Download The delimitation of the tribe Vicieae

Botanical Journal o f t h e Linnean Society. 74: 131.162 . With 7 figures
February 1977
The delimitation of the tribe Vicieae
(Legurninosae) and the relationships of Cicer L .
FRANCES K . KUPICHA. F.L.S.
Department o f Botany. British Museum (Natural History). Cromwell Road.
London SW7 5BD
Accepted f o r publication September 1976
A survey of morphological. anatomical. karyological and chemical characters has been carried
out. centred o n the Vicieae b u t extending t o the neighbouring tribes Trifolieae and Ononideae .
The results show that Cicer. traditionally a member of the Vicieae. has more in common with
genera of the Trifolieae and Ononideae than with the rest of the Vicieae . I t is proposed that
Cicer should be removed from the Vicieae and recognized as t h e monogeneric tribe Cicereae
Alef . The tribe Vicieae sensu stricto. a well-defined natural group. is delimited and described .
Phylogenetic relationships of the Cicereae are discussed .
KEY WORDS:-Cicer-Cicereae-Vicieae-Trifolieae-Ononideae-Leguminosae-morphology-cytology-chemotaxonomy .
CONTENTS
Introduction
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Historical background
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Taxonomic characters
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Habit
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The seedling
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Germination
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Position of first leaf
. .
Ontogeny
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Vascular anatomy
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In the mature plant
. .
In theseedling
. . .
The leaf
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Leaflet shape and venation
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Stipules
Form of the mature leaf
. .
Number of leaflets
Ontogeny
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Evolution of the leaves
.
lndumentum
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Inflorescence
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Theflower
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Corolla
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Androecium
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Pollen
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Gynoecium
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The fruit
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F. K. KUPICHA
The seed
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Seed shape
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Milurn length
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Endosperm
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Vascular supply
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The liarotype: chromosome number
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Chcniosysternatics
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Anthocyanins
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Isoflavonoids
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Nowprotein amino acids: canavanine
Seed proteins
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Discussion
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T h e delimitation of the Vicieae
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Description of t h e tribe Vicieae sensu strict0
T h e taxonomic position of Cicer
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Phylogenetic relationships of Cicer
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Acknowledgements
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Rcferences
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INTRODUCTION
The tribe Vicieae contains several economically important species ( Vicia faba
L.-broad bean; Lathyrus odoratus L.-sweet pea; Pisum sativum-garden pea;
Lens culinaris-lentil and Cicer arietinum-chickpea) and consequently has been
much studied. Its members are found throughout the north temperate zone and
to a lesser extent in South America, and modern taxonomic accounts of most
of its genera have been published in Floras covering the chief centres of
distribution, as well as in monographic accounts. Despite this concentrated
activity, no-one has recently taken a broad view of the tribe, whose
delimitation is problematic. This work sets out to define the problem, survey
the available taxonomic evidence, and achieve a more natural tribal
classification.
Authorities for species are given on first mention in the text except for
species listed in Tables 3 and 5 .
HISTORICAL BACKGROUND
The first post-Linnean taxonomist to recognize the Vicieae was Adanson
(1763), who called this entity a ‘section’, and included in it Tournefort’s
genera Aphaca, Cicer, Clymenum, Ervum, Lathyrus, Lens, Nissolia, Orobus,
Pisurn and Vicia. De Candolle was the first to give the Vicieae tribal rank. He
stated (1825a and 182513: 353) that the essential characters of the tribe are 1,
germination hypogeal; 2, first plumular leaves alternate, never opposite; 3 ,
leaves epulvinate; 4, leaves paripinnate, with the rachis prolonged into a tendril,
or (in some species of Cicer) leaves imparipinnate. The genera which De
Candolle accepted as members of the tribe were Cicer L., Ervum L., Faba L.,
Lathyrus L., Orobus L., Pisum L. and Vicia L.
The number of genera into which the species of the Vicieae are grouped has
tended to decrease with time, at least until very recently. Bentham (1865: 524)
recognized six, viz. Cicer, Vicia, Lens Miller, Lathyrus and Pisum (comprising
the Vicieae sensu DC.), and Abrus L. He was uncertain whether Abrus was
correctly placed in the Vicieae, as some of its characters suggested affinity with
DELIMITATION O F THE VICIEAE-LLEGUMINOSAE
133
the Phaseoleae or Dalbergieae. Bentham’s decision to include Abrus was
followed by several taxonomists, e.g. Taubert (1894: 350), Ascherson &
Graebner (1909: 898) and Gams (1924: 1497);but on the other hand, various
workers who made comparative morphological, anatomical and karyological
studies in the Leguminosae, e.g. Streicher (1902: 493), Popov (1928-29: 236),
Senn (1938: 273) and Dormer (1946: 161), advocated that Abrus should be
excluded from the Vicieae. In the most recent generic and tribal revision of the
family Hutchinson (1964: 451) placed Abrus in its own tribe, the Abreae,
immediately before the Vicieae. Table 1 shows that the decision to separate
Abrus from the Vicieae is amply supported by the evidence of many
differential characters.
Table 1. Characters separating Abrus from the Vicieae
Abrus
1. plants usually woody
2. stems usually twining
3. first two seedling leaves opposite
4. stems not containing cortical vascular
bundles
5. phyllotaxy polymerous
6. leaves with pulvinus at base of petiole
7. stipels present
8. leaves not tendrillous
9. flowers borne in ‘pseudoracemes’
(panicles with very contracted branches),
these terminal o n leafy branches
10. vexillum united with staminal tube
11. androecium with 9 stamens
12. pollen grains with unthickened endoapertures and microreticulate
ornamentation (provisional, based o n one
specimen of A. precatorius L; cf. Clarke
& Kupicha, 1976: 43)
1 3 . style glabrous
14. germination epigeal
15. haploid chro’mosome number:
n=ll
16. chromosomes relatively small
17. geographical distribution:
pantropical
*
Vicieae
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
plants herbaceous, rarely woody
stems not twining
first two seedling leaves alternate
stems containing cortical vascular bundles
(except in Cicer)
phyllotaxy dimerous
leaves with epulvinate petiole
stipels absent
leaves often tendrillous
flowers in axillary racemes, very rarely in
panicles
vexillum free from staminal tube
androecium with 10 stamens
pollen grains with thickened endoapertures and
a widely reticulate ornamentation (except in
Cicer)
13.
14.
15.
16.
17.
style pubescent (except in Cicer)
germination hypogeal
haploid chromosome number:
n = 5, 6 , 7, 8
chromosomes relatively large
geographical distribution:
temperate Eurasia and North America,
temperate South America
Generic limits in the Vicieae are still a matter of debate. The genera which I
recognize as constituting the Vicieae sensu DC. are Cicer (whose position is
discussed in this paper), Vicia, Lathyrus, Lens, Anatropostylia (Plitm.)
Kupicha, Pisum and Vavilovia Feodorov.
Apart from the controversy over Abrus, the boundaries of the Vicieae have
remained constant since the early 19th century. At the same time, many
authors have commented o n the isolated position of Cicer within the tribe, and
have speculated on its possible relationship with other parts of the
Papilionoideae. De Candolle (1825a) himself pointed out the apparent affinity
of Cicer and Ononis L.: “The aristate peduncle is not the only similarity
between these two genera. The sharp teeth of the leaflets and stipules of Cicer,
F. K. KUPICHA
134
the form of its hairs, the arrangement of the flowers, the shape of the calyx and
corolla and the appearance of the fruit, all recall certain species of Ononis,
especially those with pinnate leaves. The swollen cotyledons and mode of
germination are the best characters to distinguish Cicer from Ononis.”
(translated).
Ononis has had a very unstable taxonomic history. In the earliest
classifications, e.g. that of Bronn (1822: 132), it was associated with members
of the Genisteae. Bentham (1865: 485) considered that Ononis belongs
somewhere between the Genisteae and Trifolieae, because it resembles the
former in its monadelphous androecium and dimorphic anthers, and the latter
in its leaflets, inflorescence and filament apices; on balance, he decided to place
Ononis in the Trifolieae. Gams (1924: 1216) believed that Ononis has no true
connections with either the Trifolieae or the Genisteae, but is an advanced
genus related to Cicer and thus indirectly to the rest of the Vicieae. However,
although he expressed this opinion, he placed Ononis in its traditional
taxonomic position. In his monograph of Ononis, Sirjaev (1932: 414)
concluded that the intermediate characteristics of this genus justified the
creation of a separate tribe, the Ononideae. Hutchinson (1964: 454) also
recognized the Ononideae; in his system it comprises Ononis and the
monospecific segregate genus Passaea Adanson (P. ornithopodioides (L.) Adanson differs from other members of the Ononideae only in having internally septate fruits, and it is treated here as a species of Ononis). According to Hutchinson,
the Trifolieae include six genera: Parochetus Buch.-Ham., Melilotus Miller,
Trigonella L., Factorovskya Eig, Medicago L. and Trifolium L. The features
which distinguish the Ononideae and the Trifolieae are listed in Table 2. I
doubt whether these differences are really sufficient t o maintain the two tribes.
However, in the present context, where I am considering the relationships of
Cicer, it is most convenient to recognize the Ononideae as a taxon parallelling
the Trifolieae sensu stricto.
