Content uploaded by D. D. Sokoloff
Author content
All content in this area was uploaded by D. D. Sokoloff on Sep 23, 2017
Content may be subject to copyright.
97
ISSN 0096-3925, Moscow University Biological Sciences Bulletin, 2017, Vol. 72, No. 3, pp. 97–108. © Allerton Press, Inc., 2017.
Original Russian Text © D.D. Sokoloff, M.S. Nuraliev, A.A. Oskolski, M.V. Remizowa, 2017, published in Vestnik Moskovskogo Universiteta, Seriya 16: Biologiya, 2017, Vol. 72,
No. 3, pp. 115–127.
Gynoecium Evolution in Angiosperms: Monomery,
Pseudomonomery, and Mixomery
D. D. Sokoloffa, *, M. S. Nuralieva, A. A. Oskolskib, c, and M. V. Remizowaa
a Department of Biology, Moscow State University, Moscow, 119234 Russia
b Department of Botany and Plant Biotechnology, University of Johannesburg, Johannesburg, South Africa
c Botanical Museum, Komarov Institute of Botany, Russian Academy of Sciences, St. Petersburg, 197376 Russia
* e-mail: sokoloff-v@yandex.ru
Received June 1, 2017; in final form, June 15, 2017
Abstract—The presence of a gynoecium composed of carpels is a key feature of angiosperms. The carpel is
often regarded as a homologue of the gymnosperm megasporophyll (that is, an ovule-bearing leaf), but higher
complexity of the morphological nature of carpel cannot be ruled out. Angiosperm carpels can fuse to form
a syncarpous gynoecium. A syncarpous gynoecium usually includes a well-developed compitum, an area
where the pollen tube transmitting tracts of individual carpels unite to enable the transition of pollen tubes
from one carpel to another. This phenomenon is a precondition to the emergence of carpel dimorphism man-
ifested as the absence of a functional stigma or fertile ovules in part of the carpels. Pseudomonomery, which
is characterized by the presence of a fertile ovule (or ovules) in one carpel only, is a specific case of carpel
dimorphism. A pseudomonomerous gynoecium usually has a single plane of symmetry and is likely to share
certain features of the regulation of morphogenesis with the monosymmetric perianth and androecium. A
genuine monomerous gynoecium consists of a single carpel. Syncarpous gynoecia can be abruptly trans-
formed into monomerous gynoecia in the course of evolution or undergo sterilization and gradual reduction
of some carpels. Partial or nearly complete loss of carpel individuality that precludes the assignment of an
ovule (or ovules) to an individual carpel is observed in a specific group of gynoecia. We termed this phenom-
enon mixomery, since it should be distinguished from pseudomonomery.
Keywords: gynoecium, monomery, carpel, pseudomonomery, syncarpy, flower, evolution, review.
DOI: 10.3103/S0096392517030105
The presence of carpels that form a gynoecium is a
key feature of angiosperms. Ovules that give rise to
seeds are located inside these structures, and, there-
fore, the term “angiosperm” implies the presence of
carpels. Recognition of the carpel as a distinct struc-
ture is among the most fortunate generalizations in
comparative morphology of plants that facilitates
practical work as well. It is rather difficult to formulate
a definition of the term “carpel,” just as in the case of
many other basic scientific terms, and the origin and
homologies of the carpel remain among the major
puzzling questions of evolutionary botany [1–4]. A
solution to the problem of morphological origin of the
carpel would make a substantial contribution to the
elucidation of the origin and relationships of angio-
sperms.
The gynoecium is an entity formed by all carpels of
a flower. A carpel is usually defined as a structural unit
of the gynoecium [5]. This “cyclic” definition does
not shed light on the morphological nature of the car-
pel and the gynoecium, although it is convenient for
practical use. The use of this definition is obviously
restricted to the cases when the flower under investiga-
tion has distinct borders (although difficulties related
to the identification of the borders of a flower arise rel-
atively seldom [6–9]). The definition also makes sense
only if flowers of all angiosperms are regarded as
homologous structures.
The carpels can be free or fused, and the number of
carpels in gynoecia varies considerably. Flowers with
several free carpels probably represent the ancestral
(plesiomorphic) state of the flower in angiosperms
[10]. Indeed, all representatives of the basal grade of
angiosperms, with the exception of Nymphaeaceae,
have free carpels [10, 11]. The presence of several free
carpels in the gynoecium is characteristic of Amborel-
laceae, a putative sister group to other angiosperms
[10, 11].
Usually, the gynoecium formed by several fused
carpels can be easily distinguished from that formed by
a single carpel, although some exceptions have been
reported [12–17]. The present review is aimed in the
analysis of problematic situations when the task of car-
pel counting is not trivial. A brief description of the
current concepts of the origin of carpel is necessary for
a discussion of these problems.
BOTANY
98
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
SOKOLOFF et al.
CONCEPT OF A CONDUPLICATE CARPEL
AND THE PROBLEM OF THE ORIGIN
OF GYNOECIUM
The conduplicate carpel concept was widely recog-
nized in the second half of the 20th century [18–20].
It regards the carpel as an originally leaf-like organ
(phyllome) that gives rise to ovules. The ovules are
formed on the morphologically upper (adaxial) sur-
face of the carpel, usually near its edges. The carpel is
folded upwards along the middle vein. The leaves of
many plants are folded in a similar way within the
buds, but the folding of the conduplicate carpel is pre-
served in the definitive state as well. Moreover, right
and left edges of the carpel become fused. Fusion of
the edges leads to internalization of the adaxial surface
and the ovules located thereon and, thus, results in the
formation of the ovary cavity. On the one hand, fusion
of the edges is regarded as an evolutionary trend, and,
on the other hand, it can be observed during the mor-
phogenesis of the conduplicate carpel. Fusion that
involves the contact between organ surfaces and can
occur during morphogenesis proper is termed post-
genital [21]. The capacity for postgenital fusions is
believed to have developed during the evolution of
higher plants due to the emergence of carpels in angio-
sperms [22]. The formation of a completely closed
ovary cannot occur in the absence of postgenital
fusion of the edges [17] if the primary morphological
surface remains continuous [23] and the ovule primor-
dia are formed exogenously. The fusion of carpel edges
always occurs on the ventral side (that is, on the side
facing the center of the flower in the case of a gynoe-
cium with several carpels), and, therefore, the fusion
line was termed the ventral slit.
The concept of the conduplicate carpel implies that
a fertile leaf (megasporophyll [18, 19]) with ovules
developing on the upper side was the evolutionary pre-
cursor of the carpel (each ovule incorporated a
megasporangium, i.e. nucellus). Evolutionary fixation
of the early morphogenetic stage of this sporophyll
characterized by longitudinal folding similar to that
observed in the bud [19] and the emergence of post-
genital fusion of the edges allow to imagine the origin
of carpel. Researchers in the field of developmental
genetics supported the hypothesis of the phyllomic
nature of all elements of a flower [24–27].
The absence of extant or extinct gymnosperm that
would carry ovules on the morphologically upper part
of the flat phyllomes is a weakness of the concept of
the carpel as a megasporophyll. Ovules are indeed
located on the upper part of the ovuliferous scales of
conifers, but these structures are definitely not phyl-
lomes, since they emerged due to a transformation of
entire lateral axes and organs located thereon (the so-
called axillary complex). The surface of the structures
(termed cupules or capsules) that incorporated the
sufficiently internalized ovules in fossil gymnosperms
of the orders Caytoniales and Glossopteridales (Arbe-
riales) is considered the adaxial surface [1, 2]. The
interpretation of the origin of these structures (that
contained several orthotropic unitegmic ovules)
implies a fundamental evolutionary transformation of
megasporophylls or their parts. These structures
(cupules) are currently regarded as putative homo-
logues of the outer integument of the ovule in angio-
sperms, since this point of view provides an explana-
tion for the origin of both the double integument and
the ovule of the anatropous type [2, 3]. The structures
that incorporated the ovules in Caytoniales and Glos-
sopteridales cannot be considered as carpel homo-
logues in this case. Thus, the data collected by paleo-
botanists do not provide a convincing proof for the
theory of the carpel as a megasporophyll.
HYPOTHESES THAT CHARACTERIZE
THE CARPEL AS A PHYLLOME BUT
NOT A MEGASPOROPHYLL
S.V. Meyen [28] and the authors of the Mostly
Male Theory of flower origin [29, 30] believe that the
carpel is probably homologous to the microsporophyll
of the ancestors of flowering plants. The emergence of
ovules on the carpel, as well as the disappearance of
microsporangia, are assumed to have occurred upon
the dramatic homeotic transformations that played an
important role in the origin of the carpel. The expla-
nations of the origin of bitegmic ovules of angiosperms
used by Meyen and the authors of the Mostly Male
Theory [4, 30] do not appear sufficiently convincing
and, therefore, represent a weakness of their views.
