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Accepted Ar tic le
Comparative anther and pistil anatomy of three flowering morphs of Acer
oblongum Wall. ex DC. (Sapindaceae s.l.) and its adaptive significance
Neha Yadav, Arun K. Pandey, Ashok K. Bhatnagar
Department of Botany, University of Delhi, Delhi – 110007, India
Corresponding author: Arun K. Pandey, Department of Botany, University of Delhi,
Delhi – 110007, India. Email: [email protected]
Decision date: 17-Oct-2017
This article has been accepted for publication and undergone full peer review but has
not been through the copyediting, typesetting, pagination and proofreading process,
which may lead to differences between this version and the Version of Record. Please
cite this article as doi: [10.1111/njb.01572].
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Abstract
A comparative anatomical study of reproductive parts of the three floral morphs of Acer
oblongum (Sapindaceae) was done to ascertain the functionality of the parts present and
its adaptive significance. Individual trees of A. oblongum possess three types of flower
morphs. Though morphologically all flowering morphs appeared to be bisexual,
temporally the male or female function is suppressed to achieve successful crosspollination. In addition, the role of endothecial thickenings in selective dehiscence of
anther was also studied. Anatomical analysis showed the presence of fibrous
thickenings in the cells of endothecium of staminate type I flowers. However, minimal
opening of anther along the line of dehiscence was observed in hermaphrodite flowers
that showed poor differentiation of endothecium. Although endothecium is formed in
anthers of hermaphrodite flowers, the failure of anthers to dehisce is because not all the
endothecial cells showed the presence of fibrous thickenings, especially towards the
stomium. Mature pollen grains in hermaphrodite flowers were formed only after stigma
divergence when the receptivity was already lost (after Stage 3). Pistil anatomy revealed
functional embryo sac in only hermaphrodite flowers. Functionally male flowers, with
undeveloped pistil, serve as the only source of pollen for fertilization.
Keywords: Acer oblongum, floral morphs, anther anatomy, endothecial thickenings,
pistil structure, receptivity, stigma, stomium.
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Introduction
The genus Acer comprises approximately 160 species (van Gelderen et al. 1994)
distributed across the world. With a centre of diversity in China, maples range across
the northern hemisphere from North America to Europe, the very north of Africa, most
of the Asia, including the Himalaya (Gibbs & Chen 2009). Maples are known for their
extensive foliage and autumn leaf colour phenomenon. Often species of Acer blossom
in early spring providing abundant pollen and nectar to the bees and other insects
(Haragsim 1977, Batra 1985).
Acer oblongum (Himalayan maple) is a 15-18 m tall semi-deciduous tree. It is an
economically important species known for its valuable timber. The trees flower from
late February to early April, showing an andromonoecious type of sexual system
(Yadav et al. 2016). Andromonoecy is the occurrence of male and hermaphrodite
(perfect) flowers on the same individual. Three types of floral morphs viz., staminate
type I, hermaphrodite and staminate type II, develop on the same tree in the Central
Himalaya. Staminate type I flowers are pentamerous, pedicellate, hypogynous,
morphologically perfect (rudimentary pistil is present), with 9 to11 anthers present in
two whorls. A rudimentary pistil can be seen with the help of hand lens as it is
surrounded by tuft of hairs. Staminate type II flowers resemble staminate type I in all
aspects except that these have an abortive pistil rather than rudimentary. Pistil abortion
in these flowers is seen at varying stages but the ovary remains undeveloped with
abortive ovules. The number of anthers is 8 or 9 in staminate type II flowers.
Hermaphrodite flowers are morphologically perfect, having both androecium and
gynoecium. Stigma is dry, papillate and bifid. (For different floral morph types see
result section). Anthers in hermaphrodite flowers cannot be distinguished in two whorls.
Temporal separation of flowering between different floral morphs was observed.
