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Anther and gynoecium structure and development of male and female gametophytes of Koelreuteria elegans subsp. formosana (Sapindaceae): Phylogenetic implications
Abstract
Anther and gynoecium structure and embryological information in Koelreuteria and Sapindaceae as a whole remain understudied, as well as the evolution of imperfect flowers in the latter. The aims of this study were to analys in K. elegans subsp. formosana the anther and gynoecium structure and the development of male and female gametophytes in the two floral morphs of putatively imperfect flowers. Standard techniques were applied for LM and SEM. Compared to the normal anther development in staminate flowers, a delayed programmed cell death of tapetum, septum and middle layers on the onset of microspore stage result in indehiscent anthers in the functionally pistillate flowers. Orbicules are reported for the first time in Sapindaceae. Gynoecium development in functionally pistillate flowers is normal, whereas in functionally staminate ones a pistillode with degenerated ovules at the tetrad stage is formed. The pollen tube transmitting tract consists of one layer of epithelial cells with a small lumen in the style and ovary. The anatomy of the latter revealed an axile placentation and complete septum. Reproductive characters of Koelreuteria shared with other Sapindaceae taxa are a secretory binucleate tapetum, simultaneous cytokinesis, unicellular stigmatic papillae, Polygonum type megagametophyte with ephemeral antipodals, and ovules campylotropous, with funicular obturator and amphistomic micropyle. Imperfect flowers in the family are triggered by defective sporophytic tissues impacting on the normal development of microspores and megaspores, disrupting embryological events in staminate and pistillate organs at different developmental stages. Reconstructing ancestral character state under parsimony revealed that two ovules per locule, absence of obturator, presence of hypostase, and binucleate tapetum may be regarded as plesiomorphic for Sapindaceae. These analyses have provided information on the evolution of embryological characters in the family and its phylogenetic significance.
... More recently an increasing amount of detailed studies focusing on the comparative morphology, anatomy, histology and ontogeny of flowers of several sapindalean taxa has been carried out (Table 1; e.g., Alves et al. 2017;Avalos et al. 2019;Endress 2008, 2009;Bachelier et al. 2011;Cao et al. 2017Cao et al. , 2018El Ottra et al. 2013, 2019Pirani et al. 2010;Ramp 1988;Tölke and Demarco 2020;Wei et al. 2011Wei et al. , 2015. Most of these studies pay special attention to detailed aspects of gynoecium structure. ...
... elegans subsp. formosana (Hayata) F.G. Mey: Avalos et al. 2019) or appear to have (K. paniculata Laxm., K. bipinnata Franch.: Cao et al. 2018;Ronse De Craene et al. 2000) an upper apocarpous zone restricted to part of the stigmatic region that is postgenitally fused. ...
... In K. paniculata, the incomplete fusion of the inner part of each carpel flank makes the epidermis of adjacent carpels partially discernable as so-called "septal cavities". These corresponds functionally to PTTT, as also observed in K. elegans (Avalos et al. 2019;Ronse De Craene et al. 2000). Also, similar to Averrhoidium, an outer median dorsal furrow is present in the style and along each of the three carpels making up the ovary, which also correspond to dehiscence lines developing early in each locule. ...
Sapindales is a monophyletic order within the malvid clade of rosids. It represents an interesting group to address questions on floral structure and evolution due to a wide variation in reproductive traits. This review covers a detailed overview of gynoecium features, as well as a new structural study based on Trichilia pallens (Meliaceae), to provide characters to support systematic relationships and to recognize patterns of variations in gynoecium features in Sapindales. Several unique and shared characteristics are identified. Anacrostylous and basistylous carpels may have evolved multiple times in Sapindales, while ventrally bulging carpels are found in pseudomonomerous Anacardiaceae. Different from previous studies, similar gynoecium features, including degree of syncarpy, ontogenetic patterns, and PTTT structure, favors a closer phylogenetic proximity between Rutaceae and Simaroubaceae, or Rutaceae and Meliaceae. An apomorphic tendency for the order is that the floral apex is integrated in the syncarpous or apocarpous gynoecium, but with different length and shape among families. Nitrariaceae shares similar stigmatic features and PTTT structure with many Sapindaceae. As the current position of both families in Sapindales is uncertain, floral features should be investigated more extensively in future studies. Two different types of gynophore were identified in the order: either derived from intercalary growth below the gynoecium as a floral internode, or by extension of the base of the ovary locules as part of the gySapindales is a monophyletic order within the malvid clade of rosids. It represents an interesting group to