Popov (1928-29: 107, 236) was impressed by the phenetically intermediate
position of Cicer between the Vicieae and Ononis, and proposed the eccentric
hypothesis that in the Paleocene epoch, Ononis appeared as a hybrid between
members of the Genisteae and Trifolieae. At this time Ononis and Vicia were
vicarious genera, separated by the Tethys sea and belonging, respectively, to a
xerophytic African and a mesophytic Asian flora. Geological and climatic
Table 2. Characters separating the Trifolieae and Ononideae
Trifolieae
androecium diadelphous
anthers monomorphic
3. anthers all versatile
4. plants never spiny
5 . inflorescence usually capitate or spicate
6 . legume not inflated, but of various
characteristic forms
7. pollen grains oblong-ellipsoid
3.
4.
5.
6.
8.
8.
1.
2.
haploid chromosome number:
n=8
1.
2.
7.
androecium monadelphous
anthers of two sizes
anthers alternately basifixed and versatile
plants often spiny
inflorescence often 1-few-flowered
legume inflated
pollen grains subspherical (Clarke & Kupicha,
1976)
haploid chromosome number:
n = 1 5 , 16 (see Table 4)
DELIMITATION O F THE VICIEAE-LEGUMINOSAE
135
changes then allowed these floras to come into contact, and crossing took place
between Vicia and Ononis; the first generation hybrid, ‘Onono-Vicia’
underwent selfing and produced a number of segregants comprising the two
parental types and four intermediates, each of which was the ancestor of one of
Popov’s four sections of Cicer. Popov decided that, in spite of its equal affinity
with Ononis, Cicer should be included in the Vicieae according to the usual
taxonomic practice.
In the light of modern evolutionary theory, this story cannot be accepted as
a serious explanation of the origin of Cicer, or any other genus; if this kind of
wide and free mixing of genetic material were possible, genera would inevitably
lose their distinctness and their status. Popov’s theory also implies that
hybridization at generic level must be common in the Papilionoideae, but this is
not the case (McComb, 1975). Several authors (e.g. Senn, 1938: 249, 273;
Simola, 1969: 655) have quoted Popov’s conclusions about the origin and
taxonomic relationships of the genus which he monographed, apparently
accepting his authority without questioning the reasoning behind these ideas.
Having examined and rejected the hypothesis which underlies his systematic
treatment of Cicer, one is left with the unsolved problem which Popov
indicated so clearly: what are the relationships of Cicer? This is the most
critical issue in the Vicieae, as presently defined.
TAXONOMIC CHARACTERS
The following paragraphs discuss all the known characters whose variation
provides evidence about the relationship of Cicer with the Vicieae, Trifolieae
and Ononideae. As there is no doubt that Cicer’s closest affinities lie within
these groups, other tribes are not considered here.
Habit
All members of the Vicieae, Trifolieae and Ononideae are herbs, ranging
from delicate, short-lived annuals to perennials with welldeveloped secondary
thickening. Cicer and Ononis are remarkable for their tendency towards
spininess, a trait not found in the other genera. The spines are variously formed
from modified stipules, leaflet-teeth, tendrils (in Cicer), bracteoles and the
sterile apex of peduncles.
The seedling
During the early part of this century many papers reported observations on
the germination of legumes, and members of the Vicieae were often
represented. It is regrettable that very little of this new information was noted
by taxonomists, and the interest in seedling characters apparently died away
leaving a residue of data about unevenly surveyed taxa, some of the findings
contradictory but some indicating that seedlings can yield significant
taxonomic characters. The following paragraphs summarize most of the
variable features found so far in the seedlings of the Vicieae and neighbouring
tribes, and show that certain patterns have emerged which are relevant to the
classification of Cicer. The recent study of Baudet (1974) in the Phaseoleae
F. K. KUPICHA
136
demonstrates that comparable variation-patterns are present in other parts of
the Papilionoideae.
Germination
All members of the Vicieae, including Cicer, have hypogeal germination,
while the Trifolieae and Ononideae are exclusively epigeal. Compton
(1912-1913: 91), who surveyed the whole of the Leguminosae for this
character, found that within the Papilionoideae the Sophoreae are mostly
hypogeal; the Podalyrieae, Genisteae, Galegeae, Loteae and Dalbergieae are
uniformly epigeal; the Hedysareae are almost entirely epigeal, and the
Phaseoleae show both types in abundance. The Vicieae are thus distinctive in
having uniformly hypogeal germination, and it is not surprising that this
character has been a heavily-weighted tribal feature.
Having observed the germination of about 20 species of the Vicieae
(Table 3 ) , I found that Cicer differs from the other genera in the direction of
growth of the radicle. In Vicia, Lathyrus, Lens and Pisum the radicle always
grows straight down past the hilum and the plumule emerges from between the
cotyledons on the side of the cotyledonary petioles away from the hilum
(Fig. l A , B). In Cicer the radicle has a variable behaviour: in some seeds it
grows past the hilum (Fig. lC, D), but in others it turns in the opposite
direction and then the plumule emerges on the hilar side of the cotyledonary
petioles (Fig. l E , F). As only two species of Cicer have been studied for this
character it is not known whether the variable direction of radiclegrowth is a
constant generic feature. It would be interesting to complete the survey and to
extend it to the neighbouring tribes.
Position of first leaf
My observation of the species listed in Table 3 showed that in Vicia,
Luthyrus, Lens and Pisum the first leaf of the plumule, which is a small
scaIe-leaf, is always borne on the side of the epicotyl away from the cotyledons
(the ‘convex’ side of the shoot). This fact was noted by van Tieghem (1871:
220) and Compton (1912-13: 86, 107). The illustrations of seedlings of the
Table 3. Species of the Vicieae in which the first-leaf position in the
seedling has been observed
Cicer arietinum L.
CC, CV
C. pinnatifidum Jaub. & Spach
Lathyrus cicera L.
CV
L . inconspicuus L.
CV
L. nissolia L. CV
L . tingitanus L.
CV
L. sphaericus Ketz. CV
Lens culinaris Medicus
Pisum sativum L.
CV
CV
CC, CV
Vicia americana Miihl. e x Willd.
V. amurensis Oettel
CV
V . anatolica T u r d
CV
V . biennis L. CV
V. bithynica (L.) L. CV
V. cracca L. CV
V. dumetorum L.
CV
V. ervilia (L.) Willd. CV
V . hybrida L. CV
V. lutea L. CV
V. peregrina L. CV
V. pubescens (DC.) Link CV
V . sativa L. CV
CC, first scale-leaf on concave side of plumule; CV, on convex side.
CV
DELIMITATION O F THE VICIEAE--LEGUMINOSAE
137
Vicieae in Csapody (1968: 261-265) show most with the first scale in this
‘convex’ position; in the remaining cases, it may be that the plumules were
twisted or drawn from a misleading angle. There is disagreement in the
literature about the situation in Cicer: van Tieghem (1871: 219) said that in C.
arietinum the first leaf is inserted on the side of the plumule nearest the
cotyledons (the ‘concave’ side), while Muller (1937: 203) stated that it is
produced on the convex side. I found that in both C. arietinum and C.
pinnatifidum the first leaf varies in position; in some seedlings it is on the
convex side of the plumule, in others it is on the concave side. As the radicle
may grow either past or away from the hilum, there are four possible kinds of
seedling, and these are illustrated in Fig. 1C-F.
Compton apparently did not observe the germination of any species of Cicer,
for he concluded that the Vicieae have a very uniform pattern of germination,
characterized by the constant insertion of the first leaf on the convex side of
the plumule. He emphasized this, and contrasted the Vicieae with the
Hedysareae, Galegeae, Trifolieae and Loteae, whose members, with few
Figure 1. Germinating seeds; in each seedling the first plumular leaf is indicated by an arrow. A ,
Vicia f a b ~ B,
; Lens culinaris: in A and B the first leaf is borne on the “convex” side of the
shoot. C-F, Cicer pinnatifidum: in C and D the radicle grows past the hilum, in E and F it
grows away from the hilum; in C and F the first leaf is borne towards the cotyledons, in D and
E it is borne away from the cotyledons. G-I, Trigonella foenum-guuecum: G , diagrammatic
longisection of seed (endosperm not drawn), with the ‘convex’ side of the cotyledon marked
with a dot; H and I , seedlings with the first leaf appearing in opposite positions. Not to scale.
138
F. K . KUPICHA
exceptions, were believed to have the first leaf inserted on the concave side of
the epicotyl (Compton, 1912-13: 107). This character is difficult to observe in
epigeal seedlings, because once the testa has been shed from the cotyledons
these straighten up and become completely symmetrical, leaving no indication
of their original orientation in the seed. In order t o discover the spatial
relationship of the cotyledons and the first leaf one must mark the cotyledons
during germination to preserve their initial asymmetry. I have followed the
germination of only one species outside the Vicieae, Trigonella foenumgraecum L.; it was found that the first leaf is sometimes borne on the concave
side of the plumule, sometimes on the convex side (Fig. l H , I). This suggests
that the Trifolieae may be characterized by a variable first-leaf position rather
than a constant concave-side insertion as Compton postulated, and in this case
Cicer would resemble the Trifolieae in this character.