Staminate type I mark the inception of flowering dominating the trees in early March,
followed by the emergence of buds of hermaphrodite flowers and staminate type II
flowers in mid of March. The staminate type II flowers open a little later (when the
stigma of hermaphrodite flowers becomes receptive). The flowers are borne terminally
in corymbose inflorescences and are odourless and nectarless. The proportion of
different flowering morphs on an inflorescence varied and staminate type I flowers
accounted for the highest proportion (72%), followed by hermaphrodite (15-16%) and
staminate type II flowers (11-13%). Temperature plays an important role in regulating
the appearance of three flowering morphs. When the temperature is mildly cold (17-19
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°C) in early March, the staminate type I flowers appear, but with an increase in
temperature (20-25°C) the development of hermaphrodite and staminate type II flowers
is seen (Yadav et al. 2016). Continued low temperature often results in a delay in
flowering of staminate type II flowers. The flowers of A. oblongum are known to show
mixed syndromes of entomophily in floral structure and anemophily in pollen
characteristics (Yadav et al. 2016).
The genus Acer has been worked upon by many authors for its various
anatomical and embryological aspects because of its diversity in floral architecture.
Comparative studies included some aspects of floral anatomy in Acer saccharum (Peck
& Lersten 1991), Acer pseudoplatanus (Anderson & Guard 1964; Haragsim 1977), and
Acer negundo (Beskaravainaya 1961, Hall 1951, 1954). Hall (1951) studied floral
anatomy of nine species of the genus Acer owing to considerable variation in floral
structure. Studies on the structure of nectaries have also been attempted (WeryszkoChmielewska & Sulborska 2011). The anatomical structure of wood and petiole in Acer
species has been investigated by different workers (Solereder 1899). Other studies
carried out on Acer include biosystematic studies on flowering and sex expression (de
Jong 1976, Sato 2002), reproductive biology (Sullivan 1983, Sakai 1990, Saeki 2008),
phylogenetic analysis and evolutionary trends towards dioecy (Renner et al. 2007).
Yang et al. (2015) have studied genetic diversity using microsatellite markers in some
maple species.
Only a few species of Acer have been studied from the anatomical point of view
(Jacobs & Lersten 1994). Despite being an economically important taxon, the
anatomical aspects of Acer reproductive structures and processes have not received
much attention. The observations are limited and scattered too. Khushalani (1963)
studied microsporogenesis in A. oblongum, but there was no mention of different
flowering morphs and their anatomical details. In the present study, a comparative
anatomical study of reproductive structures of three floral morphs was carried out to
elucidate their functional adaptations and also assess the role of endothecial thickenings
in anther dehiscence. Our study aims to document anatomical details of reproductive
parts of three flowering morphs of A. oblongum and their evolutionary significance.
Material and methods
Field observations and plant material collections were made at three sites over a period
of three years, (2013-15), in the northern hill state of Uttarakhand (Central Himalaya),
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India (details in Yadav et al. 2016). GPS locations and site descriptions were noted for
future reference and studies. The flowers examined were from individual trees growing
in the populations of Dehradun and Nainital.
Floral buds and inflorescences were fixed in formalin-acetic acid-alcohol (FAA)
in the ratio of 1:1:18 (Johansen 1940). Fixation was carried out in glass vials for 18-24 h
at room temperature and the material was later stored in 70% ethanol. The material was
processed for resin sectioning (Feder & O’Brien 1968) and paraffin sectioning (O’Brien
& McCully 1981). To enhance fixation, the plant materials were dissected before or
after fixation to remove extraneous parts. Buds and floral parts were dehydrated in
glycol methacrylate and tertiary butyl alcohol for resin and paraffin sectioning
respectively. Sections, between 2.5 and 5 µm thick, were obtained from resin sectioning
using glass knives. The sections were stained with Toluidine Blue O’ (TBO) and were
viewed under a light microscope and photographs were accessed. Sections of staminate
types were cut for bithecous, partially dehisced and completely dehisced anthers. In the
case of hermaphrodite flowers, anther sections were cut at various stages of pistil
development since no visual changes in anther development were observed. Four
different stages of development of pistil viz. S1, S2, S3, S4 were observed. S1 (when
the stigmatic lobes had small surface area with small papillae and style was not seen);
S2 (Stigmatic lobes spread with longer papillae and a short style was visible, tips of
stigma were red); S3 (stigmatic lobes started to curve inwards, stigmatic papillae were
fully elongated and style fully differentiated); S4 (stigmatic lobes fully curved with
wing differentiation from lateral walls of ovary, and papillae started turning brown in
color). Stages S1, S3 and S4 were designated for study. Stage 2 was not taken for
anatomical studies because there was not much visible difference in the appearance of
stamen within the two stages (S1, S2) of flower development. Pistil anatomy was
investigated to observe the papillae type in three different morphs and to ascertain
whether functional embryo sac is formed in morphologically hermaphrodite flowers or
not.
