translocations in the Secale genome relative to that of bread wheat. DNA clones indicated that chromosome arms 2RS, 3RL, 4RL, 5RL, 6RS, 6RL, 7RS and 7RL have all been involved in at least one translocation. Moreover, Devos et al. (1993) identified the translocated chromosomal segments, and suggested a possible evolutionary pathway that could account for the present-day structure of Secale genomes relative to one another and to those of bread wheat.
Secale primary trisomics and telo-trisomics lines (Zeller et al. 1977) as well as rye addition and substitution lines (O’Mara 1940; Driscoll and Sears 1971; Miller 1984; Schlegel et al. 1986; Zeller and Cermeño 1991; Mukai et al. 1992) have been used for chromosome and arm mapping of genes. Schlegel (1982) even produced monosomic additions of wheat chromosomes to rye. However, because all of these aneuploids do not breed true and are highly sterile, researchers preferred to use monosomic or telosomic additions of Secale chromosomes to wheat (Mukai et al. 1992) for rye (S. cereale ssp. cereale) genome mapping. Wheat-rye recombinant chromosome stocks provide further opportunities for chromosome mapping (Rogowsky et al. 1993; Lukaszewski 2000; Lukaszewski et al. 2004).
Translocations have played an important role in karyotype evolution and speciation of many plant groups (Stebbins 1958; Rieseberg 2001; Faria and Navarro 2010) and, as such, are thought to have played an important role in the evolution of the genus Secale (Stutz 1972; Koller and Zeller 1976; Shewry et al. 1985; Naranjo et al. 1987; Naranjo and Fernández-Rueda 1991; Liu et al. 1992; Rognli et al. 1992; Devos et al. 1993; Schlegel 2013). The chromosomes that were involved in the various translocations characterizing Secale species, were identified by studying the ability of trisomics of rye chromosomes (Heemert and Sybenga 1972) or chromosome arms to successfully substitute nullisomy for homoeologous wheat chromosomes (Koller and Zeller 1976; Miller 1984). This was achieved by studying pairing between rye and wheat chromosome arms in the presence and absence of the homoeologous-pairing suppressor gene, Ph1 (Naranjo et al. 1987; Naranjo and Fernández-Rueda 1991), and by using various kinds of genetic markers (Shewry et al. 1985; Liu et al. 1992; Devos et al. 1993).
Chromosome pairing at first meiotic metaphase in PMCs of F1 hybrids between Secale species, has shown that they differ from each other by a number of translocations (Riley 1955; Stutz 1957; Khush and Stebbins 1961; Khush 1962; Kranz 1973). The perennial wild S. strictum and the annual wild S. sylvestre differ from S. cereale by two reciprocal translocations that involve three pairs of chromosomes (Schiemann and Nürnberg-Krüger 1952; Riley 1955; Stutz 1957; Khush and Stebbins 1961; Khush 1962; Kranz 1963; Singh and Röbbelen 1977). These translocations appear as a hexavalent configuration in the F1 hybrids of S. strictum and S. sylvestre with S. cereale. Heemert and Sybenga (1972) used a standard tester set of reciprocal translocations in S. cereale and several primary trisomics to identify the chromosomes involved in the two translocations between S. cereale and S. strictum. They reported that the two translocations involved chromosomes I (=2R), V (=6R) and III (=7R). Later, these translocations were found to involve the short arm of 2R (2RS), and the long arms of 6R and 7R (6RL and 7RL, respectively) (Naranjo and Fernández-Rueda 1991; Devos et al. 1993). Another translocation that differs between these two species of Secale, was discovered by Shewry et al. (1985), who located the Sec2 gene on chromosome 6RS of S. strictum and on 2BS of S. cereal. They concluded that there was a translocation between 2 and 6RS in S. cereale relative to S. strictum (and probably to wheat, where homologous genes are located on 6AS, 6BS, and 6DS). This has been presented as evidence of a translocation between part of the 2R short arm and part of the 6R short arm (Devos et al. 1993). The short arm of chromosome 4R of S. cereale is homoeologous to wheat chromosome arms 4AS, 4BS and 4DL, whereas the proximal region of the long arm of 4R was translocated with a region of 7RS and is homoeologous to the short arm of wheat chromosomes 7A, 7B and 7D (Koller and Zeller 1976), and the distal region with 6RS (Devos et al. 1993). On the other hand, the proximal region of the short arm of S. cereale chromosome 7R is homoeologous to wheat chromosome arms 4AL, 4BL, and 4DS, while the distal region of 7RS is homoeologous to the distal region of chromosomes of wheat group 5 (Devos et al. 1993). The proximal region of the long arm of 7R is homoeologous to the long arm of wheat 7AL, 7BL, and 7DL, while the distal region was translocated with 2RS (Koller and Zeller 1976; Devos et al. 1993). Chromosomes 4R and 7R of S. strictum did not undergo rearrangements and are homoeologous to wheat homoeologous groups 4 and 7, respectively. The translocation between chromosomes 4R and 7R is in addition to the two translocations between 2R, 6R, and 7R in S. cereale (Koller and Zeller 1976; Devos et al. 1993). Only chromosome 1R of S. cereale was not rearranged and is homoeologous to wheat homoeologous group 1, whereas all other six chromosome pairs of this species were involved in translocations (Devos et al. 1993). Additional smaller translocations distinguish S. sylvestre from S. cereale (Khush and Stebbins 1961; Khush 1962; Kranz 1963), and a single minor translocation separates S. sylvestre from S. strictum (Khush 1962). S. strictum, subsp. africanum was found to differ from subsp. strictum by a small translocation (Khush 1962; Singh and Röbbelen 1977). It is probable that the chromosomal rearrangements separating S. sylvestre from the other two species and separating S. cereale from S. sylvestre and S. strictum, were instrumental in speciation within the genus.
The translocations characterizing the Secale genomes can be classified into five categories: (1) Translocations that are common to all Secale species, wheat and other Triticineae. King et al. (1994) reported the existence of a 4AL/5AL translocation in T. urartu. Devos et al. (1995), and Dubcovsky et al. (1996) identified the same translocation in diploid wheat, Triticum monococcum, and in hexaploid wheat, T. aestivum, which both showed identical breakpoints (Li et al. 2016), and assumed that it occurred at the diploid level. A similar 4RL/5RL translocation was found in S. cereale (Naranjo et al. 1987; Naranjo and Fernández-Rueda 1991; Devos et al. 1993). Homoeologous chromosome pairing studies between bread wheat and S. cereale, showed that the 4RL/5RL translocation underwent an additional rearrangement in which the 4RL arm was translocated to 7RS (Naranjo et al. 1987; Naranjo and Fernández-Rueda 1991; Liu et al. 1992; Rognli et al. 1992; Devos et al. 1993; King et al. 1994). Presence of the 4L/5L translocation has also been demonstrated in Ae. umbellulata and diploid Elymus farctus subsp. bessarabicus (King et al. 1994), but has not been demonstrated in diploid Elymus elongatus and in barley. Li et al. (2016) identified the breakpoints of the 4L/5L translocation in bread wheat and rye. The wheat translocation joined the ends of breakpoints downstream of a WD40 gene on 4AL and a gene of the PMEI family on 5AL. While rye shares the same position for the 4L breakpoint, its 5L breakpoint position differs, although very close to that of wheat, indicating the recurrence of 4L/5L translocations in wheat and rye. These findings suggest that if this translocation occurred recurrently in various Triticeae species, then the translocation breakpoints are the two fragile sites on the chromosome arms 4L and 5L of diploid Triticeae species and that the 4L/5L translocation breakpoints represent two hotspots of chromosomal rearrangement recurrently used during Triticeae evolution. (2) Translocations that differ between the genera Secale and Triticum. Several small translocations interfering with the homoeology between rye and wheat chromosomes but that do not separate S. cereale from S. strictum, were found by the use of various genes and DNA markers. The presence of genes belonging to wheat homoeologous group 3 on chromosome 6R, indicates possible transfer of a small 3R segment to 6R (Zeller and Cermeño 1991, and reference therein). The use of cDNA clones showed that some markers of 4R of both S. cereale and S. strictum, show phylogenetic relationship to Triticeae group 7 chromosomes (Chao et al. 1989). Likewise, substitution experiments in wheat-rye substitution lines revealed that the short arm of 4R (4RS) compensates well for group 4 of wheat chromosomes and 4RL compensates well for group 7 chromosomes (Koller and Zeller 1976). The 4RL/7RS and 3RL/6RL translocations are present in both the S. strictum and the S. cereale genomes. The evidence concerning 4RL/7RS derives from the similar plant morphology of the CS/4R of S. cereale and CS/4R of S. strictum disomic addition lines, that include the presence of the purple culm gene in both additions, which is carried on wheat 7S (cited in Devos et al. 1993). 3RL/6RL translocation exists in both S. strictum and S. cereale (Devos et al. 1993). These translocations occurred after the separation of Secale from Triticum. (3) A single minor translocation that occurred between S. sylvestre and the other two Secale species (Khush 1962). (4) Two translocations that occurred between S. cereale and S. strictum. Since these translocations characterize all examined races of S. cereale, they define its genome rather than reflect inter-varietal differences of more recent origin, and are of evolutionary significance. These translocations, involving chromosomes 2R, 6R and 7R (Heemert and Sebenga 1972), characterize only the genome of S. cereale. Another small translocation involving a fourth pair of chromosomes and characterizing the S. cereale genome, also occurred between S. strictum and S. cereale (Riley 1955). These translocations presumably happened during the evolvement of cereale from strictum. (5) A small intraspecific translocation occurring between the two subspecies of S. strictum (Khush 1962; Singh and Röbbelen 1977) as well as intraspecific translocations between races of S. cereale (Darlington 1933; Müntzing and Prakken 1941).
The F1 hybrids of the S. cereale x S. strictum cross are heterozygotes for the two translocations involving chromosomes 2R, 6R and 7R exhibiting hexavalent at first meiotic metaphase (Riley 1955). These hybrids had low fertility and resembled the wild parent, S. strictum, in that they had ears with brittle rachis, closely invested grains and perennial habit (Riley 1955). Translocation heterozygotes produce functional gametes consisting of the parental chromosomal combination. Hence, the F2 of the crosses between S. cereale and S. strictum segregated into three types, in terms of chromosome structure and plant morphology: those like S. cereale, those like the F1, and those like S. strictum, and with frequency of 1:2:1, respectively (Riley 1955). This pattern of segregation results from a correlation between the phenotypic expression of important taxonomic characters and the constitution of the plants with regard to three chromosome pairs involved in the two large translocations that occurred during the evolution of S. cereale from S. strictum. It seems probable, therefore, that the proximal regions of these three chromosome pairs, which are protected from cross-overs by more distal chiasma formations, and which always segregate in parental combinations, contain genes that might be responsible for the development of the differentiating characters of the species. Genes present in the proximal regions of these three chromosomes, probably control characters responsible for the adaptation of the two species. The genes segregate undisturbed, since gametes are only viable when all three chromosomes occur in parental combinations. In this way, the proximal regions of these three chromosomes may be regarded as a ‘super genes’ (Darlington and Mather 1949). Hence, a new arisen translocation might, by chance, have isolated a series of selectively advantageous genes from recombinations, and the newly structural condition would be of immediate adaptive value and become fixed. These two translocations presumably occurred simultaneously, rather than successively, since no race of S. cereale was found to have only one of the two translocations.
Are the two gene systems that control the major traits separating S. cereale from S. strictum, namely, annual growth habit and tough rachis, located on one of the translocated chromosomes? The F1 hybrid between common wheat (cv. Chinese Spring) and Elymus Farctus subsp. farctus (=6x Agropyron junceum) was perennial (Charpentier et al. 1986). Likewise, Dvorak and Knott (1974) noted that the amphiploid Chinese Spring—diploid Elymus elongatus (=Agropyron elongatum), combining the A, B, and D subgenomes of hexaploid wheat with the Ee genome of the perennial E. elongatus, is perennial. In this regard, Lammer et al. (2004) pointed out that hybrids between bread wheat and its wild perennial relatives, as well as many genetically stable amphiploids and partial amphiploids derived from these hybrids, exhibit the perennial trait, indicating that annual growth habit is a recessive trait. In hybrids derived from crosses between perennial and annual parents, the perennial habit seems to dominate (Stebbins and Pun 1953; Fedak and Armstrong 1986; Petersen 1991a). This is also the case in other interspecific and intergeneric hybrids in the tribe (Sakamoto 1967; von Bothmer et al. 1985; Frederiksen and von Bothmer 1989, 1995). Consistent with the notion that annual growth habit is a derived trait in the Triticeae, the evolvement of annual S. cereale from the perennial S. strictum, required a recessive mutation in the locus or loci determining this trait. Using a complete series of diploid Elymus elongatus (genome EeEe) chromosome addition lines in a Chinese Spring background, Lammer et al. (2004) found that chromosome 4Ee [most probably the short arm 4Ee (4EeS)] conferred the perennial growth habit. Assuming that the recessive gene(s) conferring annual growth-habit is located in S. cereale on 4RS, a chromosome arm that is not involved in translocations, and therefore, can segregate in hybrids between the two species only if it is located on the distal region.
The genetic control of non-brittle rachis in domesticated taxa was studied in several Triticeae species. Takahashi (1955) and Takahashi and Hayashi (1964) reported that two recessive, complementary and tightly linked genes, that later were designated btr1 and btr2 and located on chromosome arm 3HS of barley (Komatsuda and Mano 2002; Komatsuda et al. 2004), determine tough rachis in domesticated barley. Likewise, Sharma and Waines (1980) found that tough rachis is determined in diploid wheat T. monococcum subsp. monococcum by the two recessive complementary genes. Also in domesticated tetraploid and hexaploid wheat the tough rachis trait is controlled by recessive genes, br-A2 and br-A3, on chromosomes 3A and 3B (Levy and Feldman 1989a; Watanabe and Ikebata 2000; Watanabe et al. 2002, 2005a, b; Nalam et al. 2006; Millet et al. 2013). Comparative mapping analyses suggested that both br-A2 and br-A3 are present in homoeologous regions on their respective chromosomes. Furthermore, br-A2 and br-A3 from wheat and btr1/btr2 on chromosome 3H of barley are also homoeologous, suggesting that the location of major determinants of the tough rachis trait in these species has been conserved (Nalam et al. 2006). Assuming that the homoeologous genes are located in S. cereale on the same arm, namely, 3RS, then the genes involved in the non-shattering trait of S. cereale can only segregate in hybrids between S. cereale and S. strictum if it is located on the distal region.