The invariable position of the first leaf in the Vicieae (apart from Cicer) is
correlated with a very uniform type of vascular symmetry in seedlings of this
group (Compton, 1912-13: 86). The root and hypocotyl are triarch; two of the
protoxylem strands supply the cotyledons, which are borne at an angle of
120°, while the third continues in the plumule to become the median trace to
the first scale-leaf. Cicer arietinum, however, is tetrarch, and the cotyledons are
inserted at 180" (Muller, 1937: 203). The presence of two intercotyledonary
protoxylem strands in Cicer may explain why the first leaf is able to appear on
either the concave or convex side of the plumule. This relationship between
primary vasculature and leaf-insertion is not absolute, however; Vicia faba,
which always has the first leaf on the convex side of the plumule, is exceptional
in having tetrarch seedlings (fide Compton and Muller).
The situation in the Trifolieae and Ononideae may not be strictly
comparable with that in the Vicieae; according t o Compton (1912-13: l O l ) , in
their slender epigeal seedlings the protoxylem of the cotyledons, hypocotyl and
radicle forms a self-contained unit and is only connected by metaxylem with
protoxylem of the plumule (Erith (1924: 14) disagreed with Compton in the
case of Trifolium repens L. and stated that in this species there is a protoxylem
connection between radicle and plumule). Compton found that in the
Trifolieae and Ononideae the seedling vasculature has an unstable symmetry,
varying from tetrarch to triarch or diarch often within a species or even at
different levels in the axis of a single specimen. If there is a causal relationship
between the vascular symmetry of the embryo and the position of early leaves
on the plumule, these data would be consistent with a variable first-leaf
position in the Trifolieae and Ononideae. No firm taxonomic conclusions can
be drawn from the information available on this subject at present; a more
thorough survey in these tribes is needed to elucidate the situation.
Ontogeny
In seedlings of Vicia, Luthyrus, Lens and Pisurn the primary shoot rarely
attains more than a few inches in height before its growth ceases, and the bulk
of the plant is formed from vigorous secondary branches arising from the axils
of the scale leaves at the lowest nodes (Vicia faba and its close relatives are
exceptional in having indeterminate primary stems). My observations on Cicer
arietinum, C. pinnatifidum and C. anatolicum Alef. show that in these species
the plumular shoot continues to develop throughout the growing season,
DELIMITATION O F THE VICIEAE-LEGUMINOSAE
139
although the basal nodes often give rise to lateral branches which may overtop
the primary stem. This aspect of ontogeny is difficult to measure in herbarium
specimens, and without further studies on living material I cannot tell whether
the apparent difference in growth-pattern between Cicer and the rest of the
Vicieae has any significance. I have no parallel information about ontogeny in
the Ononideae and Trifolieae. I t would be very interesting to know if there is
systematic variation in this character within or between these tribes.
Vascular anatomy
In the mature plant
In Cicer and members of the Trifolieae and Ononideae the three leaf-traces
which supply each petiole are all emitted from the main stele at the same level
(Fig. 2C, D; see also Winter, 1932). The remaining genera of the Vicieae are
M
M
Figure 2. Cauline vascular systems in the Vicieae. A-B, Viciu f a b u : A, diagrammatic
reconstruction of nodal vascular anatomy, showing supply to stipules and petiole (for simplicity
the main stele is drawn as a solid cylinder); B, transverse section through internode, showing the
stele as a ring of primary bundles with two additional cortical bundles. C-D, Cicer ariefinum: C,
reconstruction of nodal vascular anatomy; D, transverse section through internode, showing
absence of cortical bundles. L, Lateral leaf-trace; M, median leaf-trace; S, traces to stipules;
Bud, traces t o the axillary bud.
140
F. K. KUPICHA
characterized by an unusual type of cauline vasculature in which the lateral
leaf-traces are present in the internode below the insertion of each leaf as a pair
of cortical bundles (Fig. 2A, B; see also Kupicha, 1975). This important
difference between Cicer and the rest of the Vicieae has been pointed out by
several authors, e.g. van Tieghem (1884a: 1 3 3 ) , Hkrail (1885: 223, 306) and
Dormer (1946: 161), but as yet it has had no influence on the tribal
classification.
In the seedling
The seedlings of Vicia, Latlzyrus, Lens and Pisum are remarkable in having a
very prolonged transition region between root and stem. The first two plumular
internodes contain a solid core of xylem which is exarch in the first internode
above the cotyledons; the construction of the shoot becomes progressively
more stem-like with the emission of successive endarch median leaf-traces to
the first, second and third scale-leaves (Compton, 1912-13 ; Gourley, 1931;
Muller, 1937). (The lateral leaf-traces are supplied from the two cortical
bundles which are given off from the cotyledonary leafgaps, as described by
Kupicha, 1975 .) This situation is anomalous within the Leguminosae and
among dicotyledons in general. Compton suggested that the rootlike structure
of the young epicotyl may be an adaptation enabling this region to bend, in
relation to the climbing habit of the Vicieae. His hypothesis may be supported
by the fact that Vicia faba, which has-a medullated and therefore stiffer
transition region, is a non-climber with etendrillous leaves. According to Muller
(1937), in Cicer ilrietinum the transition region between root and stem is in the
normal hypocotyledonary position and there is neither a solid core of xylem
nor any exarch protoxylem in the epicotyl; in this respect Cicer resembles the
Trifolieae and Ononideae, as far as is known.
The leaf
Leaflet shape and venation
Cicer, and genera of the Trifolieae and Ononideae, typically have serrate
leaflets in which the lateral veins end blindly in the marginal teeth (Fig. 3B).
This kind of venation is termed craspedodromous (Stearn, 1966: 541). Many
Figure 3. Leaflet shape and venation. A, Vicia sepium L.: entire leaflet with brochidodromous
venation. B, Cicer anatolicum: serrate leaflet with craspedodromous venation.
DELIMITATION O F T H E VICIEAE-LEGUMINOSAE
141
species of the Trifolieae have entire leaflets, but the venation type is constant
throughout the tribe. Craspedodromous venation is rare in the Papilionoideae;
as far as I know, it is confined to these groups.
In contrast, the remaining genera of the Vicieae are characterized by entire
leaflets with the very common brochidodromous venation pattern in which
each lateral nerve curves towards the apex as it approaches the margin and
unites with its neighbour (Fig. 3.4). A very few taxa have serrate leaflets (e.g.
Vicia grandiflora var. dissecta, V. serratifolia Jacq.), but here the teeth are not
provided with a main vein as in Cicer.
Stipu lcs
The Trifolieae and Ononideae have leaves with the stipules adnate to the
petiole; in all members of the Vicieae, including Cicer, the stipules are free.
Form of the mature leaf
The most striking vegetative feature of the Vicieae is their tendrillous leaves.
Tendrils are absent from the rest of the Papilionoideae, and their occurrence in
this group, coupled with the almost equally unusual hypogeal type of
germination, has been thought of overriding significance in considerations
about tribal limits in this area of the subfamily.
Although tendrils are so characteristic of the tribe Vicieae, many species are
etendrillous. In Vicia, Lathyrus and Vavilovia, species with etendrillous adult
leaves almost always have paripinnate leaves in which the rachis ends in a
mucro; only a very few species of Vicia (V. abbreviata Fischer ex Sprengel, V.
argentea Lapeyr., V. serniglabra Rupr. ex Boiss. and V. subvillosa (Ledeb.)
Trautv.) have leaves with a terminal leaflet. By contrast, in Cicer there are no
species with paripinnate leaves; here the leaves are either tendrillous or
imparipinnate. As will be shown, this difference between Cicer and the rest of
the Vicieae is also reflected in disparate patterns of foliar ontogeny, and the
latter in turn suggests that the two groups are at different stages with respect to
the evolution of tendrils.
Number of leaflets
Most species of Cicer have multijugate leaves, although C. incisum (Willd.) K.
Maly has leaves with 3-7 leaflets and C. chorassanicum (Bunge) Popov is
uniformly trifoliolate. The rest of the Vicieae vary widely from unijugate to
multijugate. Apart from a few species in Trifolium sect. Lupinaster with
palmately 5-9-foliolate leaves, the Trifolieae are all trifoliolate. Ononis includes
a few species with pinnate leaves (e.g. 0.fruticosa L.), but most of its members
have leaves with one or three leaflets.
Ontogeny
Having observed seedlings of some 70 species of the Vicieae, I found that
ontogeny in the tribe is very uniform; all genera, except for Cicer, are
characterized by the same pattern of development. The first two or three nodes
of the seedling bear a trifid scale-leaf. The next leaf comprises a pair of stipules,
a petiole and a pair of leaflets, the rachis ending in a minute point (Fig. 4A:
J l ) . In species with unijugate etendrillous adult leaves (e.g. Lathyrus roseus
Phil., Vicia unijuga A. Braun and Vavilovia formosa (Steven) Fedorov) further
F. K . KUPICHA
142
P
Figure 4. Ontogenetic leaf-series. A, Vicia melnnops Sibth. & Sm. B , Cicernnarolicum. J1, First
juvenile leaf of the plumule (which follows two or three scale-leaves); 54 and J5, fourth and
fifth juvenile leaves; M, mature leaf. Scale: x * j 3 .
development towards the mature leaf-form simply involves an increase in size.