For SEM studies, different parts of flowers were fixed in freshly prepared
Karnowsky’s fluid for 12 h at 4°C (Karnowsky 1965), with 0.2 M phosphate buffer at a
pH of 7.4 (O’Brien & McCully 1968). After fixation, samples were washed once with
buffer and were dehydrated in ascending acetone series (10% to 100%) at room
temperature, RT, (25±2°C) for 20 min each. Using liquid CO2 the samples were critical
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point dried in Polaron Critical Point Drier (Serial No. 12-09-R-711/A) at 31.5°C with
1100 p.s.i. Dehydrated samples were mounted on aluminium stubs and were coated with
gold particles (100 Å thickness) under vacuum on sputter coating unit (JEOL JFC-1600
Auto Fine Coater, Tokyo, Japan) for 19 sec (Hill & West 1982). The coated material
was viewed under scanning electron microscope, JEOL JSM-6610LV (Tokyo, Japan),
at an accelerating voltage of 3-5 KV, at the Department of Botany, University of Delhi.
Results
Anther anatomy
The three different types of flowering morph are shown in (Fig. 1). In staminate type I
flowers, androecium occur in two whorls and the number of stamens ranges from 9 to
11. The young anthers are bithecal and tetrasporangiate (Fig. 2A, 3A). The archesporial
cells divides to form sporogenous cells and a primary parietal layer. The latter finally
gives rise to four wall layers below the epidermis: an endothecium, two middle layers,
and a tapetum. At the free microspore stage, the endothecium cells are radially
elongated and develop the characteristic fibrous thickenings. The two middle layers are
ephemeral and degenerate relatively early during pollen development. The glandular
tapetum (Secretory type) comprises of two- and three-nucleate cells, and nuclear fusions
are seen. Microspore mother cells undergo meiosis followed by centripetal furrows. The
tetrads are tetrahedral and isobilateral. The pollen grains are tri-colporate and two-celled
when shed. Histological studies of the anthers of staminate types viz., staminate type I
(Fig. 2), staminate type II (Fig. 3), and S1, S3 and S4 stages of hermaphrodite flowers
(Fig. 4), revealed that functional pollen grains are discharged only in staminate types,
whereas only partial opening of anthers takes place in the hermaphrodite flowers and
their pollen is not discharged. The anther wall layers (epidermis, endothecium, middle
layers and tapetum) were similar in both types of staminate flowers (Fig. 2A, 3A). The
septal cells separating the two microsporangia of each theca break down, resulting in
anthers with two locules (Fig. 2B, 3B).
In the hermaphrodite flowers, no such
disintegration of septal cells was seen in any of the three developmental stages (Fig. 4AC). Although in hermaphrodite flowers the anthers shrivelled at the stage 4 and the
stomium is anatomically similar to that of staminate flower types, there was still no
opening of the stomium (Fig. 4C). In staminate type I, pollen maturation occurs during
bud development and the pollen is fully developed at anthesis (Fig. 2A). However, this
process is delayed in hermaphrodite flowers, and mature pollen grains are observed only
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after the divergence of the stigmatic lobes, when stigmatic receptivity is lost (i.e. after
S3 stage) (Fig. 4B-C). In staminate flower types, the anther opens along the stomium
slit in both thecae, and the dehiscence of anther is thus longitudinal (Fig. 2C-E, 3C-D).
In addition, well-developed fibrous thickenings were seen in every endothecial cell (Fig.
