Caryophyllales:
New Insights into the Phylogeny, Systematics and
Morphological Evolution of the Order
Proceedings of the Symposium
Moscow M.V. Lomonosov State University
24th-27th September 2012
Caryophyllales: New Insights into the Phylogeny, Systematics and
Morphological Evolution of the Order. Proceedings of the Symposium held on
24th-27th September 2012 at Moscow M.V. Lomonosov State University
Editors: A.K. Timonin, A.P. Sukhorukov, G.H. H arper, M.V. Nilova
Printed in Tula, Grif & Co.
The articles in this Symposium volume emphasize the most important problems and results of
molecular phylogeny, diversity, photosynthetic pathways, ecology, morphology and anatomy
within the order Caryophyllales. The work presents recent results from fundamental research in
theoretical botany and provides a basis for applying biology to a changing world, especially with
regard to the radiation and evolution of taxa with a global distribution such as Chenopodiaceae
and Amaranthaceae, with their important role in natural and disturbed plant communities. New
versions of the phylogeny of many taxa are included, and some taxa are lectotypified in this
publication. We believe that this book will be useful for future investigations of phylogeny and
evolutionary trends in the plant sciences.
This publication was supported by the Russian Foundation for Basic Research (project no 12-0406095-g).
Издание сборника поддержано Российским Фондом Фундаментальных Исследований
(проект 12-04-06095-г).
Организационный комитет Симпозиума: А.К. Тимонин, А.П. Сухоруков, Дж.Х. Харпер,
Н.Н. Цвелев, В.С. Новиков, А.В. Троицкий, М.В. Нилова.
Images on the title page (clockwise from top left): Rivina brasiliensis, Atriplex holocarpa,
Enchylaena tomentosa, semi-desert landscape at Elton Lake (Volga-Ural Interfluvial)
Photos from A.P. Sukhorukov
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2
FRUIT ANATOMY OF ANTHOCHLAM YS
(CHENOPODIACEAE/AMARANTHACEAE)
Alexander P. Sukhorukov* & Alexandra I. Konstantinova
Dept. o f Higher Plants, Biological Faculty, Moscow Lomonosov State University, 119234, Vorobyovy Gory 1/12,
Moscow, Russia
suchor@mail.ru; al-konst@mail.ru
*corresponding author. suchor@mail.ru
Introduction
The genus Anthochlamys comprises 5-6 species distributed in the Irano-Turanian floristic
region. Almost all the taxa can be found in Iran and West Afghanistan. Only A. tjanschanica
seems to be isolated from other species (Tien-Shan Mountains: Eastern Kazakhstan, Kyrgyzstan
and North Tajikistan: Sidorenko et al., 1968). All species are annuals with ridged or sulcate
stems that are glabrous or covered in the upper part with simple or branched hairs. The leaves are
short-petiolate or sessile, entire, lanceolate or elliptic, and are mostly basally arranged. The
inflorescence is a spike. Each bisexual flower is supported by a small bract and consists of a
white or pinkish perianth of 5 free segments, 5 stamens and a superior ovary with two stylodia.
The fruit is indehiscent, single-seeded, rounded (2.5-4.5 mm in diameter), flattened, in its seedcontaining part convex on both sides, and with a prominent, thin, wing-like pericarp outgrowth
on the margin that can form a small sinus at the top of the fruit between two stylar remnants (Fig.
1A). The seed has a vertical embryo and copious perisperm. The diagnostics of the genus are
mostly based on prominence of stem ridges, leaf shape and presence of apical sinus in the fruit
(Aellen, 1950; Hedge, 1997).
Fig. 1. A. Fruit of Anthochlamys turcomanica. Scale bar: 500 ^m; B. Cross-section of A.
polygaloides fruit. - Abbreviations. Pericarp: ol - outer layer, pa - subepidermal parenchyma, osl - outer
sclereid layer, vb - vascular bundle (derivate), isl - inner sclereid layer. Seed: sc - seed coat, co cotyledons, ps - perisperm. Scale bar: 100 ^m
Within the Chenopodiaceae/Amaranthaceae group the three genera Anthochlamys,
Agriophyllum and Corispermum form their own clade (Kadereit et al., 2003) that can be
recognized at the subfamilial level as Corispermoideae Ulbr. (Ulbrich, 1934). This clade splits
into two subclades - Agriophyllum and Corispermum+Anthochlamys. The close relationship
between Corispermum and Anthochlamys is also supported by morphological data. However, the
genus Anthochlamys still remains one of the least studied groups, especially with regard to
fruit/seed structure and its implications for evolution.