In other species successive juvenile leaves have additional pairs of leaflets, while
the rachis is extended past the distal pair and becomes tendril-like, until the
mature multijugate tendrillous leaf is achieved (Fig. 4A: J5,M). There are two
exceptions to this normal pattern of ontogeny. Firstly, Lathyrus includes four
species (L. clymenum, L. gloeospermus Warb. & Eig, L. ochrus (L.) DC. and L.
nissolia) in which the juvenile leaves are phyllodes; in the first three, adult
leaves develop leaflets, but in L. nissolia the phyllodic condition persists
throughout. Secondly, as mentioned above, there are a few species of Vicia
with imparipinnate leaves. I have seen the development of only one of these, V.
semiglabra. Among a small sample of seedlings it was found that the first true
leaf varied in construction from trifoliolate to more rarely unifoliolate or
unijugate. In every case successive leaves were imparipinnate, but, especially in
the lowest ones, the terminal leaflet was slightly asymmetrically placed,
suggesting that the leaf might be secondarily imparipinnate, the distal leaflet
having been displaced from a lateral position. There was, however, no sign of a
mucro at the end of the rachis, and the distal leaflet was apparently truly
terminal.
In Cicer, the first leaf to appear after the scales of the earliest nodes always
has two or more pairs of lateral leaflets and a terminal leaflet (Fig. 4B: J 1). (I
have observed this in C. anatolicum, C. arietinum and C. pinnatifidum, while
L.J.G. van der Maesen (pers. comm.) has very kindly supplied information
DELIMITATION OF THE VICIEAE-LEGUMINOSAE
143
about C. bijugum K. H. Rechinger, C. chorassanicum, C. judaicum Boiss., C,
pungens Boiss. and C. microphyllum Royle.) In tendrillous species of Cicer the
terminal leaflet is replaced by a tendril in leaves of the adult plant (Fig. 4B: M).
In several species, e.g. C. anatolicum, C. baldskuanicum (Popov) Lincz., C.
graecum Orph. ex Boiss. and C. songaricum Jaub. & Spach, this transition may
be represented in intermediate leaves by the presence of leaflets whose midribs,
and sometimes even the lateral veins, are produced into rudimentary tendrils.
Evolution of the leaves
I t is generally agreed that the ancestral form of leaf in the Papilionoideae was
imparipinnate, with many pairs of lateral leaflets, and this has been stated
specifically in connection with the Vicieae by van Tieghem (1884b: 339) and
Reinke (1897: 553), who said that the tendrils in this tribe evolved by
modification of the terminal and lateral leaflets. Simola (1968: fig. 22) and
Bassler (1973: fig. 3) both believe that the appearance of paripinnate adult
leaves in Lathyrus is an advanced feature, being due to loss of the terminal
tendril. I concur with these authors, but I suggest that if, in addition, patterns
of ontogeny are used to interpret the evolution of leaves in the Vicieae, the
conclusions are more interesting and have a bearing on the relationship of Cicer
with the other genera.
Since the supporting function of tendrils is much more relevant to the adult
plant than the seedling, it seems reasonable to suppose that the selection of
tendrils was focused on the adult stage of the life-cycle and that the occurrence
of reduced, paripinnate leaves in seedlings of Vicia, Lathyrus etc. is a secondary
effect consequent on the evolution of tendrils in mature leaves.
I t seems apparent that in all genera of the Vicieae apart from Cicer the
evolutionary reduction sequence ‘leaves imparipinnate -+ tendrillous +.paripinnate’ has influenced the entire ontogenetic development of the plants so
that the juvenile leaves show the most reduced and specialized form
(Fig. 4A: J1). In species with unijugate mucronate adult leaves, paedomorphosis maintains this simple state throughout the life of the plant. In species
with multijugate and/or tendrillous adult leaves, the more primitive, more
elaborate type of leaf develops towards maturity.
In Ciceu, however, the evolutionary specialization of adult leaves is curtailed
at the tendrillous stage (i.e. ‘leaves irnparipinnate
tendrillous’), and this
trend has only influenced the later part of the ontogenetic pathway; in
tendrillous species of Cicer the juvenile leaves are more primitive in form than
the adult leaves (Fig. 4B).
The occurrence of a few species of Vicia with imparipinnate leaves and a
Cicer-like ontogeny is interesting and problematic. These species are not all
closely related, and they are not particularly primitive within the genus
(Kupicha, 1976). I t is conceivable that they are secondarily imparipinnate. On
the other hand, they may represent isolated examples of the ancestral
condition in the Vicieae.
--+
Indumentum
The different kinds of hair found in the Vicieae have been described by Shah
& Kothari (1973), and I agree with their observations. The following account
144
F. K . KUPICIIA
amplifies their data, which were based on only a few species, and broadens the
survey to include the neighbouring tribes. I have examined most species of the
Vicieae, and many of the Ononideae and Trifolieae.
Most members of Vicia, Lathyrus, Lens, Pisum, Vavilovia and Anatropostylia
have sparsely hairy leaves, the hairs usually being most abundant on the lower
epidermis and along the midvein of the leaflets. The indumentum in these
genera is of three types, comprising unicellular hairs (Fig. 5C) and short-stalked
glands (Fig. 5A, 13). The simple hair varies considerably in length but is
otherwise very uniform, having a thin wall which is always smooth. I t arises
from an isodiametric, straight-walled cell which projects slightly above the
general level of the epidermis. At the base of the hair is often found a
granular cytoplasmic body which can falsely give the impression of a separate
cell. Pisum and Lathyrus tend to have nearly glabrous leaves; in Vicia and Lens
they are more densely hairy. Occasional species (e.g. Lathyrus macropus Gill.,
Vicia canescem Labill., Lens montbretii Fischer & Meyer) have villous leaves.
Vicia lutea, and a few species of Lathyrus (L. trachycarpus Boiss., etc.) have
legumes with tuberculate-based hairs. The hairs themselves are of the same type
as that shown in Fig. 5C, but the epidermal cell subtending each hair is
produced into a prominent tubercle. The glandular hair illustrated in Fig. 5A is
as widely distributed as the simple hair, occurring sparsely on the leaves of
most species, and on the young legumes of some members of Lathyrus. The
cells of the head, which contain dense, brownish, granular cytoplasm, are
usually eight, and there is always a single stalk cell. The glandular hair shown in
Fig. 5B was found in only two species, both in Lathyrus: on the young shoots
of L. odoratus, and on the fruits of L. cassius Boiss.
Figure 5 . The different types of indumentum found in the Vicieae, Ononideae and Trifolieae. A
and B, Short-stalked glandular hiars; C, unicellular, smooth-walled hair; D, unicellular,
papillate-walled hair; E, long-stalked glandular hair; F, multicellutar hair.
DELIMITATION OF THE VICIEAE-LEGUMINOSAE
145
The remaining genus, Cicer, is very distinct within the tribe in possessing
glands with multicellular stalks (Fig. 5E). These trichomes have been studied in
detail by Schnepf (1965). Their exact form and dimensions vary considerably,
due both t o specific differences and to their stage of growth. It was observed
that they grow acropetally, beginning as a simple filament; the distal cell then
starts to divide both transversely and longitudinally, until the mature head is
formed. The hair arises from a large, convex cell which protrudes above the
neighbouring cells of the epidermis, and the cuticle is wrinkled up around it.
While this type of hair is confined to Cicer within the Vicieae, it is found
also in the Ononideae and some species of Medicago and Trigonella. This
distribution pattern (Table 4) is one of the strongest lines of evidence from
vegetative characters suggesting that Cicer is related to the Ononideae and
Trifolieae. It is interesting that this unusual glandular hair is associated with the
equally rare craspedodromous type of venation.
Unfortunately, however, the taxonomic evidence provided by indumentum
is not straight-forward. Besides the long-stalked glands, Cicer also has simple,
smooth-walled hairs like those of the rest of the Vicieae (sometimes these have
very thick walls, as in C. incisurn). Members of the Trifolieae also have simple
hairs, but my survey has shown that these always have papillate walls (Fig. 5D),
and the basal cell does not project above the surrounding epidermis as in the
Vicieae. In Ononis there are no simple hairs, only multicellular hairs (Fig. 5F)
which are obviously related t o the long-stalked glands. Multicellular hairs are
not found in Cicer, but occur in some species of Medicago. The short-stalked
gland (Fig. SA) occurs throughout the Vicieae, Trifolieae and Ononideae, and is
of no systematic value within them.
Table 4 shows that the distribution patterns of these indumentum types are
taxonomically very interesting. On one hand, Cicer is linked with the
Ononideae and Trifolieae by the long-stalked glands; on the other, the
microcharacter involving the wall-structure of the unicellular hair (smooth or
papillate) supports the present systematic arrangement. The absence of simple
Table 4. Distribution of indumentum types
Genus
A
Vavilo via
Pisum
L a thyrus
A nu tropostylia
Lens
Vicia
Cicer
+
Ononis
Medicago
Trigonella
Melilotus
Parochetus
Trifolium
-, Indicates hair-type absent;
members of the genus.
11
B
Types of hair (as in Fig. 5)
C
D
E
F
+
+
+
+
+
+
-
+
+
+
+
(+)
+
+
+
+
+, hair-type present in all species;
(+), hair-type present in only some
146
F. K. KUPICHA
hairs in the Ononideae and the limited distribution of the multicellular hairs are
further complicating factors.
Inflorescence
The inflorescence in the Vicieae, Trifolieae and Ononideae is basically
racemose. In each tribe there is a complete range from few- t o many-flowered
peduncles, and this variation does not provide any guide to Cicer’s affinities,
despite the statement of De Candolle (1825a) that Cicer and Ononis have
similar inflorescences. This is true, but the same type occurs in the rest of the
Vicieae and in some members of the Trifolieae.