2D), especially in the endothecial cells near stomium (Fig. 3E-F). However, in anthers
of the hermaphrodite flowers, although the endothecium had thickenings in a similar
manner to that of staminate flower types, but the thickenings were not present in each
cell of the wall layer (Fig. 4E). In addition, it was observed with SEM that the slit at the
stomium region was minimal and the pollen grains were not released (Fig. 4D-E). In
staminate flower types, hydrated pollen grains within the anther were spheroidal (Fig.
2F), but they were ellipsoid after the pollen grains were released (Fig. 2G). The mature
pollen exine is striate in the three flower morphs and there are no additional
palynological differences between the staminate and hermaphrodite flowers.
In hermaphrodite flowers, filaments remain short throughout development and
the pistil is 1-2 mm above the level of anthers (spatial as well as temporal separation)
(Yadav et al. 2016). Stamens of hermaphrodite functionally pistillate flowers are
shrivelled and eventually degenerate unopened as the fruit develops (Fig. 4F). Often the
young samaras retain the persistent anthers, which fall off during later development.
Pistil anatomy
Staminate type I flowers showed a short rudimentary pistil, with no distinction of ovary,
style and stigma, and the epidermal cells were not differentiated into papillae (Fig. 5A).
In staminate type II flowers too, the style and ovary were inconspicuous, ovules were
absent, but stigmatic papillae were feebly differentiated into finger-like projections (Fig.
5B). In hermaphrodite flowers, stigmatic papillae were well-developed (Fig. 5C), the
style was short and solid, and the ovary contained four anatropous, crassinucellate
ovules. The female gametophyte development is of Polygonum type and a 7-celled, 8nucleate embryo sac was seen in a cross section of ovule of hermaphrodite flower (Fig.
5D). Fertilization and embryo formation took place in hermaphrodite flowers only, as
an 8-celled proembryo was seen in longisection of ovule 35 days after fertilization (Fig.
5E). Staminate type I flowers abscised as soon as anthers dehisced (Yadav et al. 2016).
Pistil of staminate type II flowers also did not take part in fertilization events and fruit
set since the flowers abscised soon after dehiscence of anthers.
Discussion
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Anther morphology and basic anatomy are similar in anthers of all the three
flowering morphs. There are variable reports on anther anatomy in species of Acer. In
Acer saccharum (Jacobs & Lersten 1994), although anthers in pistillate flowers do not
dehisce, endothecial wall thickenings were found to develop in same basic pattern as in
staminate flowers, thereby indicating that this factor does not contribute to the failure of
dehiscence. However, in the case of hermaphrodite flowers of Acer oblongum (present
study) not all the cells of endothecium were seen to develop endothecial thickenings.
The fibrous thickenings were observed only in some cells and were found to be absent
from the cells near stomium. The epidermal cells near stomium were larger, often
irregular in shape and with thick cuticle as compared to staminate types. The formation
of endothecial thickenings was delayed and was only visible in Stage 3 and Stage 4 of
hermaphrodite flowers. Anthers of hermaphrodite flowers failed to dehisce and pollen
was thus never released. Pollen development was also delayed and the pollen achieved
maturity only after stigma receptivity ceased. Similar observations were made regarding
pollen development in Acer saccharum (Jacobs & Lersten 1994). In Acer platanoides,
short stamens in functionally female flowers produce pollen grains with thick walls
(Weryszko-Chmielewska & Sulborska 2011). However, in the case of staminate types
in Acer oblongum (present study) individual endothecial cells exhibited conspicuous
and prominent fibrous wall thickenings. The thickenings formed more-or-less radially
elongated parallel bands along the anticlinal cell walls. Also, the small cells of stomium
region apparently provide a weak area in the anther wall along which the dehiscence
occurs. Anther dehiscence is longitudinal in both the staminate types. In scanning
electron micrographs of anthers of hermaphrodite flower, it was observed that anther
wall splits longitudinally along the stomium region, though the opening was minimal
and pollen was not released. Similar observations were made regarding stomium cells
by Jacobs & Lersten (1994). In Acer saccharum, it has been reported that stomium
region and endothecium are similar in both staminate and morphologically
hermaphrodite (pistillate) flowers. Thus the failure of anthers in pistillate flowers to
open is not because of any apparent lack of the requisite anatomy (Jacobs & Lersten
1994, Vary et al. 2011). In the case of Acer mono it was shown that the failure of
dehiscence of anthers of female flower might be caused by degeneration of tapetum
tissue and loss of lip cells, i.e. formation sterility (Zhang et al. 2011).