92
The first results describing the fruit anatomy of three Anthochlamys species
(A. afghanica, A. multinervis and A. tianschanica) were provided by Sukhorukov (2007). The
aims of the present study are:
(1) to investigate the fruit anatomy of all species in the genus from a taxonomic point of
view;
(2) to reveal evolutionary trends in the carpology of the Anthochlamys-Corispermum
lineage;
(3) to clarify whether the details of fruit structure in Anthochlamys appear to be unusual
within the Caryophyllales.
M aterials and Methods
Our own observations on the ecology of the Anthochlamys species were carried out in
Uzbekistan and Kazakhstan during expeditions in 2005-08. 2-3 detached fruits of Anthochlamys
species were obtained from the collections at MW, LE, and W with the permission of the
herbarium staff in each case. The material studied is listed in Appendix 1. In order to compare
the fruit/seed characters of Anthochlamys with other Caryophyllales and especially with closely
related taxa from the subfam. Corispermoideae, ca. 250 members of the order were investigated
earlier (Kadereit et al., 2010; Sukhorukov, 2007; 2008 a; 2008 b; 2011), and recent results are
still being analyzed (Sukhorukov and Mavrodiev; Sukhorukov et al., in prep.). Cross-sections
were cut either by hand or with a microtome. For tissue staining the following solutions were
used: 0.2% aqueous toluidine blue to stain living tissues, Sudan IV for revealing fatty substances,
and Lugol’s iodine for starch. Prior to scanning electron microscopy (SEM) the material was
dehydrated in aqueous ethyl alcohol solutions of increasing concentration, then in alcoholacetone solutions and pure acetone. SEM observations were made with a JSM--6380 (JEOL Ltd.,
Japan) at 15 kV after critical-point drying and sputter-coating with gold-palladium. The
carpological terms used are according to Werker (1997).
Results
F ruit anatomy of Anthochlamys
In cross-section the pericarp of the fruit comprises two zones (Fig. 1 B) - an outer zone
(I) of 1-3(-5) layers represented by parenchymatous unsclerified cells, and an inner zone (II) of
mechanical tissue (sclereids). The number of cell layers in zone I varies depending on the fruit
topography. In the wing area and in the central (seed-containing) part of the fruit there are 1-3
layers. In the transition zone between the wing and the seed-containing part, there are usually 3-5
layers.
The outer cells of the outer layer are mamillate (Fig. 2 A) or (mostly near the wing)
papillose (Fig. 2 B), 30-75 цш thick, except for the wing, which has smaller, flat cells (Fig. 2 C).
Fig. 2. A. Ultrasculpture of pericarp surface in the median part of A. afghanica fruit. Scale bar: 100 ц ш ;
B. Papillae in the seed-containing part of A. polygaloides fruit (near the wing). Scale bar: 100 ц ш . C.
Pericarp surface at the transition between the central part and the wing of A. multinervis fruit. Lower half:
mamillate ultrasculpture of the seed-containing fruit part; upper part: cells in the wing area. Scale bar: 100
цш
.
93
Some cells are impregnated with brown pigment (turning blue when stained with
toluidine). The cells of the inner layers of zone I are usually thinner. The mechanical tissue (zone
II) is discontinuous and present only in the wing area. In the fruit of some species one thin layer
(up to 5 pm) of sclerenchymatous parenchyma can sometimes be seen in the central part instead
of sclereids. In the wing area the sclereids are oriented in different directions. The innermost
layers (adjoining the seed coat) are oriented parallel to the fruit axis (in cross-section they appear
round). The outer layers comprising the greater part of the wing are arranged perpendicularly to
the fruit axis. The wing is always easily discernible, (0.55)0.8-1.6 mm long and appearing
narrowly triangular in cross-section. Air cavities between zone II of the pericarp and the seed
coat are either not visible or are up to 50 pm in diameter.
The seed coat is only (3)5-8 pm thick, closely attached to the pericarp and consisting of
two strongly compressed cell layers impregnated with tannins. There is abundant perisperm. The
embryo is well developed, with two cotyledons located mostly parallel or obliquely to the seed
(and fruit) surface. Rarely (in some fruit of A. polygaloides and A. tjanschanica) the cotyledons
are oriented perpendicularly to the seed/fruit axis.
The carpological characters of each species
Despite the uniformity of the topography, some pericarp characteristics can be useful for
taxonomy. The most important ones are given in Table 1. Surface topography cannot be regarded
as taxonomically important.