The flower
Corolla
The flowers of Cicer have petals of simpler shape than those of the rest of
the Vicieae, apart from the smallest-flowered autogamous species of Lathyrus
and Vicia (e.g. L. gloeospermus, V. hirsuta (L.) S . F . Gray). In Cicer the wing
petals are completely free from the keel (Popov, 1928-29: 22; van der Maesen,
1972), whereas in the other genera these parts are interlocked, as described by
Kupicha (1973, 1976). The Ononideae and Trifolieae resemble Cicer in this
respect; many members of these tribes, however, have flowers of more
specialized construction than Cicer, as exemplified by the ‘medicaginoid’
corolla found in Medicago and parts of Trigonella and Ononis and by the
situation in Trifolium where the petals are often adnate to the staminal tube
(Townsend, 1974).
Androecium
Although the androecium is a relatively inconspicuous part of the plant, its
variation was noted and emphasized by early taxonomists such as Bentham
(1865) in their comments on the delimitation of leguminous tribes. The aspects
which vary are: the staminal tube (monadelphous, completely diadelphous or
with vexillary stamen lightly adnate to the filament tube); the filaments
(tapering or dilated at the apex); anther size (monomorphir or dimorphic) and
anther attachment (basifixed or dorsifixed). The distribution of these different
character-states has been described by many authors, especially Bentham
(1865), Popov (1928-29), Hutchinson (1964), van der Maesen (1972),
Townsend (1974) and Gunn & Kluve (1976), although none has considered
them all together in this context.
The Vicieae are all diadelphous. In Cicer the vexillary stamen has a terete
filament which is completely free from the other nine, but in the remaining
genera this adaxial filament is flanged and lightly adnate to the others so that
the androecium is functionally monadelphous, at least until the vexillary
filament is pushed away by the expanding fruit (Kupicha, 1976). The
Ononideae are remarkable in being truly monadelphous, with the partial
exception of some species of Ononis (e.g. 0 . rotundifoliu L.) in which the
vexillary filament is united with its neighbours only at the base. The Trifolieae
are diadelphous (Townsend, 1974), although according t o Hutchinson (1964)
DELIMITATION O F T H E VICIEAE-LECUMINOSAE
147
the vexillary filament may be united with others in the middle, presumably as
in Vicia, etc.
In Vicia, Lathyrus, Lens and Anatropostylia the filaments are all slender, and
taper towards the apex. I found that Pisum and Vavilovia have alternate
filaments dilated at the apex, although other workers have stated that they are
all more or less dilated (Townsend, 1974) or linear except for the adaxial one,
which is dilated (Gunn & Kluve, 1976). Cicer typically has all or most of the
filaments swollen (van der Maesen, 1972; Gunn & Kluve, 1976). In the
Ononideae all or alternate filaments are swollen (Popov, 1928-1929). Trifolium
often has dilated filaments, but in the rest of the Trifolieae they are slender
(Townsend).
The Vicieae, including Cicer, and the Trifolieae have anthers of uniform size.
The Ononideae, however, have alternately large and small anthers (Bentham,
1865; Townsend, 1974).
The Vicieae, apart from Cicer, and the Trifolieae have versatile anthers, while
the Ononideae characteristically have alternate anthers basifixed and versatile.
Cicer seems to be variable in this respect, some species having uniformly
versatile anthers and others having them alternately basi- and dorsifixed (van
der Maesen, 1972).
Although the significance of these androecial details is obscure, the fact that
genera tend to be constant in their possession of each state suggests that they
may have some systematic value.
Pollen
A paper describing the pollen of the Vicieae, Trifolieae and Ononideae has
recently been published (Clarke & Kupicha, 1976). It was concluded that the
pollen of Cicer is quite distinct from that of the rest of the Vicieae and the
Trifolieae but is like that of the Ononideae. Unfortunately, we overlooked the
earlier paper of Gapotchka (1974) which covered very similar ground. This
author argues that the distinctive pollen of Cicer is evidence for recognizing a
separate tribe, the Cicereae.
Gynoecium
Except for members of Cicer, all species of the Vicieae have pubescent styles
which are usually flattened either dorsally or laterally and are held
approximately at right angles to the ovary (Kupicha, 1973, 1976). By contrast,
in Cicer the style is terete and glabrous and curves gently away from the end of
the ovary (van der Maesen, 1972). In all of these characteristics the gynoecium
of Cicer resembles those of the Ononideae and Trifolieae.
The fruit
Cicer has inflated fruits very similar to those of Ononis. Vicia and the rest of
the Vicieae have fruits of rather uniform shape which are typically laterally
compressed; they may be subtorulose (as in V. ervilia) but are never as inflated
as in Cicer. The Trifolieae are remarkable in the diversity of their legumes,
whose variation is useful for generic identification, but none of the fruits is like
those of Cicer and Ononis. Illustrations of these fruits can be seen in van der
Maesen (1972), Townsend (1974) and Kupicha (1976).
148
F. K. KUPICHA
The seed
The leguminous seed has been described in detail by Corner (195 l ) , and the
terms used here for the details of seed morphology and anatomy are taken
from his paper.
Seed shape
?‘he seeds of the Vicieae, with the exception of Cicer, are compressed,
spherical or oblong (though often slightly angled through contact with
neighbouring seeds in the ovary), with only a slight ridge marking the position
of the radicle. The latter is fairly long and curved and lies closely against the
cotyledons (Fig. 6A). Seeds of Cicer, on the other hand, are grooved between
the two cotyledons and the short conical radicle causes a beak above the
micropyle (Fig. 6B). Corner described the radicle of Cicer as “short and
straight”, and he likened it t o the median radicle of the mimosoid-caesalpinioid
seed in contrast t o the “long curved radicle typical of the bean seed”. I
consider, however, that the Cicer radicle is not truly of the mimosoid type, but
E x t e r n a l appearance o f seed
V a s c u l a r supply
o f seed
Seed w i t h
testa removed
Figure 6. Secds of the Vicieae, Ononideae and Trifolicae. A, Vicia sativu; B, Cicer ariefinurn;C ,
Ononis repens; D, Medicago rugosa. c, Cotyledon; ch, chalaza; e, endosperm; h, hilum; 1, lens;
m, micropyle; pvb, post-chalaza1 vascular bundle; rvb, recurrent vascular bundle. Not to scale.
Note: the lens is not invariably above the chalaza; in members of Vicia sect. Hypechusa the
chalaza is in the normal position near the hilum, b u t the lens is situated on the other side of the
seed (Kupicha, 1976: fig. 6b).
DELIMITATION O F T H E VICIEAE-LEGUMINOSAE
149
is similar to that of the rest of the Vicieae, because its axis is turned at right
angles to that of the cotyledons rather than being in line with them. The seeds
of the Ononideae and 'l'rifolieae are strongly beaked and have long, curved
radicles which are not appressed to the cotyledons (Fig. 6C, D).
Hilum length
The genera of the Vicieae, apart from Cicer, have more or less linear hila
which range from & to 3 of the seed circumference; I found that, in general,
perennial species tend to have longer hila than annuals (Kupicha, 1976; this is
also shown by Gunn, 1970). By contrast, Cicer and genera of the Ononideae
and Trifolieae have seeds with uniformly small elliptic or suborbicular hila
(Fig. 6B, C, D), and this appears to be the common condition in the
Papilionoideae.
Endosperm
Although members of the Vicieae have endosperm in the developing seed, as
shown by Maheshwari (1950: 257), this tissue is broken down as the seeds
reach maturity and the cavity within the testa becomes entirely filled by the
cotyledons and radicle (Fig. 6A, B). The absence of endosperm in seeds of the
Vicieae is related to their hypogeal mode of germination in which the
cotyledons remain in the testa and are modified to act as food stores.
There is some disagreement in the literature about the situation in the
Ononideae and Trifolieae. Lubbock (1892: 411) and Erith (1924: 4) stated,
respectively, that seeds of Ononis ultissirna Colm. and Trifolium repens are
exalbuminous. I have observed, however, that seeds of the Ononideae and
Trifolieae contain a tough hyaline endospermous sheath round the embryo,
which readily imbibes water, becoming swollen and mucilaginous (Fig. 6C, D).
The survey of Reid & Meier (1970) confirms that this tissue is present in
species of Medicugo, Melilotus, Trifoliurn and Trigonella. Reid (1971) found
that the endosperm of Trigonella foenum-graecurn is composed of large,
thin-walled cells completely filled with the polysaccharide galactomannan,
which is degraded during germination. I t is this storage carbohydrate which
gives the seeds of the Trifolieae (and presumably the Ononideae) their
characteristic mucilaginous property.
Vascular supply
According to my investigations in some 30 species of the Vicieae (Table 5 ) ,
in members of this tribe there is a long post-chalaza1 vascular bundle in the
antiraphe. In Cicer the trace dichotomizes at a point about opposite the chalaza
(i.e. on the other side of the seed), and its branches run laterally in the testa,
often dividing again (Fig. 6B). This pattern of seed vasculature was observed by
Kuhn (1928: 347). In the other genera of the tribe there is always a simple,
unbranched vascular bundle forming a hoop round the periphery of the seed
(Fig. 6A). I d o not agree with Kuhn, who stated that in Vicia faba this trace
divides weakly at its extremity. In the Ononideae and Trifolieae (judging from
the small sample in my survey) the seeds have a very short vascular bundle
which ends at the chalaza (Fig. 6C, D).