The putative ancestors of flowering plants selected
within the abovementioned concepts (Bennettitales
and Corystospermaceae) do not allow for a simple
representation of a putative mechanism for the emer-
gence of the outer integument from the wall of the
structure that incorporated the unitegmic ovules, in
contrast to Caytoniales and Glossopteridales. How-
ever, researchers in the field of developmental genetics
showed that overexpression of WUSCHEL in Arabi-
dopsis led to the formation of additional integuments,
and, therefore, a similar mechanism was assumed to
underlie the emergence of bitegmic ovules of angio-
sperms [31, 32].
Some authors draw parallels between the wall of
the angiosperm carpel and the leaves of Glossopterid-
ales that carried the ovule-bearing structures (always
on the upper side). One of the viewpoints implies con-
genital fusion of the axillary shoot that bore the folded
megasporophylls to the respective subtending leaf in
Glossopteridales. In this case, the subtending leaf may
be a homologue of the carpel wall (again, a phyllome,
but not a megasporophyll) provided that the megaspo-
rophylls themselves are the homologues of the outer
integument of flowering plants [1, 2]. The weaknesses
of this opinion are the following: (1) a large time gap
between Glossopteridales (until the transition from
Permian to Triassic) and the most ancient of the reli-
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
GYNOECIUM EVOLUTION IN ANGIOSPERMS 99
ably identified angiosperms (Cretaceous) [2]; (2) the
absence of any structural or developmental proof of
the different origin of the placenta and ovary wall in
the representatives of the basal grade of f lowering
plants [11] (with the possible exception of Illicium,
since some authors assume that the single ovule of this
plant is formed on the axis of the f lower in the axil of
the carpel [33]). Caytoniales, which have many com-
mon features with Glossopteridales, coexisted with
the first angiosperms, in contrast to Glossopteridales,
but the character of the arrangement of capsule-bear-
ing axes on the plant has not been established for Cay-
toniales because of poor preservation of the material.
According to one of the existing hypotheses, the
arrangement of capsule-bearing axes in Caytoniales
was similar to that in Glossopteridales [1, 2], but there
is no direct proof for this idea.
Certain data of developmental genetics support the
idea of a carpel as a phyllome but not a megasporo-
phyll. The regulation of ovule morphogenesis shares
many features with the regulation of shoot morpho-
genesis, and there are many similarities between the
initiation and development of integuments and leaves
[31 , 32 ]. T his is i ndicative of cons iderabl e au tonomy of
ovule morphogenesis relative to carpel morphogene-
sis. The AGAMOUS (AG) gene is the key regulator of
the development of carpels (in Arabidopsis) [32, 34].
Plants with mutations in this gene lack normal carpels.
However, the flowers of Arabidopsis plants that lack an
active AG gene can sometimes give rise to ovules that
are ectopically located on sepals. Therefore, the regu-
lation of ovule development is apparently partially
independent of the regulation of carpel wall develop-
ment as a whole. Normal development of the carpel in
Arabidopsis requires the contributions of four genes
from the same family: the abovementioned AG gene
functions in concert with SEEDSTICK (STK) and
SHATTERPROOF (SHP1 and SHP2) [32, 34]. AG
determines the location of the carpels in the center of
a flower and defines the sites of expression of STK and
SHP that are “responsible” for ovule development.
Characteristically, the stk shp1 shp2 mutants develop
the gynoecium proper but lack normally formed
ovules [34].
The facts listed in the previous paragraph cannot be
regarded as the components of fundamental argumen-
tation for the carpel being a phyllome but not a
megasporophyll, since a similarly autonomous char-
acter of ovule morphogenesis must be observed in the
true megasporophylls of gymnosperms. The data on
the similarity of genetic regulation of the morphogen-
esis of the entire ovule-bearing placenta to that of the
axillary meristem in Arabidopsis [32 ] is of m uch greater
interest. However, the distinction between the pro-
cesses of placenta and ovule morphogenesis in carpels
with a single ovule that predominate in representatives
of the basal grade of angiosperms is not completely
clear.
ASCIDIATE CARPEL AND THE STRUCTURE
OF THE SYNCARPOUS GYNOECIUM
The conduplicate carpel concept does not provide
a comprehensive description of the diversity of angio-
sperm carpels. The ventral slit does not reach the car-
pel base in many plants. The distal area with the ven-
tral slit is termed the plicate zone in these cases,
whereas the proximal area that remains sac-like
throughout the development is termed the ascidiate
zone [33, 35, 36]. The relative lengths of the two zones
in carpels of different angiosperms vary greatly. Ovules
can be restricted to one of the zones or located in both
zones. If there is only a single ovule per carpel, the
ovule is often (although not always) attached to the
ventral side in the so-called cross-zone at the border of
the ascidiate zone and the plicate zone [35, 36]. The
ascidiate carpels of certain angiosperms are com-
pletely devoid of a plicate zone. Particularly, this type
of structure is characteristic for most members of the
basal grade of f lowering plants [11], and, therefore, it
is identified as the ancestral (plesiomorphic) type
upon the reconstruction of the evolution of carpel
types according to the maximum parsimony proce-
dure [10]. The ascidiate carpel concept allows for con-
venient description of the diversity of angiosperm
gynoecia, but it does not provide a solution for the
problem of the origin and homologies of the carpel
formulated above. Indeed, the ovules are located on a
morphologically adaxial surface both in the ascidiate
carpel and in the conduplicate carpel.
The fusion between carpels in gynoecia, when
present, is usually congenital, that is, the fused parts of
carpels form a single entity from the earliest stages of
development onwards. We will use the terminology of
researchers who call a gynoecium syncarpous in the
case of congenital fusion between carpels and use the
term “apocarpous” for gynoecia that do not exhibit
congenital fusion of carpels [35, 36]. Comprehensive
comparison of gynoecia of a broad range of flowering
plants is the preferred way to confirm the presence of
several carpels in a syncarpous gynoecium. A syna-
scidiate zone and a symplicate zone are identified
within a syncarpous gynoecium composed of ascidiate
carpels [35, 36]. The former zone is formed by con-
genitally fused ascidiate zones of the carpels, and,
therefore, a cross-section of this zone is multilocular
from the moment of zone formation, with each locule
corresponding to the cavity of an individual carpel.
The symplicate zone is formed by congenitally fused
plicate zones of the carpels and is unilocular at the
moment of formation. The cavity of the symplicate
zone is directly connected to the locules of the syna-
scidiate zone. As mentioned above for the free individ-
ual carpel, the ventral edges of each carpel (or actually,
the walls formed by congenitally fused edges of each
pair of neighboring carpels) can undergo postgenital
fusion accompanied by the formation of ventral slits in
the symplicate zone. The symplicate zone becomes
100
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
SOKOLOFF et al.
multilocular if the fusion occurs. The formation of the
ventral slit is not a decisive factor in ovule internaliza-
tion in this case, and, therefore, the formation of ven-
tral slits in the symplicate zone occurs only in some
plant species, whereas this zone remains unilocular in
many other plants. An asymplicate zone (an analogue
of the apocarpous gynoecium) characterized by the
absence of congenital fusion of the plicate parts of
individual carpels can be located above the symplicate
zone [36].
The presence of an originally unilocular area (sym-
plicate zone) in the gynoecium is of great importance
for the organization of the growth of pollen tubes. The
pollen tubes of most f lowering plants grow along the
so-called transmitting tissue that is usually derived
from the cells of the internal surface of the carpel or
from the cell layers located close to the internal surface
[5]. The pollen tubes of some other plants grow in the
carpel cavity, either along the internal carpel surface or
inside the mucilage that fills the carpel cavity [5]. The
presence of a symplicate zone allows to form of a spe-
cial area (compitum) in all these cases. The growth
paths of different pollen tubes meet in the compitum,
so that the tubes that extend from pollen grains germi-
nated at different stigmas can undergo redistribution
between the carpels and compete with each other.
These processes are of great biological importance [5,
35, 37, 38]. Complete occlusion of the carpel cavity in
the symplicate zone can occur upon the formation of
pollen tube transmitting tissue, so that the cavity
becomes undetectable on cross-sections. Compitum
formation is not unique for typical syncarpous gynoe-
cia, since it can also be observed in apocarpous gynoe-
cia with postgenital carpel fusion [37, 39–41]. Simul-
taneous internalization of ovules by several carpels is
the common feature of these structural variants.