address questions on floral structure and evolution due to a wide variation in reproductive traits. This review covers a detailed overview of gynoecium features, as well as a new structural study based on Trichilia pallens (Meliaceae), to provide characters to support systematic relationships and to recognize patterns of variations in gynoecium features in Sapindales. Several unique and shared characteristics are identified. Anacrostylous and basistylous carpels may have evolved multiple times in Sapindales, while ventrally bulging carpels are found in pseudomonomerous Anacardiaceae. Different from previous studies, similar gynoecium features, including degree of syncarpy, ontogenetic patterns, and PTTT structure, favors a closer phylogenetic proximity between Rutaceae and Simaroubaceae, or Rutaceae and Meliaceae. An apomorphic tendency for the order is that the floral apex is integrated in the syncarpous or apocarpous gynoecium, but with different length and shape among families. Nitrariaceae shares similar stigmatic features and PTTT structure with many Sapindaceae. As the current position of both families in Sapindales is uncertain, floral features should be investigated more extensively in future studies. Two different types of gynophore were identified in the order: either derived from intercalary growth below the gynoecium as a floral internode, or by extension of the base of the ovary locules as part of the gynoecium. Sapindales share a combination of gynoecial characters but variation is mostly caused by different degrees of development of the synascidiate part relative to the symplicate part of carpels, or the latter part is absent. Postgenital fusion of the upper part of the styles leads to a common stigma, while stylar lobes may be separate. Due to a wide variation in these features, a new terminology regarding fusion is proposed to describe the gynoecium of the order.noecium. Sapindales share a combination of gynoecial characters but variation is mostly caused by different degrees of development of the synascidiate part relative to the symplicate part of carpels, or the latter part is absent. Postgenital fusion of the upper part of the styles leads to a common stigma, while stylar lobes may be separate. Due to a wide variation in these features, a new terminology regarding fusion is proposed to describe the gynoecium of the order.
... More recently an increasing amount of detailed studies focusing on the comparative morphology, anatomy, histology and ontogeny of flowers of several sapindalean taxa has been carried out (Table 1; e.g., Alves et al. 2017;Avalos et al. 2019;Endress 2008, 2009;Bachelier et al. 2011;Cao et al. 2017Cao et al. , 2018El Ottra et al. 2013, 2019Pirani et al. 2010;Ramp 1988;Tölke and Demarco 2020;Wei et al. 2011Wei et al. , 2015. Most of these studies pay special attention to detailed aspects of gynoecium structure. ...
... elegans subsp. formosana (Hayata) F.G. Mey: Avalos et al. 2019) or appear to have (K. paniculata Laxm., K. bipinnata Franch.: Cao et al. 2018;Ronse De Craene et al. 2000) an upper apocarpous zone restricted to part of the stigmatic region that is postgenitally fused. ...
... In K. paniculata, the incomplete fusion of the inner part of each carpel flank makes the epidermis of adjacent carpels partially discernable as so-called "septal cavities". These corresponds functionally to PTTT, as also observed in K. elegans (Avalos et al. 2019;Ronse De Craene et al. 2000). Also, similar to Averrhoidium, an outer median dorsal furrow is present in the style and along each of the three carpels making up the ovary, which also correspond to dehiscence lines developing early in each locule. ...
... However, the phylogenetic relationships of some clades, including Paullinieae, remain unclear and, therefore, data from reproductive anatomy and embryology would provide Avalos et al. 2019). For the family as a whole, few embryological studies are available and these will be addressed in the discussion. ...
... According to the classification proposed by Davis (1966), the ontogeny of the anther recognizes three types. Embryological studies carried out for the family show the presence of the basic and the dicotyledonous types, although the latter is less frequent (Nair and Joseph 1960;Gulati and Mathur 1977;Mathur and Gulati 1980, 1989Cao et al. 2008;Solís et al. 2010;Zini et al. 2012;Zhou and Liu 2012;González et al. 2014González et al. , 2017Avalos et al. 2019). The basic type, found in S. meridionalis as well as in other species of Paullinieae, such as Serjania incana Radlk. ...
... (Solís 2011), could be interpreted as a reversion to a previous development stage. In staminate flowers of the two species studied here, the maturation of the anther wall, as well as the development of microsporogenesis, microgametogenesis and pollen grain release, follow the general pattern of development observed in most Angiosperms and coincide with previous studies carried out in other genera of different tribes of Sapindaceae (Nair and Joseph 1960;Mathur and Gulati 1981;Ha et al. 1988;Cao et al. 2008;Solís et al. 2010;Zini et al. 2012;González et al. 2014González et al. , 2017Avalos et al. 2019). ...