Levan (1942) observed bivalents, trivalents and quadrivalents in low frequency in the first meiotic metaphase of haploid S. cereale, averaging 0.08–0.83 chiasmata per cell. Likewise, Neijzing (1982) observed several associations of two or more chromosomes in meiosis of haploid rye. Heneen (1963) noted a bivalent of rye chromosomes in a single cell of the pentaploid hybrid octoploid Elymus arenarius x S. cereale. Intragenomic chromosome pairing of S. cereale chromosomes, indicated by the presence of homomorphic large bivalents, was also observed in the intergeneric hybrids between diploid and polyploid Hordeum species and Secale cereale (Gupta and Fedak 1987a, b; Wagenaar 1959; Thomas and Pickering 1985; Petersen 1991b) and in hybrids between Aegilops species and S. cereale (Melnyk and Unrau 1959; Majisu and Jones 1971; Su et al. 2016). In addition, although occurring at a lower frequency than in haploid plants of S. cereal (Müntzing 1937; Nordenskiöld 1939; Levan 1942; Heneen 1965; Puertas and Giraldez 1979), pairing between S. cereale chromosomes is a usual feature in wheat-rye hybrids (Dhaliwal et al. 1977; Schlegel and Weryszko 1979). In wheat-rye hybrids, the preferential homoeologous pairing between wheat and rye chromosomes competes with that of rye-rye chromosomes (Schlegel and Weryszko 1979). No rye-rye recombinant chromosomes were observed at first anaphase, therefore rye-rye associations at first metaphase could be considered non-chiasmatic (Orellana 1985). Yet, Neijzing (1982), using Giemsa C-banding, detected chromatid exchanges between differently marked chromosome arms at first anaphase, verifying that chromosome associations observed at first metaphase of haploid rye were due to chiasma formations, which were non-randomly located and probably occurred in homologous segments. Ten to twelve sets of homologous segments were found to be present in the haploid rye genome (Neijzing 1985), likely as a result of ancient duplications. The association between C-banded and un-banded arms indicated that the telomeric heterochromatic does not act as promoter or suppressor of homologous pairing in haploid rye (Neijzing 1982).
Martis et al. (2013), using high-throughput transcript mapping, chromosome survey sequencing and integration of conserved synteny information of three sequenced model grass genomes [Brachypodium distachyon, rice (Oryza sativa), and sorghum (Sorghum bicolor)], established a virtual linear gene order model (genome zipper) comprising 22,426 or 72% of the detected set of 31,008 S. cereale genes. This enabled a genome-wide, high-density, comparative analysis of rye/barley/model grass genome synteny. Seventeen syntenic linkage blocks conserved between the model grass genomes and the rye and barley genomes, were identified. Strikingly, differences in the degree of conserved syntenic gene content, gene sequence diversity signatures and phylogenetic networks were found between individual rye syntenic blocks. This indicates that introgressive hybridizations (diploid or polyploid hybrid speciation) and/or a series of whole-genome or chromosome duplications played a role in rye speciation and genome evolution (Martis et al. 2013).
6.4 Crosses with Other Triticineae Species
6.4.1 Opening Remarks
Spontaneous intergeneric hybrids between Secale species and other Triticeae seem to be rare (Frederiksen and Petersen 1998), with the octoploid Elymus arenarius L. being one of the few reported (Heneen 1963). On the other hand, many artificial intergeneric hybrids between Secale species and other Triticeae have been produced. These hybrids have primarily involved diploid and polyploid taxa of Triticum, Aegilops, and Hordeum (e.g., Majisu and Jones 1971; Hutchinson et al. 1980; Pagniez and Hours 1986; Gupta and Fedak 1986; Petersen 1991a). In addition, artificial hybrids with several other diploid and polyploid Triticeae, e.g., diploid Elymus spicatus (Pursh) Gould, diploid Agropyron mongolicum Keng, tetraploid A. cristatum (L.) Gaertn., tetraploids Elymus pseudonutans, E. shandongensis, and E. semicostatus, and hexaploid Elymus hispidus (Opiz) Melderis, have also been studied (Stebbins and Pun 1953; Fedak and Armstrong 1986). In all combinations, Secale has been used as the pollen donor, as crossing experiments using Secale as the female parent have always failed (Majisu and Jones 1971; Petersen 1991a). The hybrids are generally described as morphologically more or less intermediate between the parents (Stebbins and Pun 1953; Wang 1987, 1988; Petersen 1991a).
The chromosomes of Secale are larger than the chromosomes of most species of the Triticeae, enabling simple identification of the parental origin of the chromosomes in artificial hybrids (von Berg 1931; Stebbins and Pun 1953; Melnyk and Unrau 1959; Wagenaar 1959; Bhattacharyny et al. 1961; Heneen 1963; Majisu and Jones 1971; Wang 1987; Fedak and Armstrong 1986; Petersen 1991b; Gill and Friebe 2009). At mitosis and meiosis, rye chromosomes can be easily distinguished from chromosomes of other Triticeae species in intergeneric hybrids, also by the presence of massive blocks of terminal heterochromatin (Lima-de-Faria 1953; Gill and Kimber 1974). In rye, C-heterochromatin is predominantly located in terminal blocks, whereas in Triticum, Aegilops and other related species, it is mostly situated in centromeric and pericentromeric regions or dispersed throughout the chromosomes. Thus, techniques such as Giemsa C-banding (Fedak and Armstrong 1986; Gill and Friebe 2009) and in situ hybridization (Hutchinson et al. 1980) have also been used to identify parental chromosomes. The ability to identify the parental chromosomes in these hybrids is of great help in determining whether the type of pairing is auto- or allo-syndetic.
Hybridizations of Secale species with species of over ten Triticeae genera have been reported (e.g., Crasniuk 1935; Stebbins and Pun 1953; Dvorak 1977; Hutchinson et al. 1980; Gupta and Fedak 1987a, b; Wang 1987, 1988; Lu et al. 1990; Lu and von Bothmer 1991; Petersen 1991b). Most authors have been able to clearly demonstrate very low levels of allosyndetic pairing between the chromosomes of such species, irrespective of the ploidy level (Stebbins and Pun 1953; Heneen 1963; Majisu and Jones 1971; Hutchinson et al. 1980; Gupta and Fedak 1987a, b; Fedak and Armstrong 1986; Wang 1987, 1988; Lu et al. 1990; Lu and von Bothmer 1991; Petersen 1991b).
6.4.2 Chromosome Pairing in Hybrids Between Elymus or Agropyron Species and Secale Species
Meiotic chromosomal pairing was analyzed in several intergeneric diploid hybrids between diploid Elymus or Agropyron species and Secale strictum (Wang 1987). Hybrids of Elymus spicatus x Secale strictum, having the genome formula StR, presented an average of 12.97 univalents, 0.49 bivalents, and 0.01 trivalents at first meiotic metaphase. The hybrid of Agropyron mongolicum x S. strictum, which have the PR genomes, had an average of 12.86 univalents, 0.51 bivalents, 0.03 trivalents and 0.004 quadrivalents. The hybrid between E. spicatus and Agropyron mongolicum (genome StP) had a mean configuration of 8.05 univalents, 2.86 bivalents, 0.07 trivalents and 0.01 quadrivalents. Chromosome pairing in PMCs of additional diploid hybrids, contained an average of 11.05 univalents, 1.22 rod bivalents, 0.04 ring bivalents, 0.13 trivalents and 0.01 quadrivalents in E. farctus subsp. bessarabicus x S. strictum (genome EbR), while in E. spicatus x E. farctus subsp. bessarabicus (genome StEb), average pairing included 4.34 univalents, 2.77 rod bivalents, 1.42 ring bivalents, 0.24 trivalents and 0.14 quadrivalents (Wang 1988). All hybrids had intermediate spike morphology, compared to their parents, and were sterile (Wang 1987, 1988). The meiotic pairings of these hybrids indicated that chromosome homology between the St and P genomes is higher than between the St and R and between the P and R. In addition, it demonstrated that the St genome of Elymus spicatus and the Eb genome of E. farctus subsp. bessarabicus are more closely related to each other than they are to the R genome of Secale. The R genome is slightly closer to the Eb genome than to the St genome (Wang 1987, 1988). Mitotic preparations of root-tip cells of these diploid hybrids suggested that the chromosomes of the different genomes were spatially separated (Wang 1987).
Lu et al. (1990) analyzed chromosomal pairing at first meiotic metaphase in the following three intergeneric triploid hybrids, Elymus pseudonutans (2n = 4x = 28; genome StStYY) x S. cereale, E. shandongensis (2n = 4x = 28; genome StStYY) x S. cereale and E. semicostatus (2n = 4x = 28; genome StStYY) x S. strictum. Meiotic configurations of the F1 triploid hybrids (2n = 3x = 21; genome StYR) included a mean 14.64 univalents, 2.82 bivalents, 0.20 trivalents, and 0.01 quadrivalents and 16.38 univalents, 2.02 bivalents and 0.16 trivalents, for two combinations of E. pseudonutans x S. cereale, 15.59 univalents, 2.62 bivalents and 0.08 trivalents for E. shandongensis x S. cereale and 19.63 univalents and 0.65 bivalents for E. semicostatus x S. strictum. A large number of chromosomes were involved in secondary associations. Most pairing between chromosomes of the Elymus St and Y genomes was autosyndetic. The pairing data showed higher pairing (2.02–2.82 bivalents per cell) between the St and Y genomes of Elymus in the presence of the S. cereale genome than in the presence of the S. strictum genome (0.65 bivalents per cell). Moreover, the bivalent frequency in haploid E. pseudonutans (averaging 0.55 bivalents/cell) and in haploid E. shandongensis (averaging 0.69 bivalents/cell) (Lu et al. 1990) was much lower than that in the hybrids of these species with S. cereale. These observations suggest that the genome of S. cereale promotes meiotic pairing of homoeologous chromosomes in Elymus species (Lu et al. 1990).
Lu and von Bothmer (1991) crossed Secale cereale with three polyploid Elymus species, namely, E. caninus (2n = 4x = 28; genome StStHH), E. brevipes (2n = 4x = 28; genome StStYY) and E. tsukushiensis (2n = 6x = 42; genome StStHHYY). Chromosome pairing at first meiotic metaphase in the F1 hybrids included 20.74 univalents and 0.14 bivalents for the triploid E. caninus x S. cereale (genome StHR), 16.35 univalents, 2.17 bivalents and 0.09 trivalents for the triploid hybrid E. brevipes x S. cereale (genome StYR), and 25.84 univalents, 1.10 bivalents and 0.02 trivalents for the tetraploid hybrid E. tsukushiensis x S. cereale (StHYR). Several secondary associations were also observed in the hybrids. The researchers concluded that (1) the homoeologous relationship between “St”, “H” and “Y” genomes in the investigated Elymus species, differ, namely, St is closer to Y than to H; (2) low homoeology exists between genomes of Elymus (either St, H or Y) and rye (R); (3) the Secale genome affects homoeologous chromosome pairing between different genomes in E. brevipes and E. tsukushiensis. This is in accord with earlier findings suggesting that the Secale genome can promote pairing of homoeologous chromosomes (Lelley 1976; Dvorak 1977; Gupta and Fedak 1985, 1987a, b; Lu et al. 1990).
Fedak and Armstrong (1986) produced hybrids between hexaploid Elymus hispidus (2n = 6x = 42; genome EeEeEeEeStSt) and Secale cereale. Mean chromosome pairing at first meiotic metaphase of the hybrid (2n = 4x = 28; genome EeEeStR) included 18.80 univalents, 3.71 bivalents, and 0.56 trivalents. Most of the pairing was autosyndetic. Indicating very low homology between the Elymus genomes (Ee and St) and the R of rye.
Heneen (1963) analyzed mitotic and meiotic behavior of the natural pentaploid hybrid between Elymus arennrius (2n = 8x = 56; genome EeEeEeEeStStStSt) and Secale cereale. The nucleolar organizer of rye was suppressed in this hybrid and no secondary constriction was observed in the short arm of chromosome 1R. Most of the hybrid PMCs (2n = 5x = 35; genome EeEeStStR) had 14 bivalents and 7 univalents. The univalents, which are large in size, represent the 7 chromosomes of rye. Pairing is thus autosyndetic. Various meiotic aberrations and irregularities, including spontaneous chromosome breakage, polyploid cells and plasmodia, occurred frequently in this hybrid (Heneen 1963).
6.4.3 Chromosome Pairing in Hybrids Between Hordeum and Secale Species
Meiotic chromosomal pairing in hybrids between various diploid and polyploid Hordeum species and Secale species was studied by a number of researchers (e.g., Fedak 1979, 1986; Finch and Bennett 1980; Fedak and Armstrong 1981; Thomas and Pickering 1985; Gupta and Fedak 1985, 1987a, b; Lu et al. 1990; Petersen 1991a, b). In all hybrids, pairing between Hordeum and Secale chromosomes was very low, indicating a very distant relationship between the two genera.
Several hybridizations between Hordeum and Secale were performed at the diploid level. Fedak (1979) obtained a diploid hybrid by crossing H. vulgare with S. cereale, and observed very low chromosome pairing, with an average chiasma frequency of 0.22 per cell. Phenotypically, the hybrid resembled rye, the pollen parent, but only the nucleolar organizers of barley were active. Petersen (1991a, b) produced 41 intergeneric hybrids between diploid, tetraploid and hexaploid cytotypes of several Hordeum species and Secale species and analyzed their chromosome pairing at first meiotic metaphase. H. vulgare and H. bulbosum have the same genome (genome H, while H. marinum and H. murinum each have one distinct genome, Xa and Xu, respectively; all other diploid species have the H-genome (Wang et al. 1995). The same four genomes are found in the polyploid species of Hordeum (Table 2.8). Differences between the chromosome sizes of Hordeum and Secale enabled distinction between auto- and allo-syndetic pairing. Allosyndetic pairing between chromosomes of Hordeum and Secale was very rare, indicating very little homology between any of the four basic genomes of Hordeum (H, I, Xa, and Xu) and the R-genome of Secale. Similarly low allosyndetic pairing between Hordeum and Secale chromosomes (0.40 bivalents per cell) was reported in several other diploid Hordeum x Secale hybrids (Thomas and Pickering 1985; Gupta and Fedak 1987a). Very little chromosomal pairing was also observed at first meiotic metaphase of the diploid hybrid H. chilense x Secale cereale (Finch and Bennett 1980). This hybrid combination was also studied by Thomas and Pickering (1985), who observed 12.64 univalents, 0.62 rod bivalents, and 0.02 trivalents per cell. Among the bivalents, there were 0.13 large homomorphic rye-rye bivalents, 0.23 small homomorphic chilense-chilense bivalents, and 0.64 heteromorphic chilense-rye bivalents. Only the nucleolar organizers of H. chilense only were expressed. Gupta and Fedak (1987b) studied chromosome pairing at first meiotic metaphase in the diploid Hordeum califormcum x S. vavilovii (now included in S. cereale) hybrid and observed a mean 11.74 univalents and 1.13 bivalents per cell, most of which (86.7%) were autosyndetic.