CARPEL DIMORPHISM
IN THE SYNCARPOUS GYNOECIUM
AND PSEUDOMONOMERY
The presence of a compitum accounts for the pos-
sibility of the emergence of structural and functional
dimorphism of carpels in the syncarpous gynoecium1.
A possible and very common situation (1) considered
in the following paragraph implies that one carpel (or
some of the carpels) is only involved in pollen capture
and the organization of initial stages of pollen tube
growth but does not bear fertile ovules, whereas the
1The term “carpel polymorphism” has been compromised to a
certain extent, since the studies published by E.R. Saunders (for
example, [42]) declared the presence of sterile and fertile carpels
in an unreasonably large set of flowering plants that almost
encompassed the majority of angiosperm groups. The state-
ments made by Saunders are largely due to an insufficiently crit-
ical interpretation of data on f lower vasculature [43]. However,
these statements are still of considerable interest in view of the
ideas concerning the putative dual nature of angiosperm carpels
as homologues of the reproductive structures of Glossopteri-
dales.
other carpel (or carpels) has both a functional stigma
and a fully developed ovary. Redistribution in the
compitum area enables the fertilization of ovules (or
ovule) of a fertile carpel (or carpels) by pollen tubes
from the stigma of a sterile carpel, whereas the pres-
ence of several stigmas allows for more reliable pollen
capture. However, an increase of the structural com-
plexity of the stigma of a single carpel, such as the divi-
sion into three (sometimes further branching)
branches observed in Amphibolis (Cymodoceaceae:
Alismatales), can have the same effect [44, 45].
Another kind of carpel dimorphism (2) implies that
only a single carpel (or some of the carpels) has a func-
tional stigma, whereas fertile ovules are found in all
carpels. This variant is known in Polygalaceae [46].
Finally, the situation (3) can be termed “the full divi-
sion of labor” between the carpels if one of them (or
some of the carpels) bears a functional stigma but does
not bear fertile ovules, whereas the other carpel (or
carpels) does not bear a fully developed stigma but
bears fertile ovules/ovule. Lagoecia cuminoides
(Umbelliferae: Apiales [47]) can be mentioned as an
example of this structural variant. Theoretically, one
can imagine a gynoecium (4) that includes three types
of carpels: with ovules and a stigma, with ovules and
no stigma, and with stigma and no ovules, but no
examples of such plants are known to the authors. The
functional value of carpel dimorphism in certain
gynoecia is unclear. For instance, the sterile carpels of
Triglochin (Juncaginaceae: Alismatales) do not cap-
ture pollen and the gynoecia of these plants are devoid
of a symplicate zone with a compitum [44, 48].
The number of sterile and fertile carpels may vary.
For instance, Emmotum (Icacinaceae) has three fertile
carpels and two sterile carpels [49]. The pseudomono-
merous gynoecium [5, 17, 33, 36] is a particular case
(although the most frequent case) of a gynoecium with
dimorphic carpels. All syncarpous gynoecia with a sin-
gle carpel that carries a fertile ovary can be assigned to
this type. A pseudomonomerous gynoecium can also
emerge upon postgenital fusion between carpels (as
observed in certain palm species) [40, 50]. Consider-
able reduction of the sterile carpels (or carpel), includ-
ing the loss of the capacity for pollen capture, can
occur in some pseudomonomerous gynoecia [36, 51].
It is very difficult to prove the presence of strongly
reduced sterile carpels in a syncarpous gynoecium,
since the structure in question is small, probably
devoid of specific distinctive features, and congeni-
tally fused to a fertile carpel. Morphological series with
an increasing degree of reduction of sterile carpels
provide the most convincing proof of the pseudomo-
nomerous nature of these gynoecia [51]. The con-
struction of these morphological series is not always
possible, especially if one tries to eliminate all contra-
dictions with the data of molecular phylogenetics that
define the relationships between the taxa used for the
construction of the series. We believe that the absence
of clear morphological series and traces of sterile car-
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
GYNOECIUM EVOLUTION IN ANGIOSPERMS 101
pels unambiguously reflected in structural and mor-
phogenetic data provides sufficient grounds for the
classification of the gynoecium in question as mono-
merous, because this hypothesis is more parsimoni-
ous. Let us demonstrate this using an example of a
group of families of the order Poales recently re-clas-
sified as Restionaceae s.l. [52]. Plants with obviously
polymorphic carpels were detected among Restiona-
ceae sensu stricto: for example, Leptocarpus has three
functional stigmas and an ovary with a single pendent
ovule. The location of this ovule relative to one of the
stigmas is analogous to the location of an ovule relative
to the stigma in each of the ovarian locules of Restion-
aceae species with three fertile carpels [13, 53]. This
structure of the gynoecium can be regarded as pseudo-
monomerous. The family Anarthriaceae closely
related to Restionaceae s.str. includes three genera.
The relationships between these genera can be
described as Anarthria (Lyginia + Hopkinsia) [54]. A
typical trimerous gynoecium composed of similar car-
pels is characteristic of the first two genera [53, 55],
whereas a single fully developed carpel is found in
Hopkinsia [56]. The occurrence of pseudomonomery
in Leptocarpus does not provide any arguments against
the interpretation of the Hopkinsia gynoecium as
monomerous, since these are neither sister nor closely
related genera within Restionaceae s.l. Different kinds
of gynoecium reduction observed in other Restiona-
ceae [57] cannot be used for the elucidation of the
nature of Hopkinsia gynoecium due to similar reasons.
MONOMEROUS GYNOECIUM
A monomerous gynoecium consists of a single car-
pel. According to the traditional concepts, the mono-
merous gynoecium is derived from the apocarpous
gynoecium as a result of the gradual reduction of the
number of carpels, in contrast to the pseudomono-
merous gynoecium [19]. These concepts were devel-
oped within the framework of the idea of largely irre-
versible transition from apocarpy to syncarpy during
the evolution of angiosperms. However, analysis of the
evolution of the “presence of congenital carpel fusion”
trait based on molecular phylogenetic trees of flower-
ing plants pointed at the secondary nature of apocarpy
in a large number of groups, including all apocarpous
monocotyledons and all apocarpous core eudicots
(Pentapetalae) [58]. We believe that the origin of a
gynoecium from a polymerous-apocarpous or a
polymerous-syncarpous type should not be taken into
account during making a decision on its monomerous
nature. Individual carpels of the syncarpous gynoe-
cium are very often (although not always) initiated as
individual primordia, with the congenitally fused areas
emerging at the later stages of morphogenesis. The
individuality of carpel primordia suggests that the syn-
carpous condition can not constrain the variation of
the number of primordia, including a decrease of this
number to one.
A number of convincing examples of truly mono-
merous gynoecia that evolved upon a dramatic
decrease of the merism of a syncarpous gynoecium in
the absence of a gradual series of transition forms
(with one fertile carpel and one or several sterile car-
pels) have been accumulated by now. For example, the
syncarpous condition undoubtedly was the ancestral
state for the order Caryophyllales, whereas the merism
of the gynoecium in this group varied considerably.
The monomerous gynoecium of Trichostigma (Phyto-
laccaceae) has an unsealed opening at the base; this
opening connects the outer surface of the gynoecium
to the ovarian cavity [59]. The opening is similar to the
area of the symplicate zone that contains individually
open carpels of the syncarpous gynoecia in a number
of Caryophyllales species. The preservation of such an
opening within the pseudonomomery pathway of
gynoecium reduction in this group could have been
possible upon a break of the contour of the ovary wall
(as seen in a cross-section) only, that is, secondary
separation of congenitally fused carpel parts would be
required. This explanation appears less parsimonious
than the hypothesis on the reduction of entire carpels,
i.e., on the monomery of the gynoecium in
Trichostigma.
Syncarpy and a trimery of the gynoecium were the
ancestral states for the group of families of the order
Poales that included Cyperaceae, Poaceae, Restiona-
ceae, and Centrolepidaceae. The loss of stability of
gynoecium merism occurred in the family Centrolep-
idaceae (currently regarded as a part of Restionaceae
s.l. by some authors). Both monomerous and highly
polymerous gynoecia (with up to 45 carpels) are found
in the plants of this group [9].
The presence of peculiar features that appeared
impossible for a gynoecium formed by a single carpel
was often used as an argument in favor of a pseudomo-
nomerous interpretation of gynoecia in representatives
of certain taxa. For instance, W.R. Phillipson [60]
considered the unilocular gynoecium of Polyscias
(Arthrophyllum) diversifolia (Araliaceae: Apiales) with
a single fertile ovule as pseudomonomerous. This
interpretation was argued by the presence of lobes of
stigma (regarded as the apices of individual carpels by
Phillipson) and the number of vascular bundles in the
distal part of the gynoecium being higher than could
be expected in one carpel. Phillipson stated that some
of these bundles were rudiments of the vasculature of
the sterile carpels. Our data show that gynoecium
development of this species proceeds through a horse-
shoe-shaped stage typical to carpel development of
many angiosperms, whereas the apical lobes emerge
very late. Moreover, the number and shapes of the
lobes vary from flower to flower, and, therefore, the
lobes could not be the traces of multiple carpels [61].