The tribe Paullinieae is distinguished by a monoecious reproductive system; it exhibits two floral morphs, namely staminate flowers, with gynoecium reduced to a pistillode, and morphologically hermaphrodite but functionally pistillate flowers. The aim of this study was to analyze the development of sporogenesis and gametogenesis in flowers of Thinouia mucronata Radlk. (subtribe Thinouiinae) and Serjania meridionalis Cambess. (subtribe Paulliniinae) and to elucidate the moment when pollen grains of pistillate flowers and the ovule of staminate ones stopped their development. Light and scanning electron microscopy was applied using standard techniques. In T. mucronata flowers are actinomorphic; the pistillate ones have anatropous, pseudocrassinucellate ovules, without hypostase and with placental obturator, and stamens with indehiscent anthers and well-developed pollen grains that remain inside the pollen sac at the end of anthesis. Serjania meridionalis has zygomorphic flowers, the pistillate ones have campylotropous, crassinucellate ovules, with presence of hypostase, and funicular obturator, and stamens with indehiscent anthers collapsed at the end of anthesis, showing remnants of aborted sporogenous tissue in each pollen sac. Both species share the anatomy of the anther wall; microsporocytes form tetrahedral or decussate tetrads; monads are bicellular; the pistillode has abortive megaspore; gynoecium with bithegmic ovules and Polygonum-type megagametophyte. One difference in antheral wall ontogeny between species was that T. mucronata displayed the dicotyledoneus type development, whereas S. meridionalis exhibited the basic type. These embryological characters clearly support the basal position of Thinouia in the tribe recently validated from molecular phylogeny studies and supported by the present morphological data.
... The studies performed in Anacardiaceae, Burseraceae and Kirkiaceae Endress 2008, 2009), Nitrariaceae (Bachelier et al. 2011), Rutaceae (Pirani et al. 2010;El Ottra et al. 2019), Sapindaceae (Bawa 1975;Yadav et al. 2016;Avalos et al. 2019), Simaroubaceae (Ramp 1988;Alves et al. 2017) and Meliaceae (Styles 1972;Pennington and Styles 1975;Gouvea et al. 2008a;Gama et al. 2021) indicate the occurrence of sexual dimorphism and various sexual systems and discuss the implications of floral structure and plant sexuality for the systematics and evolution of the order. ...
... Subtle sexual floral variations related to organ abortion are also known in several other members of Sapindales. For example, structurally bisexual but functionally unisexual flowers occur in Kirkia (formerly Simaroubaceae), in representatives of Anacardiaceae and Burseraceae (Bachelier and Endress 2009), Sapindaceae (e.g., Avalos et al. 2019), and were recently reported for Homalolepis (as Simaba) by Alves et al. (2017), a genus with species that were so far been described as hermaphrodites. The difficulty in adequately interpreting functional floral sexuality in Sapindales is a reflection of the subtle sexual dimorphism related to morphological differences between floral sexes and the fact that most genera of the order still need to be carefully studied. ...
Flowers of Meliaceae are traditionally described as bisexual, but functionally unisexual flowers have been reported for many genera. For Trichilia, several reproductive systems have been previously reported: subdioecy, gynodioecy, polygamy and hermaphroditism. The aim of this study was to analyze the occurrence of floral dimorphism and sexual-functional aspects of the flower of Trichilia claussenii. Structural and developmental analyses of flowers of Trichilia claussenii were performed using light and electron microscopy. In addition, male and female function of flowers was investigated through pollen viability and stigma receptivity tests, hand pollination and seed germination. Two floral morphotypes were identified in Trichilia claussenii: one morphologically male with a reduced gynoecium and the other morphologically female with anthers which do not release pollen. In the supposedly male flower, anthers are well developed and produce viable pollen grains. A conspicuous nectary disk differentiates at the base of the gynoecium, and the ovary has small ovules; however, our study proved that this ovary develops into a fruit, which contains viable seeds. In contrast, the supposedly female flower has larger gynoecium and ovules, and the nectary is smaller and inconspicuous. The stamens of female flowers have inviable pollen grains due to a tapetal necrotic product that keeps them united into an amorphous mass within the anthers. Male flowers are geitonogamous. Our results demonstrate that Trichilia claussenii exhibits subtle sexual floral dimorphism with female flowers and bisexual flowers distributed in different individuals. Our results indicate that male sterility occurs in only one morphotype; therefore, the species is gynodioecious.