Triploid hybrids between tetraploid species of Hordeum and diploid Secale also exhibited very little pairing between the chromosomes of the species of these two genera. Finch and Bennett studied chromosomal pairing at first meiotic metaphase of the triploid hybrid between tetraploid H. jubatum ssp. breviaristatum and S. strictum subsp. africanum. This hybrid had up to six bivalents between H. jubatum chromosomes and almost no pairing between H. jubatum and Secale chromosomes (Finch and Bennett 1980). These results are in accord with previous reports of hybridization between S. cereale and H. jubatum (Quincke 1940; Brink et al. 1944; Wagenaar 1959). Brink et al. (1944) and Wagenaar (1959) typically found five to six bivalents between jubatum chromosomes in the triploid hybrid, while the S. cereale chromosomes were mostly univalents. However, several autosyndetic bivalent and multivalent associations between the rye chromosomes, as well as some allosyndetic associations with H. jubatum chromosomes, were also seen in this triploid hybrid. The fairly strong autosyndesis displayed by the H. jubatum chromosomes is due to the two closely related genomes of the tetraploid H. jubatum. Similar results were obtained by Schlegel et al. (1980), who studied meiotic chromosomal pairing in the triploid hybrid Hordeum jubatum x S. kuprijanovii (now included in S. Strictum subsp. Strictum) and found that, apart from barley-barley and rye-rye, homoeologous barley-rye chiasmatic associations were also evident in about 1% of the PMCs.
Studies of chromosome pairing at first meiotic metaphase in the triploid hybrid H. parodii (4x) x S. anatolicum (included now in S. strictum subsp. strictum) showed a mean 14.74 univalents, 6.31 bivalents, 0.22 trivalents and 0.02 quadrivalents (Gupta and Fedak 1987b). Most pairing was attributed to autosyndetic among Hordeum chromosomes and among several Secale chromosomes. The scarcity of allosyndetic pairing in the form of heteromorphic bivalents between Secale large and barley small chromosomes, indicated a distant relationship between the parental genomes. In addition, in the triploid hybrid H. depressum (4x) x S. cereale, Morrison and Raihathy (1959) reported mean chromosomal pairing of 1.7 bivalents per cell, mostly between H. depressum chromosomes. They decided that there is no homology between the genomes of H. depressum and S. cereale. Studies in a triploid hybrid between tetraploid H. marinum ssp. gussoneanum and S. cereale, Staat et al. (1985) reported a frequency of 0.02 heteromorphic bivalents per cell. Hence, the triploid hybrids described above exhibited a strong preferential pairing between the two genomes of Hordeum, whereas heteromorphic bivalents involving Hordeum and Secale chromosomes were very rare.
Similar results were obtained in hybrids with higher ploidy level. The tetraploid hybrid H. lechleri (6x) x S. cereale had 0.30–0.56 heteromorphic rod bivalents per cell (Fedak and Armstrong 1981) and the trigeneric hybrid containing the genomes of Triticum aestivum, Hordeum chilense and Secale cereale showed similar low allosyndetic pairing (Fernández-Escobar and Martin 1989).
Preferential intragenomic chromosome pairing, involving Hordeum-Hordeum chromosomes, indicated by the presence of homomorphic small bivalents, and Secale-Secale chromosomes, indicated by the presence of homomorphic large bivalents, prevails in the diploid hybrids (Gupta and Fedak 1987a, b; Petersen 1991b). Autosyndetic intergenomic pairing among Hordeum chromosomes occurred in the hybrids involving polyploid species of Hordeun and Secale. In hybrids with S. cereale, the polyploids H. brachyantherum, H. jubatum, H. lechleri, H. arionicum, H. prorerum, H. capense, and H. secalinum exhibited a number of bivalents resulting from autosyndetic pairing. In general, the level of autosyndetic pairing among the Hordeum chromosomes was higher in the intergeneric combinations with S. cereale than in the corresponding Hordeum polyhaploids. It was therefore concluded that the S. cereale genome promotes homoeologous chromosome pairing between the genomes of Hordeum (Gupta and Fedak 1985). S. cereale promoted more homoeologous pairing than S. strictum subsp. africanum (Gupta and Fedak 1985). This is in accord with the finding of Lu et al. (1990), who noted a differential effect of the two Secale genomes on chromosome pairing; while S. cereale promoted homoeologous pairing in hybrids with Elymus semicostatus, S. strictum subsp. strictum did not promote such pairing.
Haploids of Hordeum vulgare were recovered at a frequency of less than 1% from pollinations of five strains of H. vulgare with cultivar Prolific of S. cereale (Gupta and Fedak 1987b). This is the first report of barley haploids obtained from barley x rye crosses. Preliminary studies suggest that haploids arose through a process of elimination of rye chromatin in the seedlings.
6.4.4 Chromosome Pairing in Hybrids Between Aegilops Species and Secale Species
The nucleolar organizer activity in several allopolyploid Aegilops species (Ae. triuncialis, Ae. variabilis, Ae. biuncialis, Ae. juvenalis) x S. cereale F1 hybrids was analyzed using a highly reproducible silver-staining procedure (Cermeño and Lacadena 1985). All the Aegilops allopolyploids share the U subgenome that derived from the diploid species, Ae. umbellulata. The Aegilops 1U and 5U chromosomes showed strong nucleolar activity, which suppressed the NOR activity of the 1R rye chromosome in all the hybrid combinations. Low activity of the nucleolar-organizer chromosomes of the other subgenomes of the allopolyploid Aegilops parents, namely, C, Sv, Mo, and DcXc, was also observed. These findings confirm earlier reports of predominant nucleolar-organizer activity of the 1U and 5U chromosomes and the suppression of the NOR activity of 1R chromosome from rye.
Several early investigations on chromosomal pairing in F1 hybrids between Aegilops and Secale were reported (von Berg 1931; Kagawa and Chizaki 1934; Karpechenko and Sorokina 1929; Kihara 1937). Because the chromosomes of Secale are larger than those of Aegilops, the parental members of the paired chromosomes can be identified at first metaphase of meiosis in the F1 hybrids. This facilitated easy identification of the wheat and rye chromosomes. A low level of chromosome pairing between Aegilops and Secale chromosomes has been reported in the intergeneric F1 hybrids between both diploid and tetraploid Aegilops species and S. cereale (Karpechenko and Sorokina 1929; von Berg 1931; Kagawa and Chizaki 1934; Melnyk and Unrau 1959; Majisu and Jones 1971).
Majisu and Jones (1971), using embryo culture, produced diploid hybrids between species of Secale and four diploid species of Aegilops section Sitopsis and Amblyopyrum muticum. Studies of chromosomal pairing at first meiotic metaphase of these hybrids showed that most Aegilops and Secale chromosomes were univalents, but some paired as normal chiasmatic bivalents. The pairing data suggested that the Secale species genome shows very little homology with the genomes of the Aegilops species (Majisu and Jones 1971). Likewise, there is no evidence that the chromosomes of Secale are homologous with those of another group of Aegilops diploid species, namely, Ae. caudata, Ae. comosa and Ae. umbellulata (Hutchinson et al. 1980), but does not preclude the presence of homologous segments between these species.
Crosses between Ae. squarrosa (currently Ae. tauschii), the donor of the D subgenome to hexaploid wheat, and S. cereale, were performed by several researchers (e.g., Melnyk and Unrau 1959; Kawakubo and Taira 1992; Su et al. 2015). Due to their large size, the chromosomes of S. cereale were easily distinguished from those of Ae. tauschii, and therefore, all observed heteromorphic bivalents were considered to be due to allosyndetic pairing between Rye and Aegilops chromosomes. Melnyk and Unrau (1959) observed chromosomal pairing with an average of 9.67 univalents, 1.61 rod-bivalents, 0.01 ring bivalents, 0.25 trivalents and 0.05 quadrivalent in the hybrid Ae. squarrosa var. typica x S. cereale (genome DR). Only 0.4% of the bivalents were formed by Secale-Aegilops pairing, and trivalents were composed of 1 or 2 cereale chromosomes, indicating that the chromosomes of these two species are distantly homoeologous but still capable of some intergeneric pairing.
Su et al. (2016) produced and analyzed hybrids from crosses of Ae. tauschii and S. cereale. The hybrids showed an average meiotic pairing configuration of 10.84 univalents, 1.57 bivalents and 0.01 trivalents. Genomic in situ staining revealed three types of bivalent associations, namely, D-D, R-R and D-R, at frequencies of 8.6, 8.2 and 83.3%, respectively. Trivalents consisting of D-R-D and of R-D-R associations were also found. These results suggested that both intra- and intergenomic chromosome homology contribute to chromosome pairing.
Kawakubo and Taira (1992) produced hybrid plants with different combinations of D and R genomes, by crossing Ae. tauschii (2x and 4x) and Secale cereale (2x and 4x). Amphidiploids were obtained directly from the cross between tetraploid parents. Diploid and triploid hybrids were completely seed-sterile, whereas the amphidiploid had an average self-fertility of 4.5%, ranging between 0 and 45%. At first meiotic metaphase, the mean chromosome associations included 13.4 univalents, 0.26 bivalents and 0.01 trivalents in the diploid hybrids, 7.1 univalents and 6.96 bivalents in the triploid hybrids, and 7.9 univalents and 10.5 bivalents in the amphidiploids. In diploids, end-to-end type pairing between D and R chromosomes was observed, presumably without chiasmata. Homologous pairing between D chromosomes was predominant in plants bearing two sets of D genomes, and homoeologous D-R pairing was scarcely observed in either triploids or amphidiploids.
The conclusion that there is very little homology between Aegilops and Secale chromosomes was also supported by the pattern of meiotic pairing in the triploid hybrid between synthetic autotetraploid Ae. tauschii and S. cereale (Majisu and Jones 1971). No trivalents were observed in the triploid hybrid, and bivalent formation was restricted to Ae. tauschii chromosomes, with the Secale chromosomes occurring as univalents.
Meiotic pairing behavior in hybrids generated between Aegilops and S. cereale was examined by in situ hybridization, using a 480-bp repeat probe, purified by Bedbrook et al. (1980), which is specific to rye and absent from Aegilops species, thus enabling the rye chromosomes to be clearly identified (Hutchinson et al. 1980). It was shown that in diploid hybrids between Ae. caudata or Ae. comosa and S. cereale, the small amount of pairing was mostly of the allosyndetic, Aegilops-rye type, although some autosyndetic associations also occurred. The two diploid hybrids showed a similar level of pairing, which, although fairly low, was slightly higher than previously reported (e.g., Majisu and Jones 1971). Hutchinson et al. (1980) concluded that the Aegilops chromosomes are more likely to pair with Secale chromosomes in diploid Aegilops x Secale hybrids, than with other Aegilops chromosomes in inter-genomic crosses. This suggests that there is partial homology between Secale and Aegilops chromosomes, and lies in agreement with the conclusions reached by Melnyk and Unrau (1959) based on studies of the meiotic pairing between Ae. tauschii and S. cereal, but contradicted the results of Majisu and Jones (1971). It should be pointed out, however, that the overall level of pairing obtained in the experiments of Majisu and Jones (1971) was lower than that reported by Hutchinson et al. (1980), and may reflect a lower level of allosyndetic pairing in the tested material. Yet, in the triploid hybrid between Ae. columnaris (4x; genome UUXnXn) and S. cereale, pairing and chiasma formation was largely limited to chromosomes of the two Aegilops subgenomes. This suggests that, as expected, the Ae. columnaris genomes U and Xn are more closely related to each other than they are to the R genome of S. cereale (Hutchinson et al. 1980).
Lucas and Jahier (1988) conducted a diallel crossing program, which included ten diploid species from the genera Triticum, Aegilops, Dasypyrum and Secale. Forty-one different interspecific hybrids were analyzed in this program. The number of associations between chromosome arms at first meiotic metaphase of the F1 hybrids was taken as an indication of the degree of homology between the parental genomes. Lucas and Jahier (1988) found little affinity between the genomes of Triticum or Aegilops and S. cereale, and concluded that S. cereale and Dasypyrum villosum are only distantly related to the Triticum and Aegilops species.
Chromosomal pairing at first meiotic metaphase of Ae. ovata (currently Ae. geniculata; 2n = 4x = 28; genome MoMoUU) x S. cereale triploid hybrid, was studied by several researchers (e.g., Leighty et al. (1926), Kagawa and Chizaki (1934), Khalilov and Kasumov (1989), Sechnyak and Simonenko (1991), Cuñado (1992) and Wojciechowska and Pudelska (2002). The studies showed a pairing frequency ranging from 0.40 to 0.86 for rod bivalents (Wojciechowska and Pudelska 2002) to 2–3 for rod bivalents (Kagawa and Chizaki 1934), 1.46 rod and 0.3 ring bivalents, 0.12 trivalents (Sechnyak and Simonenko (1991) and to 1–5 rod bivalents and 1 trivalent (Khalilov and Kasumov 1989). Cuñado (1992) crossed Ae. uniaristata (2x) with S. cereale and observed 0.38 rod bivalents per cell at meiosis. Using the C-banding technique, he was able to discern between autosyndetic Aegilops–Aegilops pairing (0.11 rod bivalents per cell), autosyndetic rye-rye pairing (0.04 rod bivalents per cell) and allosyndetic Aegilops-rye pairing (0.23 rod bivalents per cell). Cuñado (1992) also crossed several allotetraploid and allohexaploid Aegilops species with S. cereale and, using C-banding technique, found relatively little allosyndetic pairing between Aegilops and rye chromosomes (from 0.04 rod bivalents/cell in Ae. ventricosa x S. cereale to 0.30 rod bivalents/cell in Ae. triuncialis x S. cereale). On the other hand, the autosyndetic pairing between Aegilops-Aegilops chromosomes in hybrids with the allotetraploid Aegilops, ranged from 2.01 rods in Ae. geniculata x S. cereale to 6.59 in Ae. cylindrica x S. cereale. In hybrids with the allohexaploid Aegilops, it ranged from 4.41 rods in Ae. juvenalis x S. cereale to 8.77 rods in Ae. crassa x S. cereale. Autosyndetic pairing between rye-rye chromosomes also occurred in low frequency. Clearly, very little homoeologous pairing occurred between the R genome of S. cereale and the genomes of the polyploid Aegilops species. The pairing data indicate that subgenomes of the allopolyploid Aegilops species are much closer to each other than to the R genome of S. cereale.