The numerous small bundles are detected in the top
part of the ovary of related species with several fertile
carpels. The number of the bundles is several times
higher than the number of the carpels. Therefore, the
102
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
SOKOLOFF et al.
similar numerous bundles found in the ovary roof of
P. diversifolia can actually belong to a single carpel. All
data taken in combination point at the monomerous
character of the gynoecium in P. diversifolia [61].
SYMMETRY AND ORIENTATION
OF MONOMEROUS
AND PSEUDOMONOMEROUS GYNOECIA
As the angiosperm carpels (at least the carpels that
have a plicate zone) are monosymmetric, both mono-
merous and pseudomonomerous gynoecia have a sin-
gle plane of symmetry. Therefore, one could expect
that the generalizations formulated for the monosym-
metric flowers would be applicable to flowers with
pseudomonomerous and monomerous gynoecia. The
groundplan (i.e., the number and relative location of
the organs) is in most cases very stable in monosym-
metric flowers [62]; this is partially (but probably not
fully) related to the role of the genes of the
CYCLOIDEA family in the regulation of the number of
organs in a f lower (in addition to the regulation of
flower symmetry by these genes) [63]. The orientation
of the plane of symmetry is usually stable within a
taxon. The plane of symmetry is median in most cases
[64], since the bract and the axis of the inf lorescence
create a morphological gradient that influences the
development of a flower [65].
Indeed, most of the convincing examples of gynoe-
cium pseudomonomery are derived from the groups
with a stable flower groundplan usually characterized
by the presence of a median plane of symmetry. For
instance, the large family Umbelliferae (Apiaceae) is
characterized by a very stable flower groundplan. The
flower of these plants is pentamerous, with the excep-
tion of dimerous gynoecium, and the rare deviations
from this structure can be regarded as teratological
cases [64, 66]. However, pseudomonomery evolved
several times in this family, with the stable adaxial
position of the sterile carpel in some species (Lagoe-
cia) and a stable abaxial position in the others (Arcto-
pus) [47]. Legumes constitute the largest group of
angiosperms with predominantly monomerous
gynoecia. The flowers of these plants are often mono-
symmetric, the number of organs in a flower is stable,
and the carpel is located in the plane of symmetry of
the flower [64, 66, 67].
However, contrasting examples that illustrate
unstable orientation of monosymmetric gynoecia are
known as well. These cases are sometimes related to
general instability of flower groundplan in a group.
For instance, flower groundplan in Araliaceae (a fam-
ily related to Umbelliferae) is labile both at the level of
the family as a whole and at the level of individual spe-
cies in some cases [68]. Monomery of the gynoecium
evolved independently in several Araliaceae species
(all in the genus Polyscias), and the character of carpel
orientation relative to the median plane of the flower
was always unstable within a species and sometimes
even within an inflorescence [61]. Importantly, the
variation of gynoecium orientation in Polyscias is not
limited to the cases of monomery [69]. The orienta-
tion of the dimerous gynoecium in this group can vary
as well, whereas the two carpels of Umbelliferae are
always located in the median plane [69].
Instability of carpel orientation was also reported
for the pseudomonomerous (monomerous?) gynoecia
of Anacardiaceae [14]. Some Anacardiaceae also have
a monosymmetric androecium, and the planes of
symmetry of the monosymmetric androecium and
gynoecium do not necessarily coincide (within the
range of infraspecific variation), and even in the case
of coincidence the plane of symmetry does not coin-
cide with the median plane of the flower [14]. As in
Araliaceae, the flower groundplan varies greatly
within Anacardiaceae, although it can be stable within
an individual species [14, 64].
The stability of the orientation of the monomerous
and pseudomonomerous gynoecium in the groups
characterized by stable orientation of this structure is
presumably due to the very early occurrence of the key
processes defining carpel morphogenesis during the
development of the flower. Revealingly enough, the
carpel primordium in legumes often becomes appar-
ent earlier than the primordia of the stamens of the
inner whorl [67]. However, pre-patterning of carpel
positions in flowers with a strictly acropetal appear-
ance of the primordia can occur earlier than the
demarcation of stamen positions (“bipolar pre-pat-
terning” of organ positions) [64, 70, 71].
Frequent orientation of the carpel of the mono-
merous gynoecium of flowering plants in the median
plane is indicative of putative direct morphogenetic
effects of the flower subtending bract and the axis of
the inflorescence. The taxonomically significant
diversity of orientation of the carpel of the monomer-
ous gynoecium in Australian Proteaceae-Greville-
oideae [72] is extremely interesting. The authors of the
study [72] state that the different variants of carpel ori-
entation in these plants are related to the diversity of
shapes of the f lower meristem after the initiation of the
perianth and androecium. Importantly, the inflores-
cence of these plants is a double raceme (with the term
“raceme” used in a broad sense) with two-flowered
second-order axes, which is very compact at the early
stages of development. The diversity of gynoecium
orientations in Australian Proteaceae may be related to
the interaction of morphogenetic signals from the
flower subtending bract and the subtending bract of
the second-order axis as well.
The instability of gynoecium orientation (includ-
ing that observed in monomerous gynoecia) similar to
that detected in Araliaceae and Anacardiaceae may be
due to the absence (or loss?) of the bipolar pre-pat-
terning of organ positions. Furthermore, the estab-
lishment of positions of carpels in a flower probably
occurs in members of these families at a later morpho-
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
GYNOECIUM EVOLUTION IN ANGIOSPERMS 103
genetic stage than, for example, in legumes. The char-
acter of perianth symmetry can affect carpel orienta-
tion. The position of the fertile carpel in Anacardia-
ceae can be associated with the position of the
outermost sepal in the case of imbricate eastivation of
the calyx [64]: that is, positional information of the
sepals is apparently more important than the morpho-
genetic effect of the subtending bract and the inflores-
cence axis in this case.
MIXOMERY: A PHENOMENON
RESEMBLING PSEUDOMONOMERY
BUT NOT IDENTICAL TO IT
A specific gynoecium type characterized by con-
siderable loss of carpel individuality that prevents the
assignment of ovules to individual carpels is some-
times partially confused with pseudomonomery in lit-
erature. We propose a novel term mixomery (derived
from the Greek words mixis (mixing) and meros
(part)) to describe these cases. Preliminary analysis
points at the existence of three variants of mixomerous
gynoecia characterized by central columnar, basal, or
parietal placentation.
The variant characterized by central columnar pla-
centation can be illustrated by an example of Lentibu-
lariaceae. In this case, the wall of a unilocular gynoe-
cium of two carpels (with two stigmas) is formed inde-
pendently of the central placenta with numerous
ovules arranged in a regular pattern; the gynoecium
wall is not connected to the placenta [73, 74].
P.K. Endress reported gynoecia with free central pla-
centa in representatives of ten families of eudicots of
five different orders and emphasized the initiation of
the gynoecium wall in the shape of a continuous ring,
with the lobes emerging later; the lobes could be
regarded as the apices of individual carpels, although
with certain ambiguity [74]. Almost complete loss of
carpel individuality was observed in unilocular gynoe-
cia of Primulaceae, where the carpels are fused along
the entire length and the numerous ovules are located
on the central columnar placenta that emerged as a
physical continuation of the flower axis and termi-
nated in the mature gynoecium without reaching the
top of the ovary [75, 76]. Endress [74] suggested that
the lobes developing on the top of the initially tubular
wall of Primulaceae gynoecium at the relatively late
stages [75, 76] are only necessary for the closure of the
apical opening, and, therefore, they are more likely to
be the analogues of the integument lobes that sur-
round the ovule micropile in different angiosperms.
The number of teeth formed upon capsule dehiscence
may be the only source of information on the number
of carpels in this case, but the fruits of Primulaceae do
not necessarily dehisce, and, besides, transverse
dehiscence that involves the separation of a lid can
occur in some plants.