... The formation of an abnormal cytoplasm or irregular sporangia is associated with the duration of the development of tapetal and middle layer cells (Zini et al., 2012). In Koelreuteria elegans, the occurrence of programmed deaths of tapetal, septal, and intermediate cells during the initiation of microsporogenesis can cause failure in anther dehiscence (Avalosa et al., 2019). In the Magnoliaceae species Manglietia aromata (Pan et al., 2003) and Manglietia decidua (Xiao and Xu, 2006), the loss of most synergids during sac development can lead to a high oocyte abortion rate. ...
Camellia weiningensis is a typical woody edible oil tree species in the northwest alpine area of Guizhou Province, China, but its embryological development is not fully elucidated. Here, we assessed flower bud differentiation, microsporogenesis, and male-female gametophyte development in this species. We performed cytological observations of flower bud development in C. weiningensis through conventional paraffin sectioning, scanning electron microscopy, and stereomicroscopy to establish the corresponding relationships between the external morphology and internal structure. The flowers were hermaphroditic and exhibited a short flower bud differentiation time. Although pistil development occurred later than stamen development, both organs matured synchronously before flowering. The anther contained four sacs that exhibited a butterfly shape in transverse sections. The anther wall comprised the epidermis, anther chamber inner wall, two middle layers, and a glandular tapetum (from outside to inside). Microspore mother cells formed a tetrahedral tetrad through meiosis, mature pollen was two-celled with three germination pores, and the ovary comprised three to five chambers (three chambers predominated). Multiple ovules were invertedly attached to the axial placentation and exhibited double integuments and a thin nucellus. The embryo sac exhibited Allium -type development, and the mature embryo sac was seven-celled and eight-nucleated. In C. weiningensis , embryonic development does not exhibit abnormalities, and stamen development occurs earlier than pistil development. During flower bud development, the inner development process of male and female cells can be judged according to their external morphological characteristics. Our results may provide a theoretical basis for regulating flowering in and the cross-breeding of C. weiningensis .
... formosana, Magonia pubescens and Handeliodendron bodinieri (H.Lév.) Rehder, disruption of ovule development and degeneration of the nucellus and integuments were observed (Avalos et al. 2019b;Cao et al. 2008;González et al. 2017). In Xanthoceras sorbifolium, ovule abortion occurs even before integument formation (Zhou and Liu 2012). ...
Most species of Sapindaceae are described as monoecious, sharing the presence of staminate flowers and flowers that
are morphologically perfect but functionally pistillate. Duodichogamy has also been recorded in the family, but with few
evaluations of the structures of different flower types or the functionality of reproductive structures in the different genera
analyzed. Cupania L. is a monophyletic genus that occurs in tropical and subtropical America, consisting of monoecious
duodichogamous trees with functionally unisexual, actinomorphic, and nectariferous flowers. Cupania emarginata Cambess.
is endemic to Brazil, occurring in the northeast and southeast regions, mainly on sandy coastal plains (restingas). This study
described and analyzed the flowers of this species based on morphometry and anatomy, and evaluated the functionality of
the reproductive whorls and nectaries in the different floral types. Staminate flowers from the first and third flowering phases
differ morpho-structurally; the gynoecium (pistillode) in first-flowering staminate flowers is markedly more collapsed than
the gynoecium of third-flowering staminate flowers, in which the ovules may differentiate and contain embryo sacs with
hypertrophied cells; mature anthers of pistillate flowers contain pollen grains at the stage of two-celled microgametophytes,
similar to those of mature anthers of staminate flowers; and anthers of pistillate flowers are indehiscent, probably due to
ineffective dehydration, as suggested by the persistence of the septum, which remains intact. The floral nectary is functional
in all three flowering phases.
Keywords Androecium · Gynoecium · Morphometry
... This is supported by recent findings of scattered flowers bearing abortive ovules in some species of these two genera (Franceschinelli and Thomas 2000;Alves et al. 2017;Devecchi et al. 2018a, b). Flowers that are morphologically perfect but functionally unisexual are reported also to some extra-American simaroubaceous genera, as well as in many other groups of Sapindales [e.g., Meliaceae (Styles 1972;Franceschinelli et al. 2015), Anacardiaceae and Burseraceae (Bachelier and Endress 2009), Sapindaceae (Avalos et al. 2019) and Rutaceae (Kubitzki et al. 2011)]. Evolutionary paths of sexual structures and systems in Simaroubaceae and related families are discussed in Alves et al. (2021-this issue) and in Gama et al. (2021). ...