Gupta and Fedak (1985) studied meiosis in hybrids between allohexaploid Ae. crassa (2n = 6x = 42; genome DcXcD) and species of Secale. Their results provide evidence that promotion of homoeologous pairing was observed in these hybrids. The increase in pairing mainly affected autosyndetic Aegilops–Aegilops pairing (Gupta and Fedak 1985). They concluded that a meiotic pairing control system that promotes homoeologous pairing operates in Ae. crassa. Different levels of homoeologous pairing were obtained in hybrids of 6x Ae. crassa x Secale species, depending on the rye DNA and C-heterochromatin content. For instance, the S. strictum genotype suppressed the function of this system in a manner that was inversely related to its heterochromatin content and total DNA content. Similar effects were observed in S. cereale x wheat and S. cereale x Ae. ventricosa hybrids, where C-heterochromatin appeared to affect homoeologous pairing involving both the chromosome arms carrying it as well as also involving other chromosomes (Gustafson 1983; Cuñado et al. 1986).
6.4.5 Chromosome Pairing in Hybrids Between Triticum and Secale Species
The first attempt to cross wheat with rye was made by the Scottish botanist A. Stephen (Wilson 1876), who pollinated common wheat with S. cereale pollen. The resulting hybrid plants were sterile. Wilson presented his results on April 8, 1875, in a communication to the Botanical Society of Edinburgh. His attempt inspired, the American plant breeder Elbert S. Carmann, who also obtained a sterile hybrid from a cross between common wheat and rye (Carman, E. S.: Rural New Yorker, August 30, 1884). Later on, in 1888, the German plant breeder Wilhelm Rimpau, crossed common wheat with S. cereale and obtained several sterile and one fertile hybrid. The fertile hybrid presumably originated from a spontaneous chromosome doubling, thus producing the first octoploid Triticale, which yielded fertile progeny (Rimpau 1891). In 1921, the Russian plant breeder G. K. Meister, observed spontaneous pollinations of wheat plants with rye pollens from neighboring breeding plots (Meister 1921). Since these pioneering attempts in the end of the nineteenth century and beginning of the twentieth one, that aimed mainly to transfer cold hardiness from rye to wheat, numerous hybridizations between Triticum species and Secale species have been produced and their chromosome behavior at meiosis has been analyzed. In most cases, the allohexaploid T. aestivum was used, whereas in a minority of cases, several subspecies of the allotetraploid wheat, T. turgidum, were crossed with Secale species.
6.4.5.1 Chromosome Pairing in Hybrids Between Diploid Wheat and Secale Species
Very few successful hybridizations involving diploid wheat and Secale species were reported. For example, Lucas and Jahier (1988) did not obtain viable hybrids when they crossed diploid wheats, T. urartu and wild T. monococcum with S. cereale. One of these crosses was performed by Sodkiewics (1982) who observed during meiosis of the diploid hybrid of domesticated T. monococcum (genome AmAm) x S. cereale little affinity between chromosomes of these two species.
6.4.5.2 Chromosome Pairing in Hybrids Between Tetraploid Wheat and Secale Species
Longley and Sando (1930) produced hybrids between wild emmer wheat, Triticum turgidum subsp. dicoccoides, the progenitor of domesticated T. turgidum (2n = 4x = 28; genome BBAA), and S. montanum (currently S. strictum), and found a mean 0–1 bivalent pair/cell at first meiotic metaphase in the triploid hybrid (genome BAR). In the same year, Plotnikowa (1930), Aase (1930), Oehler (1931), and Vasiljev (1932), produced hybrids from the crosses of domesticated T. turgidum, ssp. durum and ssp. persicum, with S. cereale. In all these triploid hybrids (genome (BAR) pairing was scarce (0–4 bivalents/cell). Kagawa and Chizaki (1934) observed 0–5 bivalents in the ssp. durum x S. cereale hybrid, and Liljefors (1936) observed somewhat higher pairing (0–6 bivalents and rare trivalents and quadrivalents) in the T. turgidum ssp. turgidum x S. cereale hybrid. Nakajima (1955) crossed T. turgidum subsp. polonicum with S. strictum subsp. africanum and observed 0–3 bivalents at meiosis, most of which resulted from autosyndesis between the chromosomes of BA genomes of ssp. polonicum. Nakajima (1956a) analyzed the F1 hybrid progeny of the cross between domesticated emmer, T. turgidum subsp. dicoccon and S. vavilovii (currently included in S. cereale subsp. ancestrale). The hybrid resembled domesticated emmer in most traits, rather than being an intermediate between the two parents. Chromosomal pairing at first meiotic metaphase included 13–21 univalents/cell and 0–4 bivalents/cell. The bivalents were rod-, and rarely, ring-shaped and homomorphic, indicating autosyndesis of the Triticum B and A subgenome chromosomes.
Giorgi and Cuozzo (1980) crossed S. cereale with the ph1c mutant line of durum wheat cv. Cappelli, which has a deficiency of a segment on chromosome arm 5BL that includes the Ph1 locus, and thus, enables high homoeologous pairing in wheat hybrids. In meiosis of the F1 hybrid, an average of 11.4 univalents, 4.3 bivalents and 0.3 trivalents were observed per cell which is much higher count than that of the control hybrid Cappelli x rye possessing Ph1, in which only 0.36 bivalents per cell were observed (Giorgi and Cuozzo 1980). The increase in chromosome pairing, consequent to the absence of Ph1, was mainly due to autosyndetic pairing between the wheat B and A genome chromosomes. Relatively low pairing between wheat and rye chromosomes was also inferred from the frequency and size of the trivalents. Thus, the deficiency of Ph1 only slightly increased the pairing between durum and cereale chromosomes.
All the hybrids between the subspecies of T. turgidum and S. cereale were completely sterile. In rye, there are only two flowers in each spikelet whereas in T. turgidum there are always more than two flowers. The average number of flowers in the hybrids was greater than 4, indicating dominance of a larger number of flowers per spikelet (Müntzing 1935). However, rye was dominant in determination of the number of spikelets per ear; the number of spikelets for rye, T. turgidum and F1 was 31.6, 20.4 and 31.5, respectively (Müntzing 1935).
Naranjo (1982) analyzed meiotic pairing in the tetraploid hybrid (genome BARR) generated from hexaploid Triticale (2n = 6x = 42; genome BBAARR) and S. cereale (genome RR) and found that, in addition to the homologous pairing between chromosomes of the two R genomes, homoeologous pairing took place preferentially between homoeologous chromosomes of group 1. 1A–1R associations were more frequent than 1B–1R associations, although, in both cases, pairing was mostly restricted to the long arms. In tetraploid wheat and rye hybrids, most of the wheat-rye homoeologous pairing was restricted to chromosomes 1RL/1BL or 1AL and 1DL, at low frequency (Naranjo 1982).
6.4.5.3 Chromosome Pairing in Hybrids Between Hexaploid Wheat and Secale Species
Most crosses between hexaploid Triticum and Secale have been made between common wheat, T. aestivum subsp. aestivum (genome BBAADD) and S. cereale. Longley and Sando (1930) reported the presence of 28 univalents and zero bivalents in such tetraploid hybrids (genome BADR). Kihara (1924), Thompson (1926), and Aase (1930), also observed very little pairing in hybrids between bread wheat and S. cereale (0–3 bivalents/cell), whereas Bleier (1930) and Kattermann (1934) observed somewhat more pairing (0–4 to 0–6 bivalents/cell). Hybrids with S. strictum subsp. strictum as parent exhibited similar results. In the hybrid of T. aestivum subsp. aestivum, x S. strictum subsp. strictum, Longley and Sando (1930) observed 0–1 bivalents/cell and in the hybrid T. aestivum subsp. spelta x subsp. strictum, they reported 0–3 bivalents/cell. In the latter hybrid, Aase (1930), Kagawa and Chizaki (1934), and Nakajima (1956b) observed 0–4 bivalents, whereas, in subsp. spelta x S. strictum subsp. africanum, Nakajima (1956b) observed 0–5 bivalents/cell. In the hybrid T. aestivum subsp. compactum x S. cereale, Kagawa and Chizaki (1934) observed 0–3 bivalents. The number of occasional bivalents observed in all these hybrids did not exceed that seen in haploids of common wheat. Therefore, they may be regarded as a result of autosyndesis between wheat-wheat chromosomes, and not as an indication of homology between wheat and rye chromosomes. The rye genome (R) is, therefore, not close to the A, B or D subgenomes of allohexaploid wheat (Thompson 1931).
Megyeri et al. (2013) studied chromosome pairing in first meiotic metaphase of bread wheat-rye F1 hybrids, using sequential genomic and fluorescent in situ hybridization techniques. These methods enabled both discrimination of wheat and rye chromosomes, and identification of the individual wheat and rye chromosome arms involved in the chromosome associations. Mean chromosomal pairing at first meiotic metaphase of this hybrid included 25.74 univalents, 1.07 rod bivalents, 0.012 ring bivalents and 0.025 trivalents/cell. The majority of associations (93.8%) were observed between the wheat chromosomes, 5.2% between wheat and rye chromosomes and 1.0% between rye chromosomes (Megyeri et al. 2013). The largest number of wheat-wheat chromosome associations (53%) was detected between the A and D subgenomes, while the frequency of B-D and A-B associations was significantly lower (32% and 8%, respectively). Among the A-D chromosome associations, pairing between the 3AL and 3DL arms was observed at the highest frequency, while 3DS-3BS was the most frequent of all chromosome associations (0.113/cell). Pairing between the A and B chromosomes was found rarely, with 2AL and 2BL displaying the highest pairing affinity (pairing frequency was 0.011). Only four wheat chromosome arms (4AS, 5AL, 6BL, and 4DS) did not pair with other chromosome arms in the examined cells (Megyeri et al. 2013). Pairing between wheat and rye chromosomes was low. The frequency of A-R associations was 0.007, of B-R was 0.015 and of D-R was 0.015.
Megyeri et al. (2013) reported similar levels of wheat-wheat chromosome pairing in the wheat x rye hybrid and in the haploid of common wheat (Jauhar et al. 1991), suggesting that the S. cereale genome does not significantly influence the pairing of wheat-wheat chromosomes in the hybrid (as discussed below).
Hutchinson et al. (1983), using the C-banding technique, studied meiotic chromosomal pairing in hybrids between bread wheat cv. Chinese Spring aneuploids (nulli 3A-tetra 3B and nulli 5B tetra 5D), and S. cereale. The hybrids lacking chromosome 3A or 5B, displayed higher pairing than that observed in hybrids between euploid Chinese Spring and S. cereale. Pairing was more frequent between A and D subgenome chromosomes than between chromosomes of A or D subgenome and those of B subgenome and between B subgenome and R genome chromosomes.
Miller et al. (1994) used genomic in-situ hybridization (GISH) to compare the amount of wheat-rye chromosome pairing in Triticum aestivum x Secale cereale hybrids bearing the 5B chromosome (a), versus hybrids lacking the 5B chromosome (b) or those in which it was replaced by an extra dose of chromosome 5D (c). The mean number of chromosome arm associations per PMC in the three hybrid genotypes was as follows: (a) W-W 0.48, W-R 0.08, R-R 0.02 and total 0.58; (b) W-W 5.11, W-R 0.43, R-R 0.07 and total 5.61; and (c) W-W 4.19 (not including the 5D bivalent), W-R 0.18, R-R 0.04 and total 4.41. As expected, both of the chromosome 5B-deficient hybrid genotypes showed significantly higher pairing than the euploid wheat hybrid. The increase in pairing due to the absence of chromosome 5B was mainly between the wheat chromosomes, with much less between wheat and Secale and almost none between the Secale chromosomes.
In order to further establish the arm homoeology of common wheat and S. cereale chromosomes, Naranjo et al. (1987) studied chromosomal pairing at first meiotic metaphase in three different bread wheat (Chinese Spring) x S. cereale hybrid combinations (either bearing both 5B and 3D, 5B-deficient and 3D-deficient). The majority of individual wheat chromosomes and their arms, as well as the arms of chromosomes 1R and 5R, were identified by means of C-banding. Chromosome arm 1RL paired with 1AL, 1BL and 1DL, while 5RL was homoeologous to 5AL and partially homoeologous to 4AL and 4DL. It was thus concluded that 5RL carries a translocated segment from 4RL (see Devos et al. 1993).
Chromosome pairing at first meiotic metaphase in hybrids between bread wheat and rye, bearing the ph1b mutation in bread wheat, were analyzed by Naranjo and Fernández-Rueda (1991, 1996), in efforts to establish the frequency of pairing between individual chromosomes of wheat and rye in the absence of the homoeologous pairing suppressor, Ph1. Diagnostic C-bands and other cytological markers, such as telocentrics or translocations, were used to identify each one of the rye chromosomes and wheat arms. Both the amount of telomeric C-heterochromatin and the structure of the rye chromosomes relative to wheat affected the level of wheat-rye pairing. The degree to which rye chromosomes paired with their wheat homoeologues varied with each of the three wheat subgenomes. In most homoeologous groups, the B-R association was more frequent than the A-R and D-R associations. Recombination between arms 1RL and 2RL and their wheat homoeologues possessing a different telomeric c-banding pattern, was detected and quantified at first anaphase. The frequency of recombinant chromosomes obtained supports the premise that recombination between wheat and rye chromosomes may be estimated from wheat-rye pairing patterns.