Mixomery is also strongly manifested in gynoecia
that have a unilocular ovary with a single basal ortho-
tropous ovule and two or more stigmas (according to
the number of carpels that form the gynoecium) devel-
oped to the same extent. This gynoecium type is
superficially similar to pseudomonomerous gynoecia
with a single fertile ovule. However, the equal degree
of development of all carpels and the absence of carpel
dimorphism is a fundamental distinctive feature of the
mixomerous gynoecium. The basal ovule is formed
directly at the apex of the f loral meristem during mor-
phogenesis and cannot be attributed to any of the car-
pels, which is also evident from the analysis of flower
vasculature. Mixomerous gynoecia with a single cen-
tral orthotropous ovule are present in several angio-
sperm groups that could not be regarded as closely
related, for instance, in the families Piperaceae (Pipe-
rales) [77–79], Polygonaceae [80, 81], and Myrica-
ceae [82]. R. Sattler and his co-authors stated that
these gynoecia (as well as most gynoecia described
above) should be considered “acarpellate” due to the
presumed emergence of ovules on the axis of the
flower rather than on the carpels [82, 83]. Thus, we
return to the discussion of the possible interpretation
of a carpel as a megasporophyll. The point of view of
researchers who regard central basal (and columnar)
placentation as an evolutionarily derived state of the
trait in angiosperms (see, for example, [19, 84])
appears convincing to us. At least, this type of placen-
tation was not observed in any representative of the
basal grade of angiosperms [11]. However, there is no
reason to doubt the truly terminal location of the ovule
in Piperaceae, Polygonaceae, and Myricaceae. This is
confirmed by the entire body of data on the structure
and morphogenesis of the f lower in these plants. The
existence of a terminal ovule should not be considered
as morphological nonsense (comparable, for example,
to a terminal leaf). As mentioned above, the meristem
that gives rise to the ovule shares many features with
shoot apical meristem.
The emergence of a strictly terminal ovule charac-
terized by radial symmetry can be compared to the
emergence of terminal f lowers or f lower-like str uc-
tures in racemes, spikes, or thyrses reported for differ-
ent groups of angiosperms [85]. If similarity to the
emergence of terminal structures in the inf lorescences
is presumed, the terminal ovule can be assumed to
have evolved as a result of an abrupt transformation in
some cases, and this can explain the absence of clear
continuous ranges of transitional forms leading to
gynoecia with a terminal ovule (for instance, in Polyg-
onaceae). The similarity between the appearance of
terminal ovules in angiosperms and in conifers of the
genus Juniperus (Cupressaceae) [86] is even more
impressive. The ovules of conifers are usually located
on the ovuliferous scale that is fused to the bract in
Cupressaceae. However, a terminal ovule is located at
the end of the main axis of the female cone in certain
representatives of the genus Juniperus. This ovule can
104
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
SOKOLOFF et al.
be the only ovule of the cone and sometimes has three
planes of symmetry (associated with trimerous whorls
of scales in the cone) [86] rather than two, as in all
other conifers [87]. The example of Juniperus demon-
strates that the instances of terminal ovule emergence
are not unique for angiosperms. These instances con-
sidered in isolation apparently do not provide any
information on the morphological origin of the carpel.
The single terminally initiated ovule of certain
plant taxa retains radial symmetry at early develop-
mental stages only and becomes anatropous (in
Cyperaceae [88]), anatropous with a funiculus twisted
by 180 degrees (in Plumbaginaceae [89]), or bent to
varying degrees, often with a twisted funiculus (in
Chenopodiaceae [90, 91]) at the later stages. A change
in funiculus curvature of a single terminal ovule both
before and after pollination was demonstrated in the
genus Polycnemum closely related to Chenopodiaceae
[92]. The direction of ovule curvature could have been
used as an argument for the assignment of an ovule to
a specific carpel, but the validity of this argument
requires proof, preferably presented as a report of the
existence of a series of transitional forms. Moreover,
information on flower vasculature confirms the termi-
nal position of these ovules (see, for example, [88]).
The multilocular part of the gynoecium (the syna-
scidiate zone or the bases of plicate carpels congeni-
tally fused to the flower axis?) is located below the sin-
gle terminal ovule in certain groups, such as Juglans
[93, 94] and Basella [83]. This multilocular area
appears after the ovule initiation during morphogene-
sis. The position of the ovule in all these kinds of mix-
omerous gynoecium is indicative of partial loss of car-
pel individuality.
Most representatives of the clade that includes the
families Chenopodiaceae and Amaranthaceae have a
single ovule characterized by terminal initiation, but
the formation of numerous ovules on a free columnar
central placenta is observed in a small group of these
plants [80]. The presence of multiple ovules in this
group was hypothesized to represent an evolutionarily
derived state [64, 95]; this hypothesis is in good agree-
ment with the data of molecular phylogenetics [96].
Morphological interpretation and origin of the
gynoecium of Peperomia (Piperaceae) are of consider-
able interest. This closed tubular structure either has
no lobes on the edge or has two poorly developed lobes
that emerge at late developmental stages; a single basal
orthotropous ovule is located in the center of the
gynoecium [97, 98]. Phylogenetic data clearly demon-
strate that this gynoecium is derived from a mixomer-
ous gynoecium with a single basal ovule and several
stigmas [99]. The reduction of the number of carpels
to one is usually believed to have occurred upon the
emergence of Peperomia gynoecium (which is thus
monomerous), but the hypothesis of the origin of this
gynoecium upon a complete loss of carpel individual-
ity similar to that observed in Primulaceae is as valid as
the former one (for a review of the hypotheses, see
[97]).
The example of Cyperaceae convincingly demon-
strates the loss of evolutionary stability of the number
and position of carpels upon a partial loss of carpel
individuality [88]. Trimerous gynoecia of monocots
that do not have bracteoles on the pedicel usually con-
sist of a single median-abaxial carpel and two trans-
versal-adaxial carpels, with extremely rare exceptions
[100]. Dimerous gynoecia that can be interpreted as a
result of loss of the median carpel occur in many
Cyperaceae. In some Cyperaceae taxa, however, two
carpels are located in the median plane, that is why
their homology with the carpels of original trimerous
gynoecium remains obscure [88].
Basal or central columnar placentation is charac-
teristic of all mixomerous gynoecia described above.
The possibility of “collectivization” of ovules located
in the symplicate zone of a syncarpous gynoecium is of
considerable interest. Indeed, it is sometimes difficult
to assign a particular (or single) ovule located on the
parietal placenta to one of the neighboring carpels in
gynoecia with a fertile symplicate zone. These diffi-
culties arise (1) when numerous ovules are arranged in
multiple rows on a parietal placenta (for example, in
Papaveraceae [101]) and (2) in gynoecia with ortho-
tropous ovules or ovules bent in the vertical plane are
arranged in a single row on a parietal placenta. The
gynoecium of Scaphocalyx (Achariaceae, Malpighia-
les) is among the most convincing examples challeng-
ing the concept of the carpel. This gynoecium contains
a tubular ovary and five to seven stigmas. The ovule
wall bears orthotropous ovules, with one ovule at the
radius of each stigma (this is the lower circle of ovules)
and one ovule at each radius between the stigmas (the
upper circle of ovules) [102]. Thus, the degree of indi-
viduality of the carpels in the symplicate zone of the
gynoecium is likely to vary between the different
groups of flowering plants, and further research on
this issue appears justified.
CONCLUSIONS
The delimitation of pseudomonomerous and
monomerous gynoecia has traditionally been a key
point in the discussion related to these structures. We
believe that the existence of mixomerous gynoecia,
along with monomerous and pseudomonomerous
gynoecia, should be recognized. A monomerous
gynoecium consists of a single carpel. A pseudomono-
merous gynoecium is a particular case of a gynoecium
characterized by carpel dimorphism (one carpel is fer-
tile, whereas the other(s) are sterile). A mixomerous
gynoecium is characterized by partial or nearly com-
plete loss of carpel individuality, so that the assign-
ment of the ovule or ovules to specific carpels is
impossible in this case. A pseudomonomerous gynoe-
cium is a monosymmetric structure. If the morpho-
genesis of a pseudomonomerous gynoecium is stable
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
GYNOECIUM EVOLUTION IN ANGIOSPERMS 105
in a certain species, a special regulatory mechanism
that may show fundamental similarity to the regula-
tion of morphogenesis of flowers with a monosym-
metric perianth is expected to exist. The regulatory
mechanisms involved in the formation of floral mono-
symmetry were mostly addressed by studies of the
perianth and androecium, and, therefore, the analysis
of genetic mechanisms that underlie the development
of the pseudomonomerous gynoecium is a promising
area of research.