F. K. KUPICHA
150
Table 5 . Species in which the seed vasculature has been observed
Cicer arietinum L. F
C. pinnatifidum Jaub. & Spach
F
Lathyrus annuus L. S
L. aphaca L. S
L. blepharicarpus Boiss. S
I,. clymenum L. S
L. gorgoni Parl. S
L . hirsutus L. S
L . niger (L.) Bernh. S
L . nissolia L. S
L. rotundifolius Willd. S
I,. sariwus L. S
L. sphaericus Retz. S
L . tingitanus L. S
Lens culinaris Medicus
S
Vicia anatolica Turrill
V. articulata Hornem.
V. benghalensis L. S
S
S
A, Post-chalaza1 vascular bundle absent;
S, simple.
Vicia bithynica (L.) L. S
V. cuspidata Boiss. S
V.graminea Smith S
V . grandiflora Scop. S
V. hyrcanica Pischer & C . A. Meyer
V. meianops Sibth. & Sm. S
V. michauxii Sprengel S
V. pannonica Crantz S
V . peregrina L. S
V. sativa L. S
V. villosa Roth S
S
Ononis repens L. A
0. spinosa L. A
Medicago rugosa Desr.
A
Melilotus alba Medicus
A
Trifolium constan tinopolitanum
Ser. A
F , S , post-chalaza1 bundle present: F, forked;
The karo type: chromosome number
The distribution of chromosome numbers throughout the Leguminosae was
discussed by Senn (1 9 3 8), and subsequently Turner & Fearing ( 1 95 9) provided
a modified phyletic interpretation of chromosome number relationships within
the Caesalpinioideae and Papilionoideae. These authors suggested that the
Papilionoideae evolved from caesalpinioid ancestors along two main lines: one,
characterized by the base number 1 1 , led to the Phaseoleae and Dalbergieae
and parts of the Galegeae and Hedysareae; the other, with primitive base
number 8, gave rise t o the ‘Galegeae complex’: Genisteae, Loteae, Trifolieae
and Vicieae, together with the rest of the Hedysareae and Galegeae. The
Podalyrieae and Sophoreae, with x = 9, formed a third branch connected to the
Galegeae complex.
Many authors have noted the usefulness of chromosome numbers as a simple
taxonomic character. Darlington (1956: 102) said that where the numbers are
constant they can reveal ancestry or phyletic lines: “they label whole tribes,
families or orders”. The situation in the region of the Vicieae is not as
straightforward as this but even so the pattern of variation of chromosome
numbers does provide useful taxonomic evidence.
Table 6 shows the haploid chromosome numbers ( n ) found in genera of the
Vicieae, Ononideae and Trifolieae. It was compiled from data given by
Darlington & Wylie (1955), Cave (1958-60 and 1961-651, Ornduff (1967 and
1968), Moore (1973 and 1974), van der Maesen (1972) and Contandriopoulos
e l al. ( 1 972). Several interesting facts emerge from the table. Vicia, Lathyrus,
Lens and Pisum are characterized by n = 7 ; some lower numbers are found but
n = 8 is completely absent. The genera of the Trifolieae are characterized by
y1 = 8, with only a small spread of lower and higher numbers. Polyploidy is
28
2
8
3
1
1
6
11
53
2
51
1
41
5
8
14
23 113
20
8
7
1
4
9
10
1
1
I1
4
4
1
1
12
13
5
1
1
5
1
3
I4
16
1
18
1
9 1 2
14
15
1
17
1
18
19
1
20
21
2
22
23
5
2
24
25
26
27
1
1
28
29
1
30
31
2
4
32
N o t e . The scores indicate the approximate number of species in each genus having a particular value for n , as reported in the literature. When a species was
recorded as having two or more values for n , each of these values was scored as if equivalent to the single value of a species yielding only one haploid
chromosome number. The report of 2n = 16 for Vicia faba in Moore (1973)is erroneous.
Pisum
La f hyrus
Lens
Vicia
Cicer
Ononis
Medicago
Trigonella
Melilo tus
Trifolium
n=5
Table 6. Cliromosome numbers in the Vicieae, Ononideae and Trifolieae
152
F. K. KUPICHA
relatively infrequent in these two groups. The indices for Cicer are striking, as
they show this genus with a strong representation of both YZ = 7 and IZ = 8,
typical of neither the rest of the Vicieae nor the Trifolieae, but intermediate
between them! Here again there is little polyploidy. The Ononideae prove t o be
quite distinct; they are entirely polyploid, predominantly with ii = 15 and 16.
According to the hypothesis of Turner & Fearing, the Vicieae, belonging to
the ‘Calegeae complex’, have x = 8 as the ancestral base number. This number,
however, is apparently unrepresented in Vicia, Lathyrus, Lens and Pisum,and
so i suggest that these genera probably had a more recent common ancestor
with n = 7. Ciccr, on the other hand, has both ii = 7 and n = 8. If Ciccr is
closely related to the rest of the Vicieae, it must either have diverged from
them before the appearance of the y1 = 7 ancestor, or, if it was descended from
this ancestor, the presence of 11 = 8 must be due to recent ascending aneuploidy
and be merely a parallelism imitating the situation in the Trifolieae. The former
alternative is more parsimonious and seems to me the more likely.
C/icmosy st ema tics
Anthocyanins
The important plant pigments, anthocyanins, which are largely responsible
for flower colour, are glycosidic derivatives of anthocyanidins (cf. Harborne,
1967). Variation in the composition of anthocyanin sugar residues within the
Papilionoideae may be of systematic value. A recent review showed that
whereas many members of the subfamily have glucose residues, the Vicieae
(including Cicev), which have been quite thoroughly surveyed, are characterized by anthocyanins with rhamnose residues (Harborne, 19712: 34). At
the time of this review the Trifolieae and Ononideae had been very sparsely
screened, and found to possess anthocyanidin glucosides. The published data
thus imply that the Vicieae can be separated from their neighbours by
anthocyanin chemistry. However, J . L. Ingham (Botany Ilept., University of
Reading) has informed me that malvidin-3-rhaninoside has been provisionally
identified from one member of the Trifolieae, Parochetus cornmuPiis Buch.-Ham.
ex D. Don. This suggests that the glycosidic variation-pattern, when fully
exposed, might link the Vicieae and Trifolieae rather than separating them. A
more intensive investigation in this area would be a worthwhile operation.
Is0 fluvonoids
The isoflavonoids are a group of compounds which have a very limited
distribution among flowering plants in general but which occur in many
members of the Papilionoideae (Harborne, 197 l a : 47); here, morcover, their
diversity promises t o be of considerable taxonomic significance. in the
Papilionoideae isoflavonoids exist as constitutive substances in healthy plant
tissues but they also function as phytoalexins, being produced in response to
stimulus by toxic chemicals or infecting micro-organisms (Ingham, 1972).
Cicev appears to be distinct from the rest of the Vicieae in its isoflavonoids,
but similar to the Trifolieae and Ononideae. The constitutive isoflavones
biochanin A, formononetin, pratensein and daidzein have been found in C
urietirzum; the first two, in particular, occur in large quantities in the stems,
roots and leaves (Ingham, in press). None of these has been detected in other
DELIMITATION O F THE VICIEAE-LEGUMINOSAE
153
genera of the Vicieae despite several detailed surveys (Ingham, personal
communication), but all have been found in Trijulizim (Francis et al., 1967)
and formononetin was reported from Ononis (Harborne, 1971a: 49 & 60).
C. arietinum produces the isoflavonoid phytoalexins medicarpin and
maackiain (Ingham, in press). Medicarpin has been found in small quantities in
Vicia faba and its close relatives I? galilaea Plitm. & Zohary and V. narbonensis
L. (Hargreaves et at., 1976) but in no other member of the Vicieae.
I t is, however, a characteristic phytoalexin of Trigonella, Medicago and
Melilotzts (Ingham & Harborne, 1976) and Trifolium (Higgins & Smith,
1972). Maackiain is produced by many members of the Trifolieae and was also
reported from Pisum (Stoessl, 1972; here it is called inermin). On the other
hand, two phytoalexins which have been isolated from members of the Vicieae,
the isoflavonoid pisatin from Pisum and the polyacetylenic compound wyerone
from Vicia (Harborne, 1971b: 276) are unknown in Cicer and the Trifolieae
and Ononideae.
Studies in this area of plant biochemistry are developing rapidly and yielding
welcome taxonomic information. This brief account indicates the current
feeling about Cicer's position with regard to its isoflavonoid chemistry; a
proper appreciation of the taxonomic importance of presence or absence of the
various compounds would, however, require a full understanding of their
biosynthetic relationships.