Cuadrado et al. (1997) performed fluorescence in situ hybridization (FISH), with multiple probes, to meiotic chromosome spreads derived from hybrid plants of the bread wheat ph1b mutant, i.e., has a deficiency of a region on chromosome arm 5BL that includes the Ph1 gene, x S. cereale. Homoeologous pairing was expected to be increased due to the absence of Ph1. The probes used allowed for unequivocal identification of all of the rye and most of the wheat chromosomes, in both unpaired and paired configurations. Thus, it was possible to identify the pairing partners and to determine the frequency of wheat-wheat and wheat-rye associations. Most of the wheat-rye pairs, which averaged about 7–11% of the total pairs detected in the hybrids, involved B subgenome chromosomes (about 70%), and to a much lesser degree, D (almost 17%) and A (14%) subgenome chromosomes. In these pairs, rye arms 1RL and 5RL showed the highest pairing frequency (over 30%), followed by 2RL (11%) and 4RL (about 8%), and much lower values for all the other arms. 2RS and 5RS were never observed in pairings in the analysed sample. Chromosome arms 1RL, 1RS, 2RL, 3RS, 4RS and 6RS were exclusively bound to wheat chromosomes of the same homoeologous group. The opposite was true for 4RL, which paired with 6BS and 7BS and for 6RL, which paired with 7BL. 5RL, on the other hand, paired with 4WL arms or segments, in more than 80% of the cases, and with 5WL in the remaining 20% of pairings. Additional cases of pairings involving wheat chromosomes belonging to more than one homoeologous group, occurred with 3RL, 7RS and 7RL. These results support previous evidence (Naranjo and Fernández-Rueda 1991; Devos et al. 1993) of the existence of several translocations in the rye genome relative to that of wheat.
Meiotic pairing in euploid rye-triticale hybrids (2n = 4x = 28; genome BARR) was compared with that of three hypo-aneuploid BARR hybrids, two with 2n = 26 chromosomes and one with 2n = 27, also obtained from the triticale x S. cereale cross (Naranjo and Palla 1982). The aneuploid with 2n = 27 chromosomes was identified, by C-banding, as mono-5R; its meiotic pairing indicated that chromosome 5R of S. cereale is a strong promoter of homologous rye pairing and is also able to influence homoeologous wheat chromosome pairing. The results show that the application of hypo-aneuploidy compensated by homoeologous chromosomes, is useful in the study of genetic control of meiotic pairing in diploid species.
The ability to promote and suppress homologous and homoeologous chromosomal pairing in wheat x rye hybrids by S. cereale genes, is an important question and has been investigated by several researchers. Miller and Riley (1972), Naranjo et al. (1979), Jouve et al. (1980) Naranjo (1982) reported that hybrids between tetraploid or hexaploid wheat and rye bearing an extra dose of the rye R genome, resulting in hybrid genomes of BARR or BADRR, displayed higher homoeologous pairing between the chromosomes of the wheat subgenomes than in hybrids with a single R genome. A dosage effect of rye genomes on homoeologous pairing has also been shown by comparing BARR, BARRR, BADR combinations; however, BADRR hybrids frequently showed lower homoeologous wheat-rye pairing than BADR (Naranjo 1982). Similar results have been obtained by comparing Hordeum-Secale hybrids with bearing various genome ratios (Gupta and Fedak 1985). Thus, it appears that not only the number of rye genomes but also depending, at least partly, on rye DNA and C-heterochromatin, the genome ratio can affect the extent of homoeologous pairing. Naranjo et al. (1979) also noted an effect of rye promoters on homologous pairing between tetraploid and hexaploid wheat chromosomes of genomes BBAA in hybrids (genome BBAADRR) between hexaploid (genome BBAARR) and octoploid (genome BBAADDRR) triticale.
The increased homoeologous pairing in these hybrids has been explained by Cuñado et al. (1986), as an inhibition of the effect of a single dose of the Ph1 locus on chromosome 5B by two or more doses of chromosome 5R (Jouve et al. 1980). However, Miller and Riley (1972) ascribed the promotion of homoeologous chromosome pairing by the rye genotypes to the activities of the complete genome and not necessarily to the homoeologous group 5 chromosome. It seems clear that the rye genome may modulate the wheat homologous and homoeologous pairing in wheat x rye hybrids, but the mechanism of this control is unknown; further studies combining genomes in different doses are still required.
Studies performed by Lelley (1976), Dvorak (1977), Romero and Lacadena (1982) and Cuadrado and Romero (1984), in bread wheat x rye hybrids with one dose of the R genome, provided evidence of the possible existence of rye pairing promoting and suppressing gene(s) affecting both wheat-wheat and wheat-rye pairing (Dvorak 1977). These findings are in contrast to those of Megyeri et al. (2013), who reported that the S. cereale genome does not significantly influence wheat-wheat chromosomes pairing in the hybrid. The promotion of homoeologous pairing is greater in wheat-wheat than in wheat-rye homoeologous pairing. However, significant variation of wheat-rye pairing frequencies has been detected in different genotypes with the same genome constitution (Naranjo et al. 1979; Naranjo and Palla 1982).
Evidence for the existence of variation in the effect of such genes on homoeologous pairing among Secale taxa, was obtained by Cuadrado and Romero (1984). They analyzed meiotic pairing in wheat x rye hybrids obtained by crossing T. aestivum cv. Chinese Spring (CS) with two cultivars of S. cereale subsp. cereale (Elbon and Ailés) and S. vavilovii (currently included in S. cereale subsp. ancestrale). The results showed that the level of homoeologous pairing in hybrids was affected by the genotype of the rye cultivar used. The CS x S. cereale cv. Elbon hybrids exhibited fewer pairing (0.27 mean bivalents/cell) than T. aestivum haploids, CS x S. vavilovii hybrids had a similar number of bivalent pairings than did bread wheat haploids, and CS x S. cereale cv. Ailés hybrids had more pairings (0.44 mean bivalents/cell) than haploids of common wheat. Consequently, Cuadrado and Romero (1984) assumed that rye cultivar Ailés possesses genes that promote homoeologous pairing in hybrids with common wheat, while cv. Elbon possesses suppressor(s) of such pairing. The hybrids generated with S. cereale cultivars, that are allogamous, displayed much greater variation in the amount of pairing than hybrids with S. vavilovii, which is an autogamous taxon. This variation was interpreted by Cuadrado and Romero (1984) as being due to the different effect of the rye genotypes on the homoeologous pairing in relation with the reproductive systems (allogamy or autogamy) of the particular rye.
Similar evidence was obtained by Gupta and Fedak (1986) who studied the effect of two rye cultivars on chiasmata frequency in bread wheat-rye hybrids. Chiasmata frequencies ranging from 0.07 to 10.40 per cell were recorded in hybrid plants derived from the cross of bread wheat x F1 between two cultivars of S. cereale (Gupta and Fedak 1986). These included one group of plants from the cross Triticum aestivum ‘Chinese Spring’ x Secale cereale F1 (‘Petkus’ x ‘Prolific’) and another group from the cross ‘Chinese Spring’ x F1 (‘Prolific’ X ‘Puma’). These hybrids used to study the inheritance of genetic variation in rye affecting homoeologous chromosome pairing. In the progeny of the cross ‘Chinese Spring’ x Secale cereale F1 (‘Petkus’ x ‘Prolific’) segregation for major genes affecting pairing was evident, since a bimodal distribution was observed and chiasmata frequencies ranging from 6.11–10.40 and 3.0–6.0 chiasmata/cell. In the second cross involving F1 rye plants derived from ‘Prolific’ x ‘Puma’, a smaller-sample hybrids gave a continuous distribution of chiasmata with a single mode, and the chiasmata frequency never exceeded 2.70/cell. Gupta and Fedak (1986) concluded that the genetic system in ‘Petkus’ differs from that in ‘Puma’, and that both genes with major effects and minor effects on chromosome pairing, may be simultaneously present in different cultivars of rye. This could be due to a difference in genetic systems found in ‘Puma’ and ‘Petkus’, since ‘Prolific’ was a common parent in both crosses.
Direct involvement of rye chromosomes in homoeologous pairing is very low in wheat-rye hybrids (Hutchinson et al. 1983) and in Aegilops-rye hybrids (Gupta and Fedak 1985; Cuñado et al. 1986). Miller and Riley (1972) stated that rye chromosome arm 5RL, like 5BL of wheat, suppresses homoeologous pairing. But pairing analysis of hybrids involving disomic and monosomic substitution individuals of bread wheat, in which chromosome 5B of hexaploid wheat is replaced by the long arm of chromosome 5R of rye x Aegilops peregrina, quantitatively demonstrated that chromosome 5RL lacks the pairing regulator gene of chromosome 5BL. Lelley (1976), Cuadrado and Romero (1984), and Gupta and Fedak (1985) suggested that a polygenic system in rye that affects homoeologous pairing. The involvement of major genes was also suggested by Gupta and Fedak 1985).
Orellana et al. (1984) studied meiosis in wheat-rye addition and substitution lines and suggested that S. cereale and bread wheat chromosomes affect each other’s homologous pairing. They also found that chromosomes 5R and 3R are pairing suppressors and that the effect of 5R in the decrease of wheat chromosome pairing was the strongest and that of 3R the weakest. Gupta and Fedak (1986) studied the effect of individual rye chromosomes on meiotic homologous pairing in hybrids between hexaploid and tetraploid wheat, as well as the effect of loss of specific heterochromatin blocks on meiotic pairing in these hybrids. In the pentaploid hybrids between tetraploid wheat, Triticum turgidum subsp. turgidum cv. ‘Ma’, and T. aestivum cv. ‘Chinese Spring’, an average 10.30% reduction in chiasmata frequency was observed, while addition lines with rye chromosome 6R reduced chiasmata frequencies only by an average of 7.4%. Hybrids involving the 4R-bearing rye addition line showed a 25.04% reduction in chiasmata frequency. Hence, chromosome 6R promotes homologous pairing and 4R suppresses such pairing in these hybrids. Chromosome 2R was also found to impart a promotional effect on chromosome pairing (Gupta and Fedak 1986). Telomeric heterochromatin of 7RL did not influence homologous pairing in the pentaploid hybrids while a slight increase in chiasmata counts was observed upon loss of telomeric 6R heterochromatin.
Riley and Law (1965) reported more pairing in a nulli-5B haploid of T. aestivum as compared to the hybrid between nulli-5B of T. aestivum and S. cereale, and suggested that the rye genotype has a suppressing influence on chromosome pairing similar to that of chromosome 5B. However, Bielig and Driscoll (1970) showed that chromosome 5R of S. cereale did not compensate for the absence of chromosome 5B, indicating that it does not carry a homoeologous pairing suppressor.
The number of genes transferred from rye to wheat in breeding programs is usually small despite the amount of homoeologous pairing observed in bread wheat x S. cereale hybrids, indicating that there is a discrepancy between pairing and recombination in these hybrids. Since insufficient data are available on the relationship between wheat-rye homoeologous pairing and wheat-rye recombination in such hybrids, Orellana (1985) was able to distinguish between three types of wheat-rye associations (end-to-end extremely distal, end-to-end distal and interstitial) between homoeologous chromosomes at different first meiotic metaphase stages (early, middle and late) by analyzing telomeric C-bands. In addition, he estimated the actual recombination frequencies for such associations at first anaphase of wheat-rye hybrids. In all plants analyzed, only open bivalents were found. There was a decrease in the frequency of the end-to-end associations during first metaphase progressed, whereas the number of interstitial associations remained without significant change in all metaphase stages. Assuming a maximum of one chiasma per bond, a good correlation was found between the frequencies of interstitial associations at metaphase and the number of recombinant chromosomes at anaphase. In addition, rye-rye homologous pairing was observed at metaphase, but no evidence for rye-rye recombination was found at anaphase. Moreover, wheat-rye hybrids lacking chromosome 5B (either nulli-5B or nulli-5B tetra-5D) and the hybrids with suppressed Ph1 activity, in which homoeologous pairing between wheat-wheat and wheat-rye chromosomes was increased, there was a clear reduction in the number of bound arms during the progression of first metaphase for all bivalents identified. Thus, even in the absence of Ph1, end-to-end homoeologous and nonhomologous associations are actually non-chiasmatic and are a remnant of prophase pairing (Orellana 1985). In contrast, Naranjo et al. (1989) found a good correspondence between the levels of pairing at first metaphase and those expected from the frequency of first anaphase recombination for the C-band-marked wheat chromosomal arm 1BL in wheat-rye hybrids with a ph1 mutant. Yet, upon analysis of several C-banded marked chromosomal arms, in addition to 1BL, Orellana (1985) reported a significant excess of wheat-rye metaphase associations as compared to the frequency of anaphase recombinant chromosomes.
Benavente et al. (1996) made similar observations, upon genomic in situ hybridization of first metaphase and first anaphase stages of meiosis of bread wheat x S. cereale hybrids carrying the ph1b mutation. The frequency of associations between wheat and rye chromosomes greatly exceeded the level of wheat-rye recombination found in the examined hybrids. Extremely distal associations, accounting for about 50% of the total wheat–rye metaphase chromosomal pairing, were non-chiasmatic, which can explain the discrepancy between metaphase and anaphase recordings. If non-chiasmatic wheat-rye chromosomal pairing were the source of the excess metaphase associations, then it can be said that the very distal associations do not reflect chiasma formation, whereas interstitial and subterminal associations may be chiasmatic and lead to wheat-rye recombination.
In hybrids with bread wheat, the rye nucleolar organizer on 1R became inactive and its secondary constriction was no longer distinguishable. Silver staining showed that when the SAT chromosomes 1B or 6B of wheat or 1U or 5U of Aegilops umbellulata were present, the nucleolar activity of the rye SAT chromosome 1R appeared to be suppressed (Cermeño and Lacadena 1985). Suppression of the NORs of Secale genome R was reversed in wheat x rye hybrids and triticale (a synthetic allopolyploid between tetraploid wheat and rye, Secale cereale) upon treatment with the demethylating agent 5-aza-cytosine, suggesting that nucleolar suppression is triggered by cytosine methylation (Vieira et al. 1990; Neves et al. 1995; Amado et al. 1997).
Sallee and Kimber (1976) studied chromosome pairing in the hybrid between the auto-allo-hexaploid Triticum timopheevii var. zhukovskyi (currently T. zhukovskyi) (2n = 6x = 42; genome GGAAAmAm) and S. cereale. Mean chromosomal pairing per cell in the tetraploid hybrid (2n = 4x = 28; genome GAAmR) included 12.65 univalents, 5.50 rod bivalents and 2.65 ring bivalents, 0.95 trivalents and 0.05 quadrivalents. Pairing between the A and Am genomes and in multivalents between these two genomes and the G genome, was mainly autosyndetic.