Many questions remain open in the area under
investigation, and the identification of gynoecium
type in the representatives of specific taxa is one of the
most important among these questions. Earlier reports
of the existence of pseudomonomery in some taxa
cannot be considered correct. The basic conditions for
the use of the transitional form criterion to reveal the
pseudomonomerous nature of gynoecium must be
clarified. An intermediate form is not necessarily a
putative transitional form. A form that corresponds to
a state fixed within a taxon usually allows for unambig-
uous interpretation. On the other hand, the use of ter-
atology data is much less likely to lead to reliable con-
clusions. Let us consider two related species with
flowers that contain a single carpel in one species and
two carpels in the other species. As the size of sample
of material investigated is increased to infinity, the
range of intermediate structural types that connect the
one- and two-carpel variants will expand towards
completion. However, this range will not necessarily
be reflective of the scenario of evolutionary transfor-
mation of the trait.
Gynoecia that combine the traits of pseudomono-
merous and mixomerous structures require further
analysis. For instance, two of the three carpel locules
in the gynoecium of Viburnum are regarded as strongly
reduced, whereas the common placenta of these two
carpels contains an ovule that extends into the large
locule of the third (sterile) carpel [103]. These cases
argue against the concept of pseudomonomery and
mixomery as two states of the same trait. It is probably
more appropriate to consider several individual traits,
including “carpel dimorphism” and “connections
between the ovules and specific carpels” as long as the
analysis of trait evolution is concerned.
ACKNOWLEDGMENTS
Analysis of the diversity of pseudomonomerous
gynoecia was performed with financial support from
the Russian Foundation for Basic Research, project
no. 15-04-05836, and the analysis of morphological
nature of the carpel was performed in the framework
of a government order to Moscow State University
(themes АААА-А16-116021660045-2 and АААА-
А16-116021660105-3).
REFERENCES
1. Doyle, J.A., Integrating molecular phylogenetic and
paleobotanical evidence on origin of the flower, Int. J.
Plant Sci., 2008, vol. 169, no. 7, pp. 816–843.
2. Doyle, J.A., Molecular and fossil evidence on the ori-
gin of angiosperms, Annu. Rev. Earth Planet. Sci., 2012,
vol. 40, pp. 301–326.
3. Frohlich, M.W. and Chase, M.V., After a dozen years of
progress the origin of angiosperms is still a great mys-
tery, Nature, 2007, vol. 450, no. 7173, pp. 1184–1189.
4. Sokoloff, D.D. and Timonin, A.C., Morphological and
molecular data on the origin of angiosperms: On a way
to a synthesis, Zh. Obshch. Biol., 2007, vol. 68, no. 2,
pp. 83–97.
5. Endress, P.K., Evolutionary diversification of the f low-
ers in angiosperms, Am. J. Bot., 2011, vol. 98, no. 3,
pp. 370–396.
6. Prenner, G. and Rudall, P.J., Comparative ontogeny of
the cyathium in Euphorbia and its allies: Exploring the
organ – flower – inflorescence boundaries, Am. J. Bot.,
2007, vol. 94, no. 10, pp. 1612–1629.
7. Sokoloff, D.D., Rudall, P.J., and Remizowa, M.V.,
Flower-like terminal structures in racemose inf lores-
cences: A tool in morphogenetic and evolutionary
research, J. Exp. Bot., 2006, vol. 57, no. 13, pp. 3517–
3530.
8. Rudall, P.J., Remizowa, M.V., Prenner, G., Pry-
chid, C.J., Tuckett, R.E., and Sokoloff, D.D., Non-
flowers near the base of extant angiosperms? Spatio-
temporal arrangement of organs in reproductive units of
Hydatellaceae and its bearing on the origin of the
flower, Am. J. Bot., 2009, vol. 96, no. 1, pp. 67–82.
9. Sokoloff, D.D., Remizowa, M.V., Linder, H.P., and
Rudall, P.J., Morphology and development of the
gynoecium in Centrolepidaceae: The most remarkable
range of variation in Poales, Am. J. Bot., 2009, vol. 96,
no. 11, pp. 1925–1940.
10. Endress, P.K. and Doyle, J.A., Reconstructing the
ancestral flower and its initial specializations, Am. J.
Bot., 2009, vol. 96, no. 1, pp. 22–66.
11. Endress, P.K., The flowers in extant basal angiosperms
and inferences on ancestral flowers, Int. J. Plant Sci.,
2001 , vol. 162, no. 5, pp. 1111 –1140.
12. Kedrov, G.B., To the definition of the type of gyne-
cium, Vestn. Mosk. Univ., Ser. Biol. Pochv., 1969, no. 6,
pp. 44–47.
13. Philipson, W.R., Is the grass gynoecium monocarpel-
lary?, Am. J. Bot., 1985, vol. 72, no. 12, pp. 1954–1961.
14. Bachelier, J.B. and Endress, P.K., Comparative floral
morphology and anatomy of Anacardiaceae and
Burseraceae (Sapindales), with a special focus on
gynoecium structure and evolution, Bot. J. Linn. Soc.,
2009, vol. 159, no. 4, pp. 499–571.
15. Shamrov, I.I. and Yandovka, L.F., Development and
structure of gynecium and ovule in Cerasus vulgaris
(Rosaceae), Bot. Zh., 2008, vol. 93, no. 6, pp. 902–914.
16. Shamrov, I.I., The morphological nature of gynecium
and fruit in Ceratopyllum (Ceratophyllaceae), Bot. Zh.,
2009, vol. 94, no. 7, pp. 938–961.
106
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
SOKOLOFF et al.
17. Sokoloff, D.D., Correlations between gynoecium mor-
phology and ovary position in angiosperm f lowers:
Roles of developmental and terminological constraints,
Zh. Obshch. Biol., 2015, vol. 76, no. 2, pp. 146–160.
18. Bailey, I.W. and Swamy, B.G.L., The conduplicate
carpel of dicotyledons and its initial trends of special-
ization, Am. J. Bot., 1951, vol. 38, no. 5, pp. 373–379.
19. Takhtajan, A., Evolutionary Trends in Flowering Plants,
New York: Columbia Univ. Press, 1991.
20. Swamy, B.G.L. and Periasamy, K., The concept of the
conduplicate carpel, Phytomorphology, 196 4, vol. 14,
no. 7, pp. 319–327.
21. Verbeke, J.A., Fusion events during floral morphogen-
esis, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1992,
vol. 43, pp. 583–598.
22. Endress, P.K., Origins of flower morphology, J. Exp.
Zool. (Mol. Dev. Evol.), 2001, vol. 291, no. 2, pp. 105–
115 .
23. Endress, P.K., Angiosperm floral evolution: Morpho-
logical developmental framework, Adv. Bot. Res., 2006,
vol. 44, pp. 1–61.
24. Theißen, G. and Saedler, H., Floral quartets, Nature,
2001, vol. 409, no. 6819, pp. 469–471.
25. Becker, A., Kaufmann, K., Freialdenhoven, A., Vin-
cent, C., Li, M.-A., Saedler, H., and Theissen, G.,
A novel MADS-box gene subfamily with a sister-group
relationship to class B floral homeotic genes, Mol.
Genet. Genomics, 2002, vol. 266, no. 6, pp. 942–950.
26. de Almeida, A.M.R., Yockteng, R., Schnable, J., Alva-
rez-Buylla, E.R., Freeling, M., and Specht, C.D., Co-
option of the polarity gene network shapes filament
morphology in angiosperms, Sci. Rep., 2014, vol. 4,
article 6194.
27. Prunet, N. and Meyerowitz, E.M., Genetics and plant
development, C. R. Biol., 2016, vol. 339, nos. 7–8,
pp. 240–246.
28. Meyen, S.V., Origin of the Angiosperm gynoecium by
gamoheterotopy, Bot. J. Linn. Soc., 1988, vol. 97, no. 2,
pp. 171–178 .
29. Frohlich, M.W. and Parker, D.S., The Mostly Male
Theory of flower evolutionary origins: From genes to
fossils, Syst. Bot., 2000, vol. 25, no. 2, pp. 155–170.
30. Frohlich, M.W., An evolutionary scenario for the origin
of flowers, Nat. Rev. Genet., 2003, vol. 4, no. 7,
pp. 559–566.
31. Groß-Hardt, R., Lanhard, M., and Laux, T., WUS-
CHEL signalling functions in interregional communi-
cation during Arabidopsis ovule development, Genes
Dev., 2002, vol. 16, no. 9, pp. 1129–1138.
32. Mathews, S. and Kramer, E.M., The evolution of
reproductive structures in seed plants: A re-examina-
tion based on insights from developmental genetics,
New Phytol., 2012, vol. 19 4, no . 4, pp. 910–923.
33. Leins, P. and Erbar, C., Flower and Fruit. Morphology,
Ontogeny, Phylogeny, Function and Ecology, Stuttgart:
Schweizerbart, 2010.
34. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J.,
Baumann, E., Wisman, E., and Yanofsky, M.F.,
Assessing the redundancy of MADS-box genes during
carpel and ovule development, Nature, 2003, vol. 424,
no. 6944, pp. 85–88.
35. Endress, P.K., Diversity and Evolutionary Biology of
Tropical Flowers, Cambridge: Univ. Press, 1994.
36. Weberling, F., Morphology of Flowers and Inflores-
cences, Cambridge: Univ. Press, 1989.
37. Endress, P.K., Syncarpy and alternative modes of
escaping disadvantages of apocarpy in primitive angio-
sperms, Taxon, 1982, vol. 31, no. 1, pp. 48–52.
38. Armbruster, W.S., Debevec, E.M., and Wilson, M.F.,
Evolution of syncarpy in angiosperms: Theoretical and
phylogenetic analyses of the effects of carpel fusion on
offspring quantity and quality, J. Evol. Biol., 2002,
vol. 15, no. 4, pp. 657–672.
39. Endress, P.K., Jenny, M., and Fallen, M.E., Conver-
gent elaboration of apocarpous gynoecia in higher
advanced dicotyledons (Sapindales, Malvales, Genti-
anales), Nord. J. Bot., 1983, vol. 3, no. 3, pp. 293–300.
40. Stauffer, F.W. and Endress, P.K., Comparative mor-
phology of the female f lowers and systematics in
Geonomeae (Arecaceae), Plant Syst. Evol., 2003,
vol. 242, no. 1, pp. 171–203.
41. Remizowa, M.V., Sokoloff, D.D., and Rudall, P.J.,
Evolution of the monocot gynoecium: Evidence from
comparative morphology and development in Tof ieldia,
Japonolirion, Petrosavia and Narthecium, Plant Syst.
Evol., 2006, vol. 258, no. 3, pp. 183–209.
42. Saunders, E.R., On carpel polymorphism. I, Ann. Bot.,
1925, vol. 39, no. 1, pp. 123–167.
43. Eames, A.J., The vascular anatomy of the flower with
refutation of the theory of carpel polymorphism, Am. J.
Bot., 1931, vol. 18, no. 3, pp. 147–188.
44. Igersheim, A., Buzgo, M., and Endress, P.K., Gynoe-
cium diversity and systematics in basal monocots, Bot.
J. Linn. Soc., 2001, vol. 136, no. 1, pp. 1–65.
45. McConchie, C.A., Ducker, S.C., and Knox, R.B.,
Biology of Australian seagrasses: Floral development
and morphology in Amphibolis (Cymodoceaceae), Aus-
tral. J. Bot., 1982, vol. 30, no. 3, pp. 251–264.
46. Leinfellner, W., Zur Morphologie des Gynözeums der
Polygalaceen, Österr. Bot. Z., 1972, vol. 120, no. 1,
pp. 51–76.
47. Magin, N., Eine blütenmorphologische Analyse der
Lagoecieae (Apiaceae), Plant Syst. Evol., 1980, vol. 133,
no. 3, pp. 239–259.
48. Remizowa, M.V., Sokoloff, D.D., and Rudall, P.J.,
Evolutionary history of the monocot flower, Ann. Mis-
souri Bot. Gard., 2010, vol. 97, no. 4, pp. 617–645.
49. Endress, P.K. and Rapini, A., Floral structure of
Emmotum (Icacinaceae sensu stricto or Emmotaceae),
a phylogenetically isolated genus of lamiids with a
unique pseudotrimerous gynoecium, bitegmic ovules
and monosporangiate thecae, Ann. Bot., 2014, vol. 114,
no. 5, pp. 945–959.
50. Uhl, N.W. and Moore, H.E., The palm gynoecium,
Am. J. Bot., 1971, vol. 58, no. 10, pp. 945–992.
51. Eckardt, T., Untersuchungen über Morphologie,
Entwicklungsgeschichte und systematische Bedeutung
des pseudomonomeren Gynoeceums, Nova Acta Leop-
old., 1937, vol. 5, no. 26, pp. 1–112.
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
GYNOECIUM EVOLUTION IN ANGIOSPERMS 107
52. Angiosperm Phylogeny Group, An update of the
Angiosperm Phylogeny Group classification for the
orders and families of flowering plants: APG IV, Bot. J.
Linn. Soc., 2016, vol. 181, no. 1, pp. 1–20.
53. Kircher, P., Untersuchungen zur Blüten- und Inflo-
reszenzmorphologie, Embryologie und Systematik der
Restionaceen im Vergleich mit Gramineen und verwand-
ten Familien, Berlin, Stuttgart: J. Cramer, 1986.
54. Briggs, B.G., Marchant, A.D., and Perkins, A.J., Phy-
logeny of the restiid clade (Poales) and implications for
the classification of Anarthriaceae, Centrolepidaceae
and Australian Restionaceae, Taxon, 2014, vol. 63, no.
1, pp. 24–46.
55. Linder, H.P., The gynoecia of Australian Restionaceae:
Morphology, anatomy and systematic implications,
Austral. Syst. Bot., 1992, vol. 5, no. 2, pp. 227–245.
56. Fomichev, C.I., Barrett, M.D., Briggs, B.G., Macfar-
lane, T.D., and Sokoloff, D.D., Inflorescence, flower
and fruit morphology of Hopkinsia anoectocolea (Anar-
thriaceae) and multiple origins of one-seeded fruits in
the graminid clade of Poales, XIX International Botani-
cal Congress. Abstract. Book II. Shenzhen, 2017,
pp. 132–133.
57. Ronse De Craene, L.P., Linder, H.P., and Smets, E.F.,
Ontogeny and evolution of the flowers of South African
Restionaceae with special emphasis on the gynoecium,
Plant Syst. Evol., 2002, vol. 231, no. 1, pp. 225–258.
58. Sokoloff, D.D., Remizowa, M.V., and Rudall, P.J.,
Is syncarpy an ancestral condition in monocots and
core eudicots?, in Early Events in Monocot Evolution,
Wilkin, P. and Mayo, S.J., Eds., Cambridge: Univ.
Press, 2013, pp. 60–81.
59. Volgin, S.A., Morphology and vascular anatomy of the
flower Trichostigma peruviana (Moq.) H. Walt. (Phyto-
laccaceae), Byul. MOIP. Otd. Biol., 1986, vol. 91, n o. 1,
pp. 96–102.
60. Philipson, W.R., Griseliinia Forst., fil. – anomaly or
link?, New Zeal. J. Bot., 1967, vol. 5, no. 1, pp. 134–
165.
61. Karpunina, P.V., Oskolski, A.A., Nuraliev, M.S.,
Lowry, P.P., Degtjareva, G.V., Samigullin, T.H.,
Valiejo-Roman, C.M., and Sokoloff, D.D., Gradual
versus abrupt reduction of carpels in syncarpous gynoe-
cia: A case study from Polyscias subg. Arthrophyllum
(Araliaceae: Apiales), Am. J. Bot., 2016, vol. 103, no. 12,
pp. 2028–2057.
62. Jabbour, F., Damerval, C., and Nadot, S., Evolution-
ary trends in the f lowers of Asteridae: Is polyandry an
alternative to zygomorphy?, Ann. Bot., 2008, vol. 102,
no. 2, pp. 153–165.
63. Cubas, P., Floral zygomorphy, the recurring evolution
of a successful trait, BioEssays, 2004, vol. 26, no. 11,
p p . 117 5– 11 8 4.
64. Ronse De Craene, L.P., Floral Diagrams: An Aid to
Understanding Flower Morphology and Evolution, Cam-
bridge: Univ. Press, 2010.
65. Endress, P.K., Symmetry in flowers: Diversity and evo-
lution, Int. J. Plant Sci., 1999, vol. 160, no. S6, pp. S3–
S23.
66. Eichler, A.W., Blüthendiagramme. Teil 2, Leipzig:
W. Engelmann, 1878.
67. Tucker, S.C., Floral development in legumes, Plant
Physiol., 2003, vol. 131, no. 3, pp. 911–926.
68. Nuraliev, M.S., Oskolski, A.A., Sokoloff, D.D., and
Remizowa, M.V., Flowers of Araliaceae: Structural
diversity, developmental and evolutionary aspects,
Plant Divers. Evol., 2010, vol. 128, nos. 1–2, pp. 247–
268.
69. Karpunina, P.V., Oskolski, A.A., Nuraliev, M.S., and
Oskolski, A.A., Patterns of carpel arrangement in
gynoecia of Araliaceae: Evidence from Polyscias,
IX Apiales Symposium. Abstract Book, Oskolski, A.,
Nuraliev, M., and Tilney, P., Eds., Guangzhou, 2017,
pp. 15–16.