Microsporogenesis and pollen development in Acer spp. (black maple) follows a
common pattern observed in other dicots (Laser & Lersten 1972, Johri 1984). Normal
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appearing pollen grains develop in anthers of hermaphrodite flowers, but were of
variable size and shape, often smaller than staminate types (Vary et al. 2011, Yadav et
al. 2016).
The presence of papillate stigma in Acer spp. is consistent with the presence of
similar papillate stigma in closely related groups (Peck & Lersten 1991). Works of
Buchenau (1861), and of Khushalani (1963) suggest that there may be some variation in
the degree of papillosity within and among the species (Peck & Lersten 1991).
Khushalani (1963) concluded that in flowers of A. oblongum there occur “… two types
of ovaries, one with stunted growth having papillate hairs on the stigma, and another
which is with normal growth, the latter being more common.” Also, she (Khushalani
1963) indicated that normal embryo sacs and fertilization occurred in both types.
However, the present study indicated that functional embryo sacs are formed only in
hermaphrodite flowers. Fertilization took place in this type only.
Anatomy of reproductive parts revealed the functionality of these being
rudimentary or fertile regarding its basic structure, dehiscence and receptivity. The
potential adaptive significance of vestigial reproductive organs in unisexual flowers is
not clearly understood (Vary et al. 2011). The prevalent adaptive hypothesis to explain
the presence of non-functional indehiscent anthers in pistillate flowers is that these may
attract or reward the pollinators (Bawa & Beach 1981, Schlessman et al. 1990, Mayer &
Charlesworth 1991, Ashman 2000, Vary et al. 2011). Similar observations have been
made in hermaphrodite flowers of A. oblongum since bees were seen visiting early
appearing staminate type I flowers with dehiscent anthers and functional pollen. The
presence of non-functional stamens present cues for bees to visit the morphologically
hermaphrodite flowers too for pollination. In Actidinia polygama (Actinidiaceae) and
Sterculia urens (Malvaceae), vestigial stamens removal in functionally female flowers
resulted in reduced seed set in both the species due to lower pollinator visitation
(Kawagoe & Suzuki 2004, Sunnichan et al. 2004).
Interestingly, in other Sapindalean genera, phylogenetically distant from Acer,
there are also reports suggesting that in perfect functionally pistillate flowers the anthers
are indehiscent (Cupania, Bawa 1977; Cardiospermum and Urvillea, Solis et al. 2010;
Melicoccus, Zini et al. 2012; Alophyllus, Gonzalez et al. 2014) or they dehisce in
limited percentage (Xanthoceras, Zhou & Liu 2012). The common pattern found is the
failure in septum programmed cell death, so that the anthers maintain their tetralocular
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form. Differences among species concern degree of endothecium development (i.e.
presence or absence of radial cellular elongation and the prominence of thickenings).
Conclusions
Our findings showed that though tapetum and endothecial thickenings were formed in
anthers of hermaphrodite flowers, but the anthers do not dehisce and pollen grains are
never released. Pollen of hermaphrodite flowers mature late (only after S3 stage)
compared to both staminate types in which pollen matures at bud stage, before anthesis
of the flower. A well-developed 8-nucleate embryo sac was seen only in ovules of
hermaphrodite flowers. Both the staminate type flowers lacked functional ovary and
thus do not contribute towards fruit set. Long papillate stigma was found only in
hermaphrodite flowers, but stigma is short with stigmatic papillae feebly differentiated
into finger-like projections in staminate type II and papillae are absent in staminate type
I flowers. The papillae development permits the increase in stigma surface area and
contributes to more efficient wind pollination. Therefore, looking at the mixed
characters of wind and insect pollination displayed by A. oblongum, it can be surmised
that the species is following a trend towards an evolution from insect to wind
pollination.