The data above show that all diploid hybrids between Secale species and Triticeae species exhibit very little chromosomal pairing at first meiotic metaphase. In the triploid and tetraploid hybrids, there is somewhat higher pairing, most of which is autosyndetic between the chromosomes of the polyploid Triticeae species, a small amount is between the rye chromosomes, and only a small part of the pairing is allosyndetic between the Secale and the Triticeae species chromosomes. Evidently, Secale chromosomes underwent significant changes during the evolution of the genus, that affected their ability to homoeologously pair with other Triticeae species. Such alterations include chromosomal rearrangements, such as translocations and inversions, and accumulation of large amounts of telomeric heterochromatin. As a result, the relative position of the telomeric regions at the beginning of meiosis may shift, impairing pairing initiation of rye and other Triticeae chromosomes (Devos et al. 1995; Lukaszewski et al. 2012; Megyeri et al. 2013). Moreover, genetic and epigenetic changes, such as mutations or elimination of DNA sequences that are involved in homology recognition and pairing initiation, may underlie this restricted pairing.
Sybenga (1966) postulated that pairing is controlled by specific units or zygomeres, which, like centromeres and nucleolar organizers, become active at specific meiotic stages. Pairing between chromosomes in hybrids only occurs when certain zygomeres are common to both parental chromosomes. A genuine reduction of pairing between homoeologous chromosomes in hybrids containing the rye genotype, may thus indicate the presence of factors similar to those on chromosome 5B of wheat, that restrict pairing to chromosomes with very similar zygomeres. Evidence for such an influence of the rye genotype is not convincing, as autosyndetic pairing in hybrids between the polyploid species of Aegilops and Secale is unaffected by the rye genome (Majisu and Jones, unpublished). It seems more likely that the zygomeric system that initiates chromosome pairing in rye is different from those of Aegilops or Triticum. The disturbed alignment of chromosomes in pre-meiotic nuclei, possibly due to inactivity of zygomeres, could be responsible for the absence of homoeologous pairing in the hybrids. In conclusion, at present, differential pairing with Secale chromosomes cannot serve as evidence of evolutionary relationships with other genera in the Triticineae.
6.5 Phylogeny of Secale
6.5.1 Phylogenetic Relationships Within the Genus Secale
The genus Secale has evolved monophyletically (e.g., Hsiao et al. 1995b; Mason-Gamer et al. 2002; Petersen et al. 2004; Bernhardt 2016). Since six major translocations shaped the modern Secale genome, differing it from a putative Triticeae ancestral genome, the ancestor of the genus may have undergone chromosomal rearrangements (Martis et al. 2013). In addition, introgressive hybridizations from other Triticeae species and/or a series of whole-genome or chromosome duplications, may have played a role in Secale speciation and genome evolution (Martis et al. 2013).
Cytogenetic analyses showed that S. sylvestre is isolated from the other Secale species (Khush and Stebbins 1961; Khush 1962; Singh 1977). Crossability between S. sylvestre and other taxa of Secale is low and the hybrid plants have highly irregular meiosis, and thus, low fertility (Khush and Stebbins 1961; Khush 1962). Its isolation may have resulted from its autogamous habit (Schiemann and Nürnberg-Krüger 1952; Khush and Stebbins 1961) or from its characteristically low telomeric heterochromatin content, which results in unsynchronized mitotic cycles in embryos of hybrids with other Secale species that have larger amounts of telomeric heterochromatin (Singh 1977). In contrast, hybrids between S. strictum and S. cereale are easily made and the hybrid seeds are easily grown, even without embryo rescue techniques. The F1 hybrids exhibit somewhat reduced fertility, possibly because they are heterozygous for the two chromosomal translocations that distinguish S. cereale from S. strictum (Khush and Stebbins 1961; Khush 1962; Singh 1977). However, in areas where the two species are sympatric, introgression is believed to occur quite frequently (Stutz 1957; Khush 1962; Perrino et al. 1984; Hammer et al. 1985; Zohary et al. 2012), and it is difficult to distinguish even the first-generation hybrids from their parental species (Frederiksen and Petersen 1997). Hybrids between S. strictum subsp. strictum and S. strictum subsp. africanum are highly fertile (Khush 1962). A larger number of taxa was recognized within S. strictum previously (e.g., Roshevitz 1947), yet, although minor chromosomal differences have been reported between some of these taxa cytogenetic analyses have shown high chromosome pairing in meiosis of the hybrids, as well as high pollen fertility and large seed set (Schiemann and Nürnberg-Krüger 1952; Riley 1955; Nürnberg-Krüger 1960; Khush 1962). Thus, no strong genetic isolation barrier exists between these intra-specific taxa. Hybridization between domesticated and weedy S. cereale resulted in vigorous plants, generally with normal meiosis and high fertility (Nürnberg-Krüger 1960; Khush 1963a). Although some meiotic irregularities have been observed in hybrid plants (Stutz 1976), only S. vavilovii (currently included in S. cereale; Sencer and Hawkes 1980; Frederiksen and Petersen 1998) seems to have a karyotype of its own (Khush and Stebbins 1961; Kranz 1961, 1963; Khush 1962, 1963b; Singh and Robbelen 1977). All other specimens of S. cereale seem to possess very similar karyotypes (Stutz 1972).
The phylogenetic relationships between species within the genus Secale have been studied via isozyme electrophoretic patterns (Jaaska 1975; Vences et al. 1987), thin-layer chromatography (Dedio et al. 1969; Sencer 1975), ribosomal DNA spacer lengths (Reddy et al. 1990), characterization of the internal transcribed spacer of the rDNA (de Bustos and Jouve 2002), distribution of other repeated DNA sequences (Jones and Flavell 1982a, b), and plastid RFLPs (Murai et al. 1989). All these studies clearly showed that S. sylvestre occupies an isolated position within the genus and differs substantially from both S. strictum and S. cereale. It was also evident that the difference between S. cereale and S. strictum is not extensive. Thus, morphological and cytogenetic evidence suggest that S. sylvestre is the most ancient Secale species (Reddy et al. 1990).
Likewise, a phylogenetic analysis, based on RFLP of the plastid genome, showed that S. sylvestre is the sister group of the rest of the genus and the only well separated taxon (Petersen and Doebley 1993). Similarly, using amplified fragment length polymorphism (AFLP), Chikmawati et al. (2005) showed that S. sylvestre is the most distantly related taxa in the Secale genus. They found the annual forms of S. cereale and the perennial forms of S. strictum, as more closely related to each other than to S. sylvestre. The data of Chikmawati et al. (2005) confirmed that S. sylvestre is the most ancient species, whereas S. cereale is the most recently evolved species. AFLP analysis clearly separated all Secale species into three major species groups: S. sylvestre, S. strictum for perennial forms, and S. cereale for annual forms. In contrast to the above studies, Del Pozo et al. (1995) failed to clearly distinguish S. sylvestre from S. strictum by PCR of amplified DNA fragments. However, in the phenogram constructed based on PCR amplified band polymorphisms at the species level, S. sylvestre separated early from the other two species, while S. strictum and S. cereale appeared relatively close. Del Pozo et al. (1995) also found that S. vavilovii (currently included in S. cereale) is closer to S. strictum than to S. cereale. This contradicts the accepted taxonomic classification and cytogenetic and molecular data that placed S. vavilovii within S. cereale. Similarly, Achrem et al. (2014), using inter-simple sequence repeat (ISSR) and inter-retrotransposon amplified polymorphism (IRAP) techniques, reported the highest value of similarity between S. cereale and S. vavilovii, thus, justifying the classification of the latter in S. cereale. Shang et al. (2006), using 24 Secale cereale microsatellite markers, found that the S. sylvestre accessions were clearly divergent from the accessions of other species and that the S. vavilovii accessions were closely related to the S. cereale accessions.
S. cereale and S. strictum specimens are intermingled on the phylogenetic tree and S. strictum ssp. africanum cannot be distinguished from the other S. strictum specimens. Yet, the tested specimens of S. strictum ssp. strictum var. ciliatoglume had unique restriction sites (Petersen and Doebley 1993). However, a multivariate analysis describing the variation in a number of morphological characters of S. cereale and S. strictum, showed no clear distinction between the two taxa (Frederiksen and Petersen 1997).
Ren et al. (2011), using inter-simple sequence repeat (ISSR) markers to analyze phylogenetic relationships among wild and domesticated Secale taxa, found that the annual weedy S. cereale subsp. ancestrale evolved from S. strictum subsp. strictum. These results support the division of the genus Secale into three species: the annual wild species S. sylvestre, the perennial wild species S. strictum, including several differential subspecies forms such as strictum, africanum, and anatolicum, and S. cereale, which includes domesticated and weedy rye as subspecies forms. No differences were found between the weedy and the domesticated forms of S. cereale (de Bustos and Jouve 2002).
Al-Beyroutiová et al. (2016) evaluated genetic diversity and phylogenetic relationships using 13,842 DArTseqTM polymorphic markers. Extracted genomic DNA samples were sent to Diversity Arrays Technology Pty Ltd. (http://www.diversityarrays.com) whole genome genotyping service for Secale analysis. The model-based clustering (STRUCTURE software) separated the 84 samples into three main clusters: perennial cluster, annual cluster, and S. sylvestre cluster. The same result was obtained using Neighbor-Joining tree and self-organizing maps. Their data confirm the taxonomic classification of Sencer and Hawkes (1980) and Frederiksen and Petersen (1998), which defined Secale sylvestre, S. strictum, and S. cereale as the three main species of the genus Secale. Several authors (Reddy et al. 1990; de Bustos and Jouve 2002; Chikmawati et al. 2005; Shang et al. 2006) considered S. sylvestre the oldest species, from which all other species evolved, while Hammer (1987) claimed that S. sylvestre evolved separately, and its evolution might have begun very early. All bioinformatical tools used by Al-Beyroutiová et al. (2016) confirmed the antiquity of S. sylvestre and showed that it is the most diverged species of all the Secale taxa. Three of the 84 Secale samples they studied (MON1, MON2 and MON3) were in basal positions in phylogenetic trees. MON3 is the oldest of all the Secale accessions and likely the ancestor of S. sylvestre. MON1 and MON2 show an ancestral position in the phylogeny of the Secale genus. The three accessions share ancient morphological characters and are probably the ancestors of different lineages within Secale. The three accessions do not belong to the same lineage (i.e., species), indicating that they are probably the ancestors of lineages leading to the formation of S. sylvestre, S. strictum and S. cereale. Furthermore, Al-Beyroutiová et al. (2016) found that var. ciliatoglume of S. strictum subsp. strictum and the semi-perennial taxon of S. cereale subsp. ancestrale, namely, var. multicaule, are genetically the most closely related to the annual forms of S. cereale. Chikmawati et al. (2005) affirmed that var. ciliatoglume is an ancestral type, being the second taxon diverging after S. sylvestre. The observations of Frederiksen and Petersen (1997), based on morphometric analyses, suggested that var. ciliatoglume should be given an intraspecific rank. Concerning var. multicaule of S. cereale subsp. ancestrale, Hammer et al. (1987) suggested its hybrid origin from the cross S. strictum x S. cereale, but the results of Al-Beyroutiová et al. (2016) did not show a reticulated origin of this variety. The definitive status of these two varieties cannot be solved by DArTseq polymorphism only. In addition, the results of Al-Beyroutiová et al. (2016) confirmed that S. vavilovii could not be considered a separate species but rather, a subspecies of S. cereale. Overall, the phylogenetic relationships on the infrageneric level are still poorly understood. Bernhardt (2016) showed that S. strictum is somewhat different from S. cereale. Similarly, Petersen et al. (2004) stated that “an increased amount of evidence indicates that S. cereale and S. strictum are not exclusive lineages”.
According to Kobyljanskij (1982), the oldest ancestor of the genus, Protosecale, appeared in the Oligocene (33.7–23.8 MYA) when early Triticeae appeared, and later evolved into a Protosylvestre and Protostrictum, from which S. sylvestre and S. strictum developed during the Pliocene epoch (5.3–1.8 MYA). In accord with this, Middleton et al. (2014), based on sequencing of chloroplast genomes, estimated that Secale diverged from Triticum approximately 3–4 million years ago.
6.5.2 Phylogenetic Relationships Between Secale and Other Triticineae Genera
The phylogenetic relationships of Secale with other Triticeae genera have been studied through morphological traits, genome analysis, isozymes, and cytoplasmic and nuclear DNA sequences, which have yielded contradictory results regarding the position of Secale. Aase (1935), assuming that the degree of chromosome pairing is a true test of genetic relatedness, concluded that Secale species are more closely related to Aegilops and Agropyron than to Triticum. In accord with this conclusion, Favorsky (1935) reported on the existence of a certain degree of relationship between S. cereale and Agropyron cristatum. Lucas and Jahier (1988) executed a diallel-crossing program, which included ten diploid species from the genera Triticum, Aegilops, Dasypyrum and Secale. The number of associations between chromosome arms in the hybrid PMCs at first meiotic metaphase was taken as an indication of the degree of homology between the parental genomes. They found little affinity between the genomes of Aegilops and S. cereale. In accord with these results, Lucas and Jahier (1988) noted that the affinity they found between the Aegilops genomes and the rye genome was as low as that reported by Sodkiewicz (1982) for the Am genome of Triticum monococcum and the R genomes of S. cereale. Lucas and Jahier (1988) concluded that S. cereale and Dasypyrum villosum are more distantly related than to the Aegilops and Triticum species. However, as stressed by Frederiksen and Seberg (1992), genome analysis is incapable of revealing phylogenetic relationships of the diploid mono-genomic taxa of the Triticeae.
Taxonomical treatments by several well-known taxonomists (e.g., Nevski 1933; Melderis 1953; Hubbard 1959; Tzvelev 1973, 1976) placed the genus Secale close to the genus Dasypyrum. In accord with this taxonomical treatment, Baum (1983), on the basis of a phylogenetic analysis of Triticeae by means of numerical methods, grouped Secale and Dasypyrum close to one another. Further analysis of morphological characteristics suggested that Secale is the sister group of a clade consisting of Dasypyrum villosum, Triticum monococcum and Aegilops species (Frederiksen and Seberg 1992; Seberg and Frederiksen 2001; Seberg and Petersen 2007).