A. afghanica
2.5-3 х
2.7
3-3.5 x 3
0.4-0.5
2-3
55-60
30-40
0.5-0.65
1-2(3)
45-55
3.5-4.5 x
3.7-4.5
3-3.2 x 3
3.2
0.7
2(3)
0.65-0.8
2(3-4)
40-60
(-75)
50-75
(35-)
40-50
30-45
(-50)
(35-)
40-60
(-65)
A. tianschanica
3.3-5 х 3
4
0.7-1
2(3)
40-50
A. turcomanica
3.3-4 x
3.2-3.7
0.7-0.9
2(3)
55-90
A. multinervis
A. polygaloides
A. rechingeri
94
Wing length in cross-section
(mm)
Cell-wall outlines of outer
pericarp layer
Thickness of outer pericarp
layer (ц т )
Pericarp thickness in seedcontaining part of fruit (ц т )
Number of pericarp layers in
seed-containing part of fruit
Thickness of seed-containing
part of fruit (mm)
Fruit length/width ratio (mm)
Species
Table 1. Fruit characteristics of the Anthochlamys ^species
m
)
3
s
es
n
О
hti
g
iniW
+/round
+/round
+/round
+/round
0.6
0.8
0.8
1.2
0.8
1.6
0.55
0.7
70-100
30-40
(-45)
convex
or +/round
0.7
1.1
60-75
50-75
+/round
0.8-1
60-100
90-130
75-100
60-75
Small fruit diameter and small wing length are additional parameters supporting the
species level of A. rechingeri. The geographical isolation of A. tjanschanica has not led to the
evolution of fruit-structure peculiarities.
Discussion
The relationship between Corispermum and Anthochlamys
The first known Anthochlamys species was described as Corispermum polygaloides
(Fischer et al., 1835). However, since 1837, when Fenzl established Anthochlamys, its generic
status has been supported in all monographs, e.g. Volkens (1893), Ulbrich (1934), Iljin (1936),
Aellen (1950), Hedge (1997) and Kadereit et al. (2003). Even the thesis that Corispermum
patelliforme might represent a morphological link between the genera (Mosyakin, 2003) is not
supported by carpological characters (Sukhorukov, 2007).
The diversification of Anthochlamys is clearly associated with the areas (Central Iran and
Afghanistan) located to the south of all the diversity centres of Corispermum, including in
particular the ‘Nitidum’ group. In this area are found only C. lehmannianum, at the southern
edge of the area, and the endemic species C. rechingeri (compare Hedge, 1997; Sukhorukov,
2008). Moreover it can be postulated that the evolution of the genera is linked to different
substrates: the ecotopes of Corispermum are sands while Anthochlamys prefers gypsum soils or
variegated rocks. The morphological differences belong mostly to the number of perianth
segments: there are 5 prominent perianth segments in Anthochlamys and (0)1 (2-3) in
Corispermum. Another character is the convexity of the fruit (excluding the wing area):
bilaterally convex in Anthochlamys and unilaterally convex in Corispermum.
The present study shows that there are several genus-specific characters in Corispermum
and Anthoclamys (Tab. 2). There are also many characters common to them, although in some
cases they have arisen indepedently in the two genera (Tab. 3).
Table 2. New genus-specific characters in the fruit anatomy of Corispermum and
Anthochlamys.
Corispermum
Anthochlamys
Papillae if present located over all the
Papillae if present located at the edge of
seed-containing part of the fruit. Wing thickness the seed-containing part of the fruit. Wing
decreases gradually towards the top of the fruit.
thickness almost equal in all parts (except the
base and top of the fruit
Table 3. Pericarp characters common to Corispermum and Anthochlamys (but with some
features derived independently in the two genera) _____________________________________
Corispermum
Anthochlamys
Outer cell walls of outer pericarp layer (if
Outer cell walls of the outer pericarp
layer convex or semi-round. Air cavity often
not papillated) usually flat or slightly convex
(except in the ‘Declinatum’ group). Air cavity
not present in the base of the wing. Mechanical
often present in the base of the wing. Mechanical
tissue present in wing area and at edge of seedcontaining part.
tissue present in wing and mostly in seedcontaining part.
The flattened wing-like outgrowth in Anthochlamys is a rare tra it within the core
Caryophyllales
Many taxa of the order Caryophyllales (in its recent circumscription: Brockington et al.,
2009; Schaferhoff et al., 2009) growing in arid regions are characterized by diverse adaptations
for wind dispersal (e.g. Ulbrich, 1928). The dissemination of indehiscent (single-seeded) fruit is
often linked to wing-like or tuberculate appendages of the perianth, for instance in many
Chenopodiaceae (Kuhn et al., 1993), especially representatives of the subfamily Salsoloideae,
and part of Polygonaceae (Brandbyge, 1993). Sometimes the seed coat of dehiscent fruit can
95
develop flattened wing-like projections (some species of Caryophyllaceae). However, in most
cases dissemination is promoted by two or several modes, termed heterodiaspory (Sukhorukov,
2010).