70. Choob, V.V. and Penin, A.A., Structure of flower in
Arabidopsis thaliana: Spatial pattern formation, Russ. J.
Dev. Biol., 2004, vol. 35, no. 4, pp. 224–227.
71. Endress, P.K., Evolution of floral diversity: The phylo-
genetic surroundings of Arabidopsis and Antirrhinum,
Int. J. Plant Sci., 1992, vol. 153, no. 3, pp. S106–S122.
72. Douglas, A.W. and Tucker, S.C., The developmental
basis of diverse carpel orientations in Grevilleoideae
(Proteaceae), Int. J. Plant Sci., 1996, vol. 157, no. 4,
pp. 373–397.
73. Degtjareva, G.V. and Sokoloff, D.D., Inflorescence
morphology and f lower development in Pinguicula
alpina and P. vulgaris (Lentibulariaceae: Lamiales):
Monosymmetric f lowers are always lateral and occur-
rence of early sympetaly, Org. Divers. Evol., 2012,
vol. 12, no. 2, pp. 99–111.
74. Endress, P.K., Patterns of angiospermy development
before carpel sealing across living angiosperms: Diver-
sity, and morphological and systematic aspects, Bot. J.
Linn. Soc., 2015, vol. 178, no. 4, pp. 556–591.
75. Caris, P., Ronse De Craene, L.P., Smets, E., and
Clinckemaillie, D., Floral development of three Maesia
species, with special emphasis on the position of the
genus within Primulales, Ann. Bot., 2000, vol. 86, no. 1,
pp. 87–97.
76. Caris, P.L. and Smets, E.F., A floral ontogenetic study
on the sister group relationship between the genus
Samolus (Primulaceae) and the Theophrastaceae, Am.
J. Bot., 2004, vol. 91, no. 5, pp. 627–643.
77. Tucker, S.C., Inflorescence and flower development in
the Piperaceae. III. Floral ontogeny of Piper, Am. J.
Bot., 1982, vol. 69, no. 9, pp. 1389–1401.
78. Liang, H.-X. and Tucker, S.C., Floral ontogeny of Zip-
pelia begoniaefolia and its familial affinity: Saururaceae
or Piperaceae?, Am. J. Bot., 1995, vol. 82, no. 5,
pp. 681–689.
79. Johnson, D.S., On the development of certain Pipera-
ceae, Bot. Gaz., 1902, vol. 34, no. 5, pp. 321–340.
80. Payer, J.B., Traité d’organogénie compare de la fleur,
Paris: Masson, 1857.
81. Galle, P., Untersuchungen zur Blütenentwicklung der
Polygonaceen, Bot. Jahrb. Syst., 1977, vol. 98, no. 4,
pp. 449–489.
82. Macdonald, A.D. and Sattler, R., Floral development
of Myrica gale and the controversy over floral concepts,
Can. J. Bot., 1973, vol. 51, no. 10, pp. 1965–1975.
83. Sattler, R. and Lacroix, C., Development and evolu-
tion of basal cauline placentation: Basella rubra, Am. J.
Bot., 1988, vol. 75, no. 6, pp. 918–927.
108
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN Vol. 72 No. 3 2017
SOKOLOFF et al.
84. Cresens, E.M. and Smets, E.F., The carpel: A problem
child of floral morphology and evolution, Bull. Jard.
Bot. Nat. Belg., 1989, vol. 59, nos. 3–4, pp. 377–409.
85. Sokoloff, D.D., Rudall, P.J., and Remizowa, M.V.,
Flower-like terminal structures in racemose inf lores-
cences: A tool in morphogenetic and evolutionary
research, J. Exp. Bot., 2006, vol. 57, no. 13, pp. 3517–
3530.
86. Schulz, C., Jagel, A., and Stützel, T., Cone morphol-
ogy in Juniperus in the light of cone evolution in
Cupressaceae s.l, Flora, 2003, vol. 198, no. 3, pp. 161–
177.
87. Meyen, S.V., Basic features of gymnosperm systematics
and phylogeny as evidenced by the fossil record, Bot.
Rev., 1984, vol. 50, no. 1, pp. 1–111.
88. Reynders, M., Vrijdaghs, A., Larridon, I., Huygh, W.,
Leroux, O., Muasya, A.M., and Goetghebeur, P.,
Gynoecial anatomy and development in Cyperoideae
(Cyperaceae, Poales): Congenital fusion of carpels
facilitates evolutionary modif ications in pistil structure,
Plant Ecol. Evol., 2012, vol. 145, no. 1, pp. 96–125.
89. De Laet, J., Clinckemaillie, D., Jansen, S., and Smets,
E., Floral ontogeny in the Plumbaginaceae, J. Plant
Res., 1995, vol. 108, no. 3, pp. 289–30 4.
90. Konycheva, V.I. and Kadyrova, R.U., Chenopodia-
ceae, in Sravnitel’naya embriologiya tsvetkovykh rastenii.
Phytolaccaceae-Thymelaeaceae (Comparative Embryol-
ogy of Flowering Plants. Phytolaccaceae-Thyme-
laeaceae), Yakovlev, M.S, Ed., Leningrad: Nauka,
1983, pp. 49–52.
91. Olvera, H.F., Smets, E., and Vrijdaghs, A., Floral and
inflorescence morphology and ontogeny in Beta vul-
garis, with special emphasis on the ovary position, Ann.
Bot., 2008, vol. 643–651, no. 4, pp. 643–651.
92. Veselova, T.D., Dzhalilova, K.K., and Timonin, A.C.,
Embryology of Polycnemum arvense L. (lower core
Caryophyllales), Wulfenia, 2016, vol. 23, pp. 221–240.
93. Langdon, L.M., Ontogenetic and anatomical studies of
the flower and fruit of the Fagaceae and Juglandaceae,
Bot. Gaz., 1939, vol. 101, no. 2, pp. 301–327.
94. Schaffer, K.L., George, M.F., Peleg, M., Gar-
rett, H.E., and Cecich, R.A., Pistillate flower devel-
opment in eastern black walnut, Can. J. For. Res., 1996,
vol. 26, no. 8, pp. 1514–1519.
95. Ronse De Craene, L.P., Volgin, S.A., and Smets, E.F.,
The floral development of Pleuropetalum darwinii, an
anomalous member of the Amaranthaceae, Flora,
1999, vol. 194, no. 2, pp. 189–199.
96. Sukhorukov, A.P., Mavrodiev, E.V., Struwig, M.,
Nilova, M.V., Dzhalilova, K.K., Balandin, S.A.,
Erst, A., and Krinitsyna, A.A., One-seeded fruits in
the core Caryophyllales: Their origin and structural
diversity, PLoS ONE, 2015, vol. 10, no. 2, e0117974.
97. Tucker, S.C., Inflorescence and flower development in
the Piperaceae. I. Peperomia, Am. J. Bot., 1980, vol. 67,
no. 5, pp. 686–702.
98. Remizowa, M.V., Rudall, P.J., and Sokoloff, D.D.,
Evolutionary transitions among flowers of perianthless
piperales: Inferences from inflorescence and f lower
development in the anomalous species Peperomia fra-
seri (Piperaceae), Int. J. Plant Sci., 2005, vol. 166, no. 6,
pp. 925–943.
99. Wanke, S., Vanderschaeve, L., Mathieu, G., Nein-
huis, C., Goetghebeur, P., and Samain, M.S., From
forgotten taxon to a missing link? The position of the
genus Verhuellia (Piperaceae) revealed by molecules,
Ann. Bot., 2007, vol. 99, no. 6, pp. 1231–1238.
100. Remizowa, M.V., Rudall, P.J., Choob, V.V., and
Sokoloff, D.D., Racemose inflorescences of mono-
cots: Structural and morphogenetic interaction at the
flower/inflorescence level, Ann. Bot., 2013, vol. 112,
no. 8, pp. 1553–1566.
101. Endress, P.K., Floral structure and evolution in
Ranunculanae, in Systematics and Evolution of the
Ranunculiflorae. Plant Systematics and Evolution. Sup-
plement 9, Jensen, U. and Kadereit, J.W., Eds.,
Vienna: Springer, 1995, vol. 9, pp. 47–61.
102. van Heel, W.A., Flowers and fruits in Flacourtiaceae.
I. Scaphocalyx spathacea Ridl., Blumea, 1973, vol. 21,
no. 2, pp. 259–279.
103. Wilkinson, A.M., Floral anatomy and morphology of
some species of Viburnum of the Caprifoliaceae, Am. J.
Bot., 1948, vol. 35, no. 8, pp. 455–465.
Translated by S. Semenova