Incongruence exists between the phylogenetic trees constructed based on morphological versus molecular data, as well as between trees constructed using various kinds of molecular data (Seberg and Frederiksen 2001; Seberg and Frederiksen 2007; Escobar et al. 2011). According to several morphological trees, T. monococcum is included in the Secale clade (Seberg and Frederiksen 2001), but, in some molecular studies, is a sister clade to the Aegilops clade (Kellogg and Appels 1995; Mason-Gamer and Kellogg 1996). Molecular data from the plastid genome suggest a relationship with Taeniatherum, Triticum and Aegilops (Mason-Gamer and Kellogg 1996; Petersen and Seberg 1997), while DNA sequence data from various parts of the nuclear genome have given diverse results. Data from internal transcribed spacers (ITS) of the rDNA suggested that Secale is the sister group of Eremopyrum and Henrardia (Hsiao et al. 1995a, b), whereas data from the spacers between the 5S RNA genes suggested a rather basal position for Secale within Triticeae (Kellogg and Appels 1995; Kellogg et al. 1996). Thus, the position of Secale remains uncertain.
Monte et al. (1993) used RFLP in combination with other approaches, to reconstruct evolutionary events, which revealed a high degree of polymorphism both between and within the species examined. The RFLP data were used to generate a cladogram and a phenogram and the results of both methods were consistent with each other and with the general taxonomic information provided by earlier morphological studies, meiotic pairing analysis, isozyme tests, and sequence alignment in the rDNA and 5S DNA loci. Both the cladogram and the phenogram showed very close associations between the genera Secale and Agropyron and the Ee and Eb genomes of Elymus. The cladogram and the phenogram also clustered Secale and Agropyron together with the genomes of Triticum.
Mason-Gamer (2005) performed a phylogenetic analysis of sequences from a portion of the tissue-ubiquitous β-amylase gene in a broad range of the mono-genomic Triticeae. The results showed close relationships among Secale, Australopyrum, and Dasypyrum. Yet, no other molecular data sets support a Secale + Australopyrum + Dasypyrum clade; in general, there is little agreement with regard to the placement of any of these taxa. Furthermore, the morphological data (Seberg and Frederiksen 2001) showed that Secale is sister to a Dasypyrum + Triticum clade, while Australopyrum forms a paraphyletic grade at the base of a large clade containing over half of the remaining taxa. Sequencing of the ITS region of nuclear ribosomal DNA of diploid Triticeae species, brought Hsiao et al. (1995a, b) to conclude that Secale is close to Taeniatherum and sister clade to Elymus bessarabicus, E. elongatus and Triticum monococcum.
Seberg and Petersen (2007) studied the phylogeny of diploid Triticeae by combining morphological observations with nucleotide sequence data from two plastid genes (rbcL, rpoA), one mitochondrial gene (coxII) and two single-copy nuclear genes (DMC1, EF-G). Their data indicate incongruence between the four data sets, partitioning morphology and the three -genome-bearing compartments, was observed. Only the mitochondrial and nuclear sequences were mutually incongruent. They concluded that S. strictum is close to Taeniatherum caput-medusae, followed by Dasypyrum villosum, Elymus elongatus Elymus bessarabicus, Crithopsis delileana and the genera Aegilops, Triticum and Amblyopyrum.
Escobar et al. (2011), using one chloroplastic and 26 nuclear genes, obtained a comprehensive molecular dataset of phylogenetic value, on the diploid species of the Triticeae. They grouped Secale, including Taeniatherum, Triticum and Aegilops in Clade V, and the genera Dasypyrum, Heteranthelium as a sister clade. Clade V is retrieved, although branching within this clade changes relative to the super-matrix tree: Secale and Taeniatherum branched together, T. monococcum branched sister to Ae. tauschii, and Ae. speltoides and Ae. longissima grouped together. Heteranthelium branched at the base of clade V and these two newly inferred clades (Pseudoroegneria-Dasypyrum and Heteranthelium-clade V) were closely related to each other. According to Escobar et al. (2011), Dasypyrum, Heteranthelium and genera of clade V, grouping Secale, Taeniatherum, Triticum and Aegilops, evolved in a reticulated manner. In conclusion, with respect to the placement of the genus Secale in the tribe-wide phylogeny, virtually all genera of the Triticeae have been suggested—either alone or in combination with other genera—as a sister group to Secale (Petersen et al. 2004).
Whole genome sequencing data has enabled to better understand the phylogenetic relationship of rye to other species from the Triticeae as described in Chap. 3. The new genome sequences have shed light on rye evolution, which so far, had been not completely resolved regarding the proximity to wheat and barley as well as to its wild relatives. It was thought that multiple introgressions might generate a mosaic genome with reticulate evolution patterns and discordance in the phylogeny of various chromosomal segments. When comparing the genomes of wheat (cv. Chinese Spring) and barley (cv. Morex) to Lo7, Rabanus-Wallace et al. (2021) found no major discordance and showed that rye is more closely related to bread wheat than to barley across the whole genome. Furthermore, Li et al. (2021), analyzing single-copy conserved orthologous loci, estimated that rye separated from wheat 9.6MYA while barley separated from wheat 15MYA. By contrast when comparing sequence clusters of k-mers from 955 cultivated and wild rye lines, Rabanus-Wallace et al. (2021) found that reticulate evolution with multiple inter-species introgression of genomic clusters played a major role in rye evolution. For example, Lo7 was found to contain mostly clusters related to S. cereale and S. vavilovii and less related to S. strictum and S. sylvestre. In summary, while there was limited reproductive isolation between rye species, inter-genera exchanges did not play a major role in rye evolution.
6.6 Domestication
Secale cereale (rye) is the only domesticated species of the genus Secale. Vavilov (1917, 1926) considered rye a classical example of a secondary crop. Secondary crops evolved first as weeds that infested cultivated fields and only later, established as crops, whereas primary crops, developed from wild progenitors that were cultivated. When a crop is introduced into areas with harsh climatic conditions, to which the weed plant is more adapted, the latter may become more successful than the crop, forcing the farmer to domesticate it as a replacement for the crop. In this respect, rye is hardier than wheat and can withstand harsher climatic conditions and poorer soils. Vavilov (1917, 1926) observed that weedy rye is common in wheat and barley fields of southwest Asia and Central Asia, but in the mountainous areas of eastern Turkey, Caucasia, and Central Asia, at altitudes of 2000–2500 m asl, where rye always succeeded more than wheat, it gradually replaced wheat as a domesticated crop. In such areas, pure stands of domesticated rye were common. As wheat moved northward and eastward to areas with harsher climatic conditions, the weedy rye was consequently, domesticated. Vavilov (1926) and Khush (1963a, b) assumed that rye was domesticated in several places independently and at different times.
Having first arisen as a weed in fields of wheat and barley, rye may have been adopted as a crop at a somewhat later date than that of wheat and barley (Ladizinsky 1998). It is also reasonable to assume that these weedy races would have only evolved with the development of agriculture in western Asia. There is also general agreement that the original ancestor of these weedy races, and hence of domesticated rye as well, was S. strictum (Vavilov 1926). Sencer and Hawkes (1980) assumed that wild populations of S. cereale, currently classified in S. cereale subsp. ancestrale (Frederiksen and Petersen 1998), which have presumably evolved from S. strictum (Khush and Stebbins 1961), invaded wheat and barley fields during the early days of cultivation and gave rise to weedy ryes with varying degrees of rachis brittleness. It is assumed that the impressive evolvement of weedy rye, as well as variation build-up in domesticated rye, may have been considerably enhanced by introgressive hybridization with the perennial Secale strictum, the wild rye species distributed over the elevated continental parts of Anatolia and adjacent areas in south-west Asia (Zohary et al. 2012).
It is not difficult to imagine the kind of selection necessary for the weedy rye to adapt to wheat fields. A more upright culm enhances competitive capacities. In addition, genes controlling non-shattering of the grains would be advantageous. Cultivation prior to sowing tended to destroy seedlings originating from seeds dropped by shattering spikes the previous year. Seeds of non-shattering genotypes would have been harvested with the main cereal crop and subjected to the same cultural procedures during the next season. At the same time, larger grains are positively selected, since even the most primitive winnowing procedure favors the retention of grains approaching the size of those of wheat and barley (Sencer and Hawkes 1980; Ladizinsky 1998; Zohary et al. 2012).
Stutz (1972), based on extensive cytological, ecological and morphological studies, hypothesized that S. cereale originated from hybridization between the perennial cross-pollinated S. strictum and the annual, self-pollinated S. vavilovii (currently included in S. cereale subsp. ancestrale; Sencer and Hawkes 1980; Frederiksen and Petersen 1998), the latter derived from S. sylvestre as a consequence of chromosomal translocations. S. sylvestre was, in turn, derived from S. strictum or a common ancestor. However, Nürnberg-Krüger (1960) and Khush and Stebbins (1961) considered this hypothesis improbable and assumed that S. cereale evolved from S. strictum as a result of progressive cytological and morphological differentiation, which was likely facilitated by adaptive superiority of translocation heterozygotes and rearrangement homozygotes. Zohary (1971) ascribed sympatric speciation of S. cereale from S. strictum to disruptive selection.
Almost all cytogenetic studies have implicated two instantaneous chromosomal rearrangements as the origin of S. cereale from S. strictum. All perennial rye taxa included in S. strictum and the annual S. sylvestre have the same chromosome arrangement and closer affinity to each other (Stutz 1972). On the other hand, annual weedy and domesticated rye taxa of S. cereale have the same chromosome arrangement and display cytogenetic affinity to each other and differ from the other two species by two translocations involving three of the seven basic chromosome sets (Riley 1955; Khush and Stebbins 1961; Stutz 1972). Thus, S. strictum subsp. strictum is a perennial, self-incompatible, species with a strictum chromosome type. S. strictum subsp. africanum is a perennial, self-fertile species with a strictum chromosome type, S. Sylvestre is an annual, self-fertile, species with a strictum chromosome type and S. cereale is an annual, self-incompatible, (rarely self-compatible), species with a cereale chromosome type. From evolutionary and phylogenetic perspectives, the annual weedy taxa of S. cereale subsp. ancestrale are considered younger than the perennial wild ones and the domesticated rye, S. cereale subsp. cereale, is thought to be the youngest of all (Sencer and Hawkes 1980).
Wild forms of S. cereale, i.e., subsp. ancestrale, with complete brittle rachis, likely invaded wheat and barley fields and gave rise, through mutations, to weedy types with annual growth habits and varying degrees of rachis brittleness. The mature ears of weeds with non-brittle rachis, that do not shatter and also tend to mimic wheat in grain size and weight, have a great adaptive advantage over types with brittle rachis, since they are harvested and threshed together with wheat. Since traditional winnowing does not separate grains of rye from those of wheat, rye seed is included in the harvest and planted with the wheat in the subsequent year (Ladizinsky 1998). Farmers in the elevated plateau of eastern Turkey, Armenia and Central Asia, tolerate some rye-weed infestation in their crop, because in years with extreme cold and dry weather, the rye weed survives when wheat does not, ensuring a supply of cereal grains (Zohary et al. 2012).
The weedy races of S. cereale, occurring in west and central Asia, were presumably interfertile, differing from one another mainly in their seed dispersal pattern, ranging from races with a brittle rachis to non-brittle rachis (Ladizinsky 1998; Zohary et al. 2012). These races are common weeds in wheat fields and those with non-brittle rachis are not separated from wheat by harvesting, threshing and winnowing (Ladizinsky 1998). Farmers domesticated rye under cultivation, by selecting for the taxa with non-brittle rachis and bigger caryopsis (Sencer and Hawkes 1980). Thus, the immediate progenitors of the domesticated form, S. cereale subsp. cereale, arose from one or more of the weedy races belonging to S. cereale subsp. ancestrale.
Most of the weedy taxa were also cross-pollinated. Secale strictum subsp. strictum, the progenitor of the weedy types of S. cereale, is a cross-pollinated species that has a perennial growth habit and brittle rachis. Hence, domesticated S. cereale is unique among cereals, being the only cross-pollinated cereal taken into cultivation in southwest Asia.
While it seems highly likely that the agriculturally dependent S. cereale evolved directly from the wild S. strictum, the actual course of events is still obscure (Sencer and Hawkes 1980; Evans 1976, 1995). When considering its morphology and breeding system, S. cereale is close to S. strictum. Khush and Stebbins (1961) proposed gradual accumulation of the chromosomal difference between the two, but intermediate chromosome types have not been found, suggesting that the two translocations occurred simultaneously (Ladizinsky 1998). If no other distinct intermediate species were involved, then the question arises as to how major structural rearrangements (involving a double translocation) could have become established, particularly in light of the initial handicap of reduced fertility which would certainly have resulted. Moreover, the hypothesis claiming direct emergence of S. cereale from S. strictum fails to explain how a homozygous type for two chromosomal translocations could emerge in a population of a self-incompatible plant such as S. strictum (Ladizinsky 1998). The main obstacle is not so much the low fertility of a spontaneous heterozygote for two chromosomal rearrangements, but the constant pollination of the new cereale-chromosomal type by S. strictum. Such continuous pollination seems necessary for the accumulation of a sufficient number of alleles in the self-incompatible gene in the cereale-chromosome type. Yet, more rapid establishment could be achieved if the heterozygous genotypes and the homozygous cereale-type had some adaptive advantage over the strictum-type (Riley 1955; Khush and Stebbins 1961; Ladizinsky 1998). The partial fertility barrier between the new and old chromosome arrangements could have served as an isolating mechanism preventing swamping of the evolving weedy races of S. cereale by their progenitor, S. strictum. Eventually, the partial isolation enabled S. cereale to establish itself and to sympatrically develop as a separate species.
Evolvement of the annual growth habit of S. cereale, via mutations in the perennial S. strictum, is highly probable. Perennial growth habit is a dominant trait presumably controlled by a small number of genes. Charpentier et al. (1986) found that perennial growth habit was a dominant trait in F1 hybrids between Elymus farctus subsp. farctus (=6x Agropyron junceum) and common wheat cv. Chinese Spring. In BC1 plants, derived from backcrossing the F1 hybrids to Chinese Spring, perennialism was less marked. They concluded that gene(s) located on two or more chromosomes of E. farctus determine perennial growth habit. Lammer et al. (2004) found that chromosome arm 4EeS of diploid Elymus elongatus confers perennial growth habit when added as a monosome or disome to Chinese Spring background. This may suggest that the gene(s) determining perennial growth habit is located on rye chromosome arm 4RS. Mutations in these genes presumably led to the formation of annual weedy races of rye. Annual growth habit is better adapted for successful infestation of cultivated wheat and barley fields and therefore, a strong selection pressure was exerted on the weedy rye, in favor of the annual forms. Therefore, it is highly probable that the weedy races of S. cereale evolved directly from S. strictum as was proposed by Riley (1955) and Khush and Stebbins (1961), via accommodation of the change from perenniality to annuality.