Anemochory seems to be the preferred mode of dissemination in Anthochlamys, but the
fruit (without the perianth) is the only dispersal unit. In contrast to the closely related
Corispermum, the fruit wing is always prominent in Anthochlamys. This obligate presence of the
flattened pericarp outgrowth is a unique character within the entire Chenopodiaceae clade. The
study of fruit evolution in Caryophyllales sensu novo, including Polygonaceae and Limoniaceae,
shows a rare convergent tendency to develop pericarp outgrowths (Sukhorukov et al., in prep.). It
is found only in a few orders, namely in the fruit of Sarcobatus (Sarcobataceae), in some
Polygonaceae (Ronse Decraene et al., 2000), and in the nutlets of Gisekia (Gisekiaeae), but
without any similarities in anatomical structure.
Conclusions: Fruit structure in six Anthochlamys species is quite uniform, differing only
in details. Fruit diameter, length and thickness of the wing are additional parameters supporting
the recognition of A. rechingeri at the species level. The geographic isolation of A. tianschanica
has not affected the evolution of its carpological traits. The genus-specific features of
Anthochlamys have been identified. The closely related genera Corispermum and Anthochlamys
are similar in fruit anatomy, but the diversification of both genera proceeded under different
ecological and geographical conditions. Although many members of the Caryophyllales appear
to be anemochorous, it is postulated that the ‘winged’ pericarp arises only rarely in the order.
The prominent flattened wing of the pericarp is characteristic of Anthochlamys and seems to be
unique within the Caryophyllales.
This work is supported by an RFBR grant (11-04-00123a).
References
Aellen, P. 1950: Ergebnisse einer botanisch-zoologischen Sammelreise durch den Iran
1948/1949. Botanische Ergebnisse I. Chenopodiaceae: Cornulaca, Anthochlamys, Aellenia,
Horaninovia. - Verh. Naturforsch. Ges. Basel 61: 157-198.
Brandbyge, J. 1993: Polygonaceae. - In: Kubitzki, K., Rohwer, J.G., Bittrich, V., (eds.),
The families and genera of vascular plants 2. P. 531-544. - Springer Verlag, New York etc.,
Brockington, S.F., Alexandre, R., Ramdial, J., Moore, M.J., Crawley, S., Dhingra, A.,
Hilu, Kh., Soltis, D.E. & Soltis, P.S.: 2009: Phylogeny of the Caryophyllales sensu lato:
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phylogeny of Atripliceae (Chenopodioideae, Chenopodiaceae): Implications for systematics,
biogeography, flower and fruit evolution, and the origin of C4 photosynthesis. - Am. J. Bot. 97:
1664-1687.
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Appendix 1
List of specimens investigated
Anthochlamys afghanica Podlech: Afghanistan, prov. Kandahar, Keshkenakhud, X.1978,
D. Podlech 32681 (LE);
A. multinervis Rech. f.: 1) Iran, prov. Semnan, road from Semnan to Firuzkuh, alt. 1400
m, IX. 1974, I. Hedge & al. 14736 (LE); 2) Iran, Kavir Kashan, XI. 1974, Terme, Moussari
30276-E (W-02617);
A. polygaloides (Fisch. & C.A. Mey.) Fenzl: 1) Iran, Tehran prov., W of Mardabad,
IX. 1974, I. Hedge & al. 14685 (W-00441); 2) Iran, Azerbaijan prov., Mianeh, X.1974, P.
Wendelbo & Shir-delpur 14925 (W-8430);
A. rechingeri Aellen: Iran, Bahram, VIII.1948, P. Aellen s.n. (W-5425; K). Several fruits
from both specimens are used for the carpology.
A. tianschanica Iljin ex Aellen: 1) [Uzbekistan], Namangan, VII.1922, N. Androsov 66
(MW); 2) Uzbekistan, Fergana valley, Tuzul-say, VIII. 1950, A.D. Pyatayeva 258 (LE); 3)
Kyrghyzstan, Dzhalalabad prov., valley of Naryn river, VI.2000, Pimenov & al. 50 (MW);
A. turcomanica Iljin: 1) Turkmenistan, Chuli, IX.1914, I. Ivanov s.n. (LE); 2)
Turkmenistan, the same place, VI.1971, A.V. Mescheryakov s.n. (LE).
97
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