Non-pro t e in amino acids : cuna van in e
The non-protein amino acid canavanine is apparently found only in the seeds
of some members of the Papilionoideae, and its pattern of distribution within
the subfamily is of taxonomic interest (Bell, 1971). Table 7 summarizes the
data available in the area related to the present discussion. This shows that the
Trifolieae and Ononideae are characterized by the constant presence of
canavanine in their seeds. On the other hand, the Vicieae, apart from some
members of Vicia subgenus Vicilla, lack this compound (Kupicha, 1976). The
report of the situation in Cicer, which was based on only one species (C.
arietinqm), should be confirmed before a firm conclusion can be drawn, but
the present results suggest that the pattern of distribution of canavanine links
Table 7. The distribution of canavanine in the Vicieae, Ononideae and Trifolieae
Genus
Pisum
1.u thyr1rs
I,ens
viciu
Cicer
Oilonis
Medicago
Trigonellu
Melilotus
Trifolium
No. species
examined
1
49
1
I17
, 30
1
4
57
3
3
17
Canavanine
prescnt (+), absent ( -)
~
~
-
+:
-I
~
+
+
+
+
+
Authority
Przybylska & Hurich (1961)
Bell (1962)
Birdsong, Alston & Turner (1960)
Bell & Tirimanna (1965); results generally
confirmed by Tschiersch & Hanelt (1967)
Birdsong, Alston & Turner (1960)
Turner & Harbornc (1967)
Turner & Harborne (1967), Bell (1971)
Turner & Harborne (1967)
Turner & Harborne (1967)
Turner & Harhorne (1967), Bell (1971)
154
F. K. KUPICHA
Cicer with the rest of the Vicieae rather than with the other tribes. Outside
these groups, canavanine occurs in most species of the Galegeae, and
sporadically in the Podalyrieae, Genisteae, Hedysareae, Dalbergieae and
Phaseoleae.
Seed proteins
The seed proteins of the Leguminosae have been investigated by many
workers, using a variety of techniques. In a number of cases the findings are
relevant to the present discussion, but while they show that variation in
protein characters is systematic, the inadequate reporting of some results and
the conflicting nature of others prevent a firm conclusion being drawn from the
evidence. It is hoped that this brief survey will encourage further studies,
focussed on the genus Cicer, which should be compared not only with the rest
of the Vicieae but equally with members of the Ononideae and Trifolieae.
The albumin fraction of legume seed protein contains enzymes, including
formic and glutamic dehydrogenases (FDH and GDH). Thurman et al. (1967’)
used gel electrophoresis to compare FDH and GDH in seeds of the Vicieae,
Trifolieae and other tribes. The presence of the proteins in the gel after
electrophoresis was detected by enzymatic production of formazan from
tetrazolium compounds. It was found that all members of the Vicieae which
were tested gave one FDH band, while there were five GDH bands in all genera
of the tribe except Cicer, which had two. The Rp value of FDH in Cicer was
higher than those of the rest and approached the Rp values of the Trifolieae
FDH bands. The number of FDH and GDH bands in the Trifolieae was not
mentioned.
The globulin fraction (i.e. the storage protein) of legume seeds has been the
object of particular interest. Boulter et al. (1967) made a wide survey of
globulins of the Papilionoideae using gel electrophoresis. The 12 species of the
Vicieae in their investigation (including Cicer arietinum) gave a very uniform
band-pattern, and this differed from the equally uniform pattern of the
Trifolieae. Jackson et al. (1967) analysed the globulin fraction of seeds of the
Vicieae by ‘fingerprinting’ the peptides resulting from hydrolysis with trypsin.
It was found, by comparing chromatograms, that the ‘fingerprints’ of the genera
were quite similar. Those of Lathyrus and Lens differed from Vicia each by
three spots, while those of Pisum and Cicer differed from Vicia by seven and
thirteen spots, respectively. It was not stated by how many spots the genera
Lens, Lathyrus, Pisum and Cicer differed from each other, or the distribution
of each spot between the genera. I t would be interesting t o extend the range of
the survey and compare globulins from the Trifolieae and Ononideae with
those of the Vicieae.
In many tribes of the Papilionoideae, including the Vicieae, Ononideae and
Trifolieae, the globuIin fraction has been found to include two major
components with sedimentation coefficients of about 7s and 12s: these are
known, respectively, as vicilin and legumin (Danielsson, 1949; Boulter &
Derbyshire, 1971). Jackson et al. (1968) separated the vicilin and legumin of
Pisurn sativum, Vicia faba and Cicer arietinum, and compared them in terms of
their amino acid composition, ‘fingerprint’ maps and gel electrophoresis
band-patterns. The results showed that there is considerable similarity between
these three species with respect to both vicilin and legumin.
DEI.IMITATION O F THE VICIEAE-LEGUMINOSAE
155
Several workers have used the immunological properties of seed storage
proteins to study the relationships of genera within the Vicieae and between
this tribe and its neighbours. Kloz & Turkova (1963) separated the vicilin and
legumin from seeds of Pisurn sativum and, having prepared antisera to each,
used immunodiffusion and electrophoresis to test them against antigens from
the other genera of the Vicieae and from other tribes. They concluded from
these heterologous reactions that both vicilin and legumin are absent from the
Genisteae and Phaseoleae; Trijbliurn and Medicago have no legumin but a
protein of vicilin type; and all members of the Vicieae, including Cicer, have
both legumin and vicilin, although the vicilin of Cicer is not the same as that in
the other genera.
Simola (1969) prepared antisera to seed proteins of several species of
Lathyrus and used them to make a serological survey of the Vicieae and other
tribes. She found that antigens of Pisum, Lens and Viciu produced
heterologous reactions almost identical with the homologous reaction. Species
of Abrus, Phaseolus, Lotus and Oxytropis gave reactions indicating distant
relationship, and there was no reaction when antigen from Trifoliurn was used.
Both Ononis and Cicer gave strong reactions; these indicated considerable
homology with Lathyrus but a relationship more distant than that of the rest
of the Vicieae.
The recent paper of Dudman & Millerd (1975) reports an investigation
carried out with particular care, based on antisera to the vicilin and legumin
from seeds of Vicia faba. The results of immunodiffusion experiments showed
that Pisum sativum and species of Lathyrus gave reactions of identity with both
legumin and vicilin antisera; Lens culinuris gave a reaction of identity to
legumin but of only partial identity to vicilin. Cicer arietinzcm, and members of
the Trifolieae (ten species) and Ononideae (five species) all gave partial-identity
reactions to legumin but had non-identity with vicilin. As Dudman & Millerd
emphasized, differences in serological techniques can have a marked effect on
the results and their interpretation, and this may account for the discrepancies
between their findings and those of Kloz & Turkova (1963) and Simola (1969).
Few generalizations can be made from the data summarized above. I t
appears that as far as proteins are concerned one must be wary of accepting
taxonomic evidence derived from any one method of analysis, because each
technique seems to produce slightIy different results. In the present case, a11 the
experiments lead to the conclusion that Vicia, Lathyrus, Pisum and Lens are
very closely related. There is also considerable agreement that the Trifolieae
(and Ononideae, although Ononis has rarely been studied) are closer to the
Vicieae than any other tribe. The position of Cicer is equivocal: some studies
decisively link this genus with the rest of the Vicieae, while others show it to be
fairly closely related but set apart from the “core” of the tribe. In order to
achieve a balanced view of the situation we need more experimental data about
the Trifolieae. Ononideae and Cicer itself.
DISCUSSION
The delimitation of the Vicieae
Table 8 is a list of the attributes of Cicer which link this genus with the rest
of the Vicieae or with the Ononideae or Trifolieae; conversely, it also shows
F. K. KUPICHA
156
Table 8. A comparison between Cicer and the rest of the Vicieae, the Ononideae
and Trifolieae
Characters of Cicer
Vi.
Ci.
Ci.
On. Tr.
On.
On. Tr.
Ci.
On. Tr.
Vi.
Vi.
Vi.
On. Tr.
Vi,
On. Tr.
On. Tr.
Tr. Vi.
on.
Tr. Vi.
On.
On. Tr.
On. Tr.
On.
On. Tr.
On. Tr.
Vi.
Vi.
Ci.
On. Tr.
Vi.
On. Tr.
Tr. Vi.
*
*
*
0
*
0
0
0
1.
2.
3.
4.
5.
6.
7.
8.
9.
0
10.
0
11.
12.
13.
14.
15.
16.
0
0
D
*
*
*
*
U
0
0
0
*
*
*
*
*
0
0
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
germination hypogcal
radicle growing towards or away from hilum
first scale-leaf of seedling having variable position
transition region in hypocotyl
plants often spiny
no cortical vascular bundles in stem
first juvenile leaf with 2 o r more pairs of lateral leaflets
juvenile leaves with terminal leaflet
mature leaves sometimes tendrillous
mature leavcs usually multijugate
stipules free from petiole
leaflets serrate, with craspedodromous venation
uniccllular hairs smooth-walled
long-stalked glands present
wing petals free from keel
androecium diadelphous
anthers alternately basifixed and versatile
anthers of uniform size
pollen grains subspherical, with relatively thin walls and large pori
apertures of pollen grains unthickened
style tcrete, glabrous
legume inflated
seeds beaked above hilum
hilum small, subcircular
endosperm absent in mature seed
post-chalaza1 vascular bundle present in sccd
post-chalaza1 vascular bundle dichotomizing
isoflavonoid chemistry shows affinity with Ononideae and Trifolieae
canavaninc absent from seeds
base chromosome number x = 8 present
chromosome complement usually diploid, not polyploid
Vi. character-state typical of the Vicieae, On. of the Ononideae, Tr. of the Trifolieae; Ci. characterstate peculiar to Cicer, or, if corresponding character-state in Ononideae and Trifolieae is unknown,
separating Cicer from the Vicieae.
m,
Charactcr-state specialized, within the context of these four tribes;
0,
character-state primitive;
*, character-state cannot be judged specialized or primitive.
where there is discontinuity of character-variation between Cicer and its
neighbours. The precise number of character-states which Cicer shares with
each of the other groups is not significant, because several of the characters
need confirmation, some do not hold true for every species, and some could be
subdivided into more characters. However, the table is a convenient summary
of the phenetic situation, as far as it is known to me. From the table, the
following conclusions can be drawn. Firstly, the characters which link Cicer
with the rest of the Vicieae are considerably outnumbered by those which
separate these groups and instead show affinity between Cicer and the
Trifolieae and/or Ononideae. Secondly, if all characters are given equal
weighting, the present evidence indicates that the affinity between Cicer and
the Ononideae is of the same order as that between Cicer and the Trifolieae.