Takahashi (1972) described two complementary dominant genes, Btr and Btr2, located on chromosome 3H, that control spike fragility in wild barley, Hordeum vulgare L. subsp. spontaneum (C. Koch) Thell. Domesticated barley, which has a non-fragile spike due to a tough rachis, contains the recessive alleles btr1btr2 of these loci. Similarly, Sharma and Waines (1980) crossed domesticated einkorn Triticum monococcum subsp. monococcum, which has a tough rachis, with wild einkorn T. monococcum subsp. aegilopoides, which has a brittle rachis, and found in F2 and backcross generations, that tough rachis is controlled by two complementary recessive genes. Two recessive genes, located on the short arms of chromosomes 3A and 3B, control the tough rachis trait in domesticated allotetraploid and allohexaploid wheats (Levy and Feldman 1989a, b; Rong 1999; Watanabe and Ikebata 2000; Watanabe et al. 2002, 2005a, b; Nalam et al. 2006; Millet et al. 2013). Comparative mapping analyses suggest that the genes controlling tough rachis in wheat, are located on the short arm of chromosomes of homoeologous group 3 (Nalam et al. 2006). Thus, it is reasonable to assume that the genes determining tough rachis in S. cereale are located on the same arm, namely, 3RS, a chromosome that is not involved in the two translocations distinguishing S. cereale from S. strictum, in terms of tough rachis and annual growth habit.
The chromosomal location of the three characters distinguishing S. cereale from S. strictum, namely, annual growth habit, non-fragile rachis, and large caryopsis, presumably are not associated with the two chromosomal rearrangements existing between these two species. Such a conclusion has been drawn from genetic analysis of F2 of S. strictum x S. cereale (Stutz 1957). Thus, it is assumed that while perennial Secale infested wheat and barley fields in northeastern Turkey, Armenia and northwestern Iran, mutation(s) supporting annual growth habit gave adaptive advantage to the weedy Secale. Shifts to tough rachis and large grains, mimic the wheat crops and increase the adaptation to harvest and threshing.
Alternatively, Sencer and Hawkes (1980) assumed that the switch to annual growth habit led to the development of early wild populations of S. cereale, which presumably evolved from S. strictum. This change improved their ability to invade wheat and barley fields during the early days of cultivation, and gave rise to the development of weedy ryes. Weedy rye presumably originated in eastern Turkey and Armenia (Zohary et al. 2012) and evolved with the development of agriculture in this region. From this area, rye spread as a weed in wheat and barley fields, towards the north, east and west and imposed itself as a secondary crop under conditions unfavorable for wheat and barley. It is probable that rye became a crop in its own right in several places independently (Sencer and Hawkes 1980). Vavilov (1917, 1926), based on the fact that the greatest accumulation of genetic diversity of S. cereale was found in southwest Asia, considered this region to be the primary center of origin of domesticated rye. At the same time, he considered Afghanistan and Tadjikistan to be a secondary center of variation of this crop (Vavilov 1917, 1926). Sencer and Hawkes (1980), based on a synthetic analysis that considered evidence from the fields of morphology, taxonomy, ecology, phytogeography, reproductive biology, genetics, cytology, palaeoethnobotany, philology, phylogeny and evolution, suggested Mt. Ararat and Lake Van area in eastern Turkey as the geographic origin of domesticated rye. Linguistic evidence suggests early acquaintance with rye by the people living in the Caucasus and the northeastern Black Sea region (Sencer and Hawkes 1980). The name ‘rye’ in the Caucasian languages was retained by the Greeks and Celts, who spread the crop during their migrations (Sencer and Hawkes 1980). These are revealed by the facts that the Greek, Celtic and Latin names of rye are derivatives of its name in the Caucasian languages.
In summary, the available evidence points to the implicates the early weedy, annual, brittle rye types as the ancestors of the weedy non-brittle types, from which domesticated rye was picked up. Despite of the two translocations that exist between these two species, genes from S. strictum introgressed into S. cereale, enriching its gene pool. Indeed, partial fertile hybrids between annual S. cereale and perennial S. strictum can be produced in experimental fields and natural hybridizations of this sort occur quite frequently near cultivated fields in eastern Turkey (Zohary et al. 2012). It is assumed that variation build-up in domesticated rye and the impressive evolvement of weedy rye could have been considerably enhanced by introgressive hybridization with the perennial S. strictum.
Archaeological records support the proposal that rye was domesticated in eastern Turkey and Armenia, but much later than wheat. Due to the scarcity of rye remains in the Neolithic and the Bronze settlements of southwest Asia, it is difficult to define the exact time of rye domestication (Zohary et al. 2012). The earliest rye remains come from Epi-Palaeolithic sites in the Upper Euphrates valley in northern Syria. Numerous charred grains, later identified as a mixture of both wild rye and wild einkorn wheat, were unearthed in ca. 11,800–11,300 cal BP Tel Mureybit (van Zeist and Casparie 1968; van Zeist and Bakker-Heeres 1985; Willcox and Fornite 1999). The narrow shape of the kernels indicates that they represent wild forms. Similar narrow rye grains, either of S. cereale subsp. ancestrale or of S. strictum, were found in the ca. 12,700–11,100 cal BP Epi-Palaeolithic Tel Abu Hureyra. Hillman (1975, 2000) and Hillman et al. (1989, 2001) suggested that these were domesticated forms, a view that was later criticized because of lack of chaff and proper dating (e.g., Nesbitt 2002; Colledge and Conolly 2010). Wild rye grains were also discovered in two Pre-Pottery Neolithic A (PPNA) northern Syria sites, ca. 11,500–11,000 cal BP J Ahmar (Willcox 2002; Willcox et al. 2008) and ca. 10,700–10,400 cal BP Djade el Mughara (Willcox et al. 2008). On the other hand, grains of domesticated rye were first found in ca. 9450–8450 cal BP PPNB Can Hasan III (Hillman 1972, 1978) and in very small quantities at the nearby ca. 9350–8950 cal BP site of Aceramic Neolithic Çatalhöyük in East Turkey (Helbaek 1964a, b; Fairbairn et al. 2002, 2005, 2007). At Can Hasan III, relatively plump grains were discovered, together with some non-brittle rachis segments. As argued by Hillman (1978), these finds suggest that rye had already entered cultivation in East Turkey in early Neolithic times, either as a non-brittle weed infesting wheat fields, or as a full-fledged domesticated cereal crop. Yet, no additional rye remains have been discovered in other Neolithic southwest Asian sites. The next record comes from ca. 4000 BP Bronze Age levels of Alaca Höyük in north-central Anatolia (Hillman 1978). There, a pure hoard of carbonized large grains of S. cereale was discovered, indicating that, at that time, rye was grown as a crop in its own right. Thus, a reasonable estimate for domestication is about 5000 BP.
Early archaeological evidence is also fragmentary in regions outside the Fertile Crescent and thus, the spread of rye cultivation in Europe is difficult to sketch (Behre 1992). Rye grains were found in Europe in Early Neolithic sites (ca. 7550–6459 cal BP) in northern Italy, from Middle Neolithic sites (ca. 6950–6650 cal BP) in Slovakia, and from several late Neolithic sites in Poland. Further evidence of rye remains in Europe came from several Bronze Age settlements in several countries of Central and East Europe (for a detailed description of the discovery of rye remains in Europe see Zohary et al. 2012). Only a limited number of rye grains were found in these sites, in contrast to the abundance of wheat or barley grains discovered, indicating that at that time, rye contaminated wheat and barley fields. In later Iron Age settlements in Germany (Hopf 1982), Denmark (Helbaek 1954), Poland (Willerding 1970), and Crimea (Januševič 1978), rye also typically appeared admixed with barley or wheat. Rye as a main crop, was part of the Roman grains-agriculture and was grown in the cooler northern provinces (Sencer and Hawkes 1980). Carbonized rye grains have been retrieved from several Roman frontier sites along the Rhine and the Danube (Hillman 1978), as well as from the British Isles (Jessen and Helbaek 1944). Yet, wide cultivation of rye in Central and Eastern Europe only became marked from the Middle Ages. Renfrew (1973) refers to excavations dating rye in Austria, Poland, Czechoslovakia and eastern Crimea to the third-fourth centuries AD, where rye was found as a weed in crops of wheat and barley. Since then, it served as the main bread cereal in most areas east of the French-German border and north of Hungary, while in Southern Europe, it was cultivated on marginal lands (Sencer and HawSkes 1980).
Rye was probably originally grown in the same areas in Europe as the other temperate cereals, but its tolerance of low rainfall, cold winters and poor light soils made it particularly suitable for large areas of northern and eastern Europe, which are less suitable for wheat and barley. By the end of the eighteenth century, it had become the major cereal of the region. Since then, however, it has been gradually replaced by wheat.
Rye introduction into Europe, as a minor admixture with wheat and barley, probably occurred via two separate routes. One route was northwards, through the Caucasus from its primary center of origin. According to Engelbrecht (1916, 1917), rye grains were transported from north-eastern Anatolia to the north of the Black Sea by Greek traders, since they had close trade relations with the Scythians (on the river Dnjepr), who cultivated cereals during the fifth century BC. A second route was westwards, via the Aegean Basin and the south Balkan. Cultivation of rye spread eastwards to Iran and Central Asia, the secondary center of variation, and later on, further east. S. cereale appeared at the end of the fourth millennium BP, in Hasanlu, Iran, and seems to have been a staple crop in this region throughout the Iron Age (Tosi 1975).
Rye (Secale cereale subsp. cereale) is an important cereal crop in the cooler parts of northern and central Europe and Russia, cultivated up to the Arctic Circle and up to 4000 m above sea level (Zohary et al. 2012). The main rye belt stretches from northern Germany through Poland, Ukraine, Belarus, Lithuania and Latvia, into central and northern Russia. Rye is also grown in North America (Canada and the United States), in South America (Argentina, Brazil and Chile), in Oceania (Australia and New Zealand), in Turkey, in Kazakhstan and in northern China. It is particularly appreciated in these regions because of its winter hardiness, resistance to drought, and its ability to grow on acidic, sandy soils (Evans 1995). Its capacity to produce an economical crop in areas of cold winters and hot summers, renders it superior to the other temperate cereals. Although spring and winter biotypes of rye exist, most of the world supply is obtained from winter varieties.
Rye is grown extensively as a grain, a forage crop and as a cover crop (Evans 1976, 1995). Its grain is used for flour, rye bread, crisp bread, rye beer, some whiskeys, some vodkas, and for animal fodder. The area under cultivation is substantially smaller than that of wheat and barley and the world rye production is lower than any of the other major cereals. In 2012, the total production of rye grains was estimated at 14,615,719 metric tons (FAO 2015; Table 6.2). Although the production levels of rye have fallen in the last several years, in most of the producing nations, rye is still an important food plant in many areas of northern and eastern Europe and central Asia. Most rye is consumed locally or exported to neighboring countries only, rather than being shipped worldwide.
Rye bread, including pumpernickel, is a widely consumed food in Northern and Eastern Europe. Rye flour is high in gliadin, but low in glutenin, with a lower gluten content than wheat flour. It also contains a higher proportion of soluble fibers than wheat. Its grains contain appreciable amounts of proteins and therefore, its flour can be baked into dark-colored rye bread. In spite of the poor baking quality of the flour, much of the present world production of rye is consumed in the form of bread, appreciated for its flavor and distinctive dense texture. It has been estimated that in the early part of the twentieth century, rye bread was the main cereal food of a third of the European population. Rye grain is also used to make alcoholic drinks, like rye whiskey and rye beer, i.e., rye is used to make whiskey in the United States and Canada, gin in the Netherlands, and beer in Russia. In all rye-producing countries, more than 50% of the grain is used in animal feed and the young green plants are also commonly used for livestock fodder. The mature straw is too tough for animal fodder, but can be used for bedding, thatching, paper making, and straw hats.
Feral plants are plants that are derived, in part or fully, from crop plants that have become partly or fully undomesticated, and are no longer dependent on managed cultivation. Feral rye, a weed of wheat and barley fields, poses a serious threat to annual winter grain yields in western and central United States. Feral rye likely spread as a contaminant in the seed of domesticated cereals, as they were introduced into new areas.
By the time conscious plant breeding began, in the later part of the nineteenth century, the early plant breeders relied heavily on locally adapted land races as their immediate source of variability (Evans 1976). Breeding methods have been influenced by the outbreeding nature of the crop. Early breeding techniques are best described as forms of simple recurrent selection. With recently improved knowledge of the genetic structure of outbreeding populations, more sophisticated methods have been used (Evans 1976, 1995).
In contrast to most grain crops that are self-pollinating, rye is a cross-pollinated cereal. It has a gametophytic two-locus incompatibility system (Lundquist 1956). Consequently, rye yields depend, among other factors, on effective wind pollination. Rye shows inbreeding depression but inbred lines of acceptable vigor can be isolated and used in the construction of synthetic varieties, following suitable progeny tests for combining ability (Evans 1976, 1995).
Unlike of the objectives in wheat and barley breeding, aspects of disease resistance have not dominated rye breeding. Improvement of grain yield, protein content and quality, together with cold tolerance and shorter straw, have been the main aims of recent breeding. Utilization of rye as forage has led to the breeding of varieties bred solely for this purpose and emphasis is then placed on characteristics other than grain production, namely, total dry matter, growth in winter and early spring and digestibility. Ergot (Claviceps purpurea) is a disease which has caused some trouble from time to time. Ergot is a fungus that parasitizes rye and is poisonous to humans and livestock. The poisonous sclerotia, which fully replace the grain and occasionally penetrate into flour, reportedly cause hallucinations in humans and abortion in farm animals. Thus, breeding for ergot resistance is also an important aim.
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Feldman, M., Levy, A.A. (2023). Secale L.. In: Wheat Evolution and Domestication. Springer, Cham. https://doi.org/10.1007/978-3-031-30175-9_6
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