Acknowledgements
The research was supported by the Ministry of Environment, Forest and Climate
Change, New Delhi as part of “All India Coordinated Research Project on Reproductive
Biology of RET Tree Species” (No. 22/2/2010-RE), and by Research and Development
Grant from the University of Delhi. Thanks are also due to Shri S. K. Dass for helping
in preparation of the photographic plates. We acknowledge the critical comments
offered by Subject Editor for improvement of the manuscript.
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207: 712-720.
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FIGURE LEGENDS
Figure 1: Flowering morphs of Acer oblongum. (A) Staminate type I with rudimentary
pistil. (B) Staminate type II with abortive pistil. (C) Hermaphrodite flower with bifid
papillate stigma and indehiscent anthers.
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Figure 2: Anther anatomy. Staminate type I (A) Transverse section of bithecous anther
showing degenerating Secretory tapetum and middle layers (Scale bar = 100µm); (B)
partially dehisced anther, two sporangia on either side of anther lobe become joined due
to breakdown of partition wall (Scale bar = 100µm); (C) completely dehisced anther
(Scale bar = 100µm); (D) portion of anther (stained with safranine) towards stomium
showing well-developed endothecial thickenings (arrow) in each cell (Scale bar = 50
µm). Note distinct cuticle layer above epidermis (arrowhead); (E) SEM of partially
dehisced anther showing opening of anther towards longitudinal line of dehiscence
(Scale bar = 100µm); (F) SEM of hydrated pollen grain (Bar = 5µm); (G) SEM of dry
(unhydrated) pollen grain with striate exine sculpturing (Bar = 10µm).
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Figure 3: Anther anatomy. Staminate type II (A) Transverse section of bithecous anther
(2DBA bud stage) showing disintegration of middle layers and degenerating tapetum
(Scale bar = 100 µm); (B) Transverse section of partially dehisced anther showing
separation of cells towards stomium (Scale bar = 100 µm); (C) on DOA completely
dehisced anther (Scale bar = 100 µm); (D) SEM of a completely dehisced anther
showing empty anther lobe (Scale bar = 100 µm); (E) Portion of transverse section of
anther near stomium showing endothecium cells with fibrous endothecial thickenings
(Scale bar = 50 µm). Arrow indicates the endothecial thickening in the cells near
stomium; (F) Portion of anther showing opening of stomium valves at time of
dehiscence (Scale bar = 50 µm).
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Figure 4: Anther anatomy of hermaphrodite flower at different stages of development
S1, S3, S4 (A) Transverse section of anther at Stage 1 with irregular epidermal cells and
tapetum and middle layers not differentiated completely (Scale bar = 100 µm); (B)
Transverse section of anther at Stage 3 with degenerating tapetum and middle layers;
mature appearing pollen grains in anther locule and endothecial thickenings in few cells
of endothecium (Scale bar = 100 µm) (C) Transverse section of anther at Stage 4,
shriveled anther lobes with degenerating pollen grains and irregular fibrous thickenings
in few endothecial cells (Scale bar = 100 µm). Note minimal opening of anther walls
towards line of dehiscence (arrow); (D) SEM of anther of hermaphrodite flower with
minimal separation of anther walls (arrowhead) seen along line of dehiscence (Scale bar
= 200 µm); (E) Part of section of anther showing absence of endothecial thickenings
from cells near stomium (Scale bar = 50 µm) (arrow); (F) SEM of anther showing
shriveled anther lobes with no sign of dehiscence yet (Scale bar = 200 µm).
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Figure 5: Pistil anatomy of three flowering morphs (A) A portion of longitudinal
section of Staminate type I flower showing rudimentary pistil (arrowhead) with lack of
stigmatic papillae (Scale bar = 500 µm); (B, C) Transverse section of stigma of
Staminate type II and Hermaphrodite flower showing collapsed (arrowhead) and welldeveloped stigmatic papillae (arrowhead) respectively (Scale bar = 100 µm); (D)
Longitudinal section of ovule of hermaphrodite flower showing 8-nucleate embryo sac
(Scale bar = 50 µm); (E) Longitudinal section of ovule of hermaphrodite flower 35 days
after fertilization showing 8-celled proembryo (arrow) (Scale bar = 50 µm).
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