The claim of De Candolle (1825a), Popov (1828-29) and many others that
Cicer has a special relationship with Ononis therefore cannot be upheld.
DELIMITATION 0 I; THE VICIEAE-LEGUMINOSAE
157
The first of these statements confirms that Cicer is anomalous within the
Vicieae. If it is removed, the range of variation within the tribe is significantly
reduced, and its delimitation from other taxa of the same rank becomes much
clearer. The effects of this alteration obviously result from the achievement of
a ‘natural’ group which is held together by the total of its attributes, in
contrast with the traditionally-defined Vicieae which were recognized merely
by their possession of tendrils and hypogeal germination. I propose, therefore,
that Cicer should be excluded from the Vicieae, which should now comprise
Vicia, Luthyrzis, Lcns, Anutropostylia, Pisirm and Vavilovia.
Description of the tribe Vicieae sensu stricto
Perennial and annual herbs with erect or more usually climbing or sprawling
habit; plants rarely tuberous. Indumentum of simple, smooth-walled hairs and
short-stalked glandular hairs. Stems with cortical vascular bundles in the
internodes, often winged; primary shoot almost always of limited growth,
plants proliferating from basal nodes. Leaves epulvinate, alternate, distichous,
hypostomatic, amphistomatic or epistomatic (stomata anomocytic), paripinnate with the rachis ending in a tendril or mucro, or very rarely imparipinnate;
leaflets many-paired to unijugate; very rarely (in Lathyrus) leaves phyllodic or
reduced to a tendril and stipules; stipules semisagittate or hastate or variously
divided, sometimes with a nectariferous spot, never adnate to the petiole.
Vernation of leaflets conduplicate or supervolute. Venation brochidodromous,
veins pinnate or parallel. Inflorescence rarely a panicle, usually a secund,
axillary raceme or sometimes 1-flowered; bracteoles almost always absent.
Vexillum oblong, platonychioid or stenonychioid, occasionally pouched. Alae
united with carina. Stamina1 tube diadelphous but with vexillary stamen
lightly adhering to its neighbours, truncate or oblique at apex; anthers introrse,
versatile, of equal size, rarely alternate filaments dilated at the apex. Style
borne at right angles to ovary, usually compressed dorsally or laterally, always
pubescent (distribution of pubescence various), sometimes spathulate, sometimes contorted; stigma terminal, very rarely double. Legume more or less
linear, laterally compressed, 2-many-seeded, usually dehiscent, occasionally
winged, sometimes with woolly or (very rarely) membranous partitions
between the seeds. Seeds compressed-spherical, with long to short hilum; testa
smooth or variously rough-textured; lens near hilum or rarely opposite;
vascular bundle continuing past chalaza but not branched; endosperm absent.
Germination hypogeal; radicle and hypocotyl triarch (very rarely tetrarch);
transition region between root and stem in epicotyl; first scale-leaf borne on
side of plumule away from cotyledons.
The taxonomic position of Cicer
Having taken Cicer out of the Vicieae, one must find a better place for this
genus within the Papilionoideae. Cicer s systematic position should be
influenced not only by the number of features which it has in common with
various alternative groups, but also by the present delimitation and variability
of those taxa and the effect which its inclusion within one of them would have
on the hierarchy.
158
F. K. KUPICHA
The Trifolieae form a very well-defined natural tribe comparable with the
Vicieae sensu stricto, and the monogeneric Ononideae are similarly limited in
their internal variability. In these circumstances, neither tribe could absorb
Cicer without profoundly altering its definition. Moreover, the differential
characters which distinguish between the Trifolieae and Ononideae (Table 2)
are of less weight than those separating each of these tribes from Cicer, so that
if the creation of the Ononideae is valid Cicer must also be excluded from both
of them. Alternatively, if Ononis is regarded as a member of the Trifolieae (as
has been done by most recent authorities), the latter becomes more
polymorphic and could be further enlarged to encompass Cicer. Although it
would be preferable to have Cicer in the Trifolieae sensu lato than in the
Vicieae, it seems unwise to blur the definition of the Trifolieae to this extent.
The most satisfactory course is to place Cicer in a tribe of its own. A suitable
name in this category already exists because Alefeld (1859), with his peculiar
concept of taxonomic ranking, made the Vicieae sensu lato a subfamily
containing the tribes Ciceridae, Viciidae and Orobidae. I propose that the
Ciceridae should be brought out of obscurity to form a new monogeneric
tribe, the Cicereae Alef.
Phylogenetic relationships of Cicer
This discussion has so far been based on the phenetic method of
classification, which gives all characters equal weight. I t is interesting to make
an alternative interpretation of the same data, using the phylogenetic
systematic method (Hennig, 1966), and to find that while the results are similar
in practical terms, the evolutionary dimension becomes much clearer.
The surest evidence that a group is monophyletic is the presence in all
members of that group, and complete absence outside the group, of one or
more uniquely derived characters. Each of the character-states of Cicer listed in
Table 8 has been judged specialized, primitive or indeterminate, in the context
of this part of the Papilionoideae (see symbols in second column). Two features
of Cicer, both of which are shared with the Trifolieae and Ononideae, can
confidently be assumed to be uniquely derived: the serrated leaflets with
craspedodromous venation (character 12 in Table 8) and the long-stalked
glandular hairs (ch. 14). The corresponding character-states in the Vicieae are
relatively primitive. This evidence immediately indicates that Cicer is
cladistically more closely related to the Trifolieae and Ononideae than t o the
Vicieae (Fig. 7).
It is theoretically impossible for Cicer to share different uniquely derived
characters with the two mutually exclusive groups Trifolieae-Ononideae and
Vicieae. This consideration throws doubt on the status of the two main
characters, hypogeal germination (ch. 1) and the presence of tendrils (ch. 9),
which link Cicer with the Vicieae. Hypogeal germination has already been
shown to be widely distributed in the Papilionoideae and possibly reversible
with epigeal germination, and is therefore of doubtful significance. Tendrils, on
the other hand, are very rare and certainly specialized. Nevertheless, I am
forced to conclude that they must have evolved separately in Cicer and the
Vicieae sensu stricto. This conclusion is supported by the presence in both
Cicer and Vicia of species which have the primitive, imparipinnate leaf-form
DELIMITATION OF THE VICIEAE-LEGUMLNOSAE
159
W
a
Figure 7. Diagram of cladistic relationships. ch, Uniquely derived character, numbered as in
Table 8.
throughout their life history, as well as by the different patterns of leaf
ontogeny in the two groups.
The Ononideae and Trifolieae together possess one unique specialized
character (ch. 11, the stipules adnate to the petiole) which suggests that they
had a common ancestor subsequent to the isolation of the line leading to Cicer.
This is shown in Fig. 7 at A. (Character 1 1 is expressed here in its derived state;
Table 8 gives the corresponding primitive state for Cicer.) I do not have enough
evidence to decide on cladistic relationships within the Trifolieae-Ononideae;
this subject needs a full independent investigation. I t is apparent, however, that
the Genisteae, which have often been proposed as close relatives of Ononis, are
cladistically further from Ononis than both the Trifolieae and Cicereae, because
they do not show the derived characters which are markers for these taxa.
I t must be admitted that up till now I have assumed that the Cicereae,
Ononideae, Trifolieae and Vicieae comprise a monophyletic group, but this
may be wrong; I know of no uniquely derived character which delimits this
group from the rest of the Papilionoideae. The only evidence which links the
Vicieae with these other tribes is phytochemical, especially serological. A
wider, very detailed assessment of character-variation within the Papilionoideae
is required to determine the closest relatives of the Vicieae. Figure 7 expresses
the present uncertain situation by the alternative branching at B and C. I
suggest that in beginning a wider survey, one should look first at tribes which
have the base chromosome number x = 8, viz. Galegeae p.p., Genisteae,
Hedysareae p.p. and Loteae.
ACKNOW I.8DGBML.NTS
This paper presents part of the work carried out for the degree of Ph.D. in
the University of Edinburgh. I thank the Science Research Council and the
Senatus Academicus of Edinburgh University for their generous financial
F. K. KUPICHA
160
support, and Profcssor R. Brown and Mr D. M. Henderson, the Kegius Keeper
of the Edinburgh Royal Botanic Garden, for their permission to work in the
University Botany Department and at the Botanic Garden, respectively. I also
thank Dr Ir L. J , G. van der Maesen for information about Cicer seedlings, Mr
4. L. Ingham for helpful discussions about the chemosystematic part of the
paper, and Dr C. J . Humphries for encouraging me to branch o u t into
phylogenetics. I am most grateful to my two supervisors, Dr P. H. Davis and Ilr
P. M. Smith, for their guidance, kindness and stimulating interest.
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