Simaroubaceae are among the families whose circumscription radically changed over time, because phylogenetic analyses undertaken since 1995 demonstrated it was a polyphyletic group in its traditional delimitation. Currently, Simaroubaceae sensu stricto are a mostly pantropical, highly supported monophyletic group composed of 22 genera and approximately 120 species. Growing knowledge about members of the family has allowed several advances over the last couple of decades. The primary center of diversity for Simaroubaceae is in tropical America, and new contributions have been recently made regarding members of the family in the region, including descriptions of several new taxa. Hence, we undertook an updated overview of general information available for the group, with focus on American taxa of Simaroubaceae, and highlighting numerous data published after the 2011 monograph. Besides aiming to contribute to a better knowledge of a family with past controversial limits, we emphasize research topics in which the current scarcity of data demands further investigation.
... The turbin structure can emerge from the development of the ovaries. The development of fruit by cell division during the crucial phase, that is, before and after flower anthesis, especially from the flowers organ that is the tissue development in the pistil (Avalos et al. 2019;Yang et al. 2019). The turbine structure resembles a bulge found at the fruit apical and it is thought that it was originated from the stigma remnants after pollination process and still drags during plant growth (Figures 1 and 2). ...
Maryanto SD, Wibowo WA, Daryono BS. 2021. Phenotypic characters and identification CYPs (Cyclophilin) gene in Cucumis melo L. cv. Gama Melon Parfum. Biodiversitas 22: 3007-3014. Cucumis melo L. cv. Gama Melon Parfum is a new cultivar with a very strong fragrance as its main character. As a new cultivar with unique characters, it is necessary to characterize phenotype and molecular related to the fragrant aroma. The research aimed to study the phenotypic of the fruit of C. melo cv. Gama Melon Parfum (F3) and to identify the CYPs gene as one of the genes that act in encoding volatile compounds. Analysis of qualitative characters was based on International Plant Genetic Resources Institute (IPGRI) and Plant Variety Protection (PVP), phenotypic characters in melons observed by abiding the Rules for Registration of Varieties from the Indonesian Minister of Agriculture Decree No. 700/Kpts/OT.320/D/12/2011, while analysis of quantitative characters was using the ANOVA methods and software PKBT-STAT-2. The methods of molecular characterization included RNA isolation, cDNA synthesis used Reverse Transcriptase-PCR, amplification of DNA target used PCR, visualization of DNA target used electrophoresis, and DNA sequencing. Analysis of the in silico approach was carried out on the CuGenDB Melon database. Analysis of protein sequences and classification was obtained from InterPro. Phylogeny analysis using MEGA-X Software. The results were 18 qualitative characters and 11 quantitative characters were stable and uniform, whereas the molecular characterization of the genes was predicted Cyclophilin with peptidylprolyl isomerase (PPIase) activity and located in chromosome 1 (17059021-17058899).
... Monoecious plant species have separate male and female flowers on the same plants and can therefore undergo self-fertilization when the pollen of staminate flowers contacts the stigma of pistillate flowers, barring other defenses against selfing (Mao et al., 2017;Avalos et al., 2019;Hildesheim et al., 2019). Heterodichogamy, which is dispersed and reported in 20 genera from 13 families of flowering plants, is one of the evolutionary pathways from monoecy to dioecy, heterodichogamous populations usually contain two sexual morphs, protogynous and protandrous, which are reciprocal (Meng et al., 2009;Liu et al., 2016). ...
Juglans mandshurica is a monoecious heterodichogamous species with protogynous and protandrous mating strategies that occur at a 1:1 ratio and are randomly distributed in the population. The inconsistent male and female flowering periods of the same mating type result in an imbalance of the ratio of male and female flowers, contributing to the low yield of this species. However, little more is known about its floral development. Following three consecutive years of observations, histological analysis, and scanning electron microscopy, we found that the morphological and anatomical development of the male and female flowers were synchronous. The male floral morphological development of J. mandshurica was divided into seven phases, while that of the female flower was nine. Four stages were shared between the male and female flower’s anatomical development. Our findings indicate that there was minimal overlap between sexual functions within the same mating type, guaranteeing synchronization, mutual non-interference, outcrossing, and avoidance of self-fertilization. These results provide a theoretical basis for the improvement of fruit yield and quality through the reasonable allocation of protogynous and protandrous individuals in a population, and for artificial pollination control. Further, these findings lay a foundation for further research on the genetic mechanisms and environmental effects on flower development of heterodichogamous J. mandshurica.
... In Sapindaceae and Meliaceae, for instance, although some species apparently have male and bisexual flowers, anthers of the bisexual morphotype are empty or have unfertile pollen grains. Sometimes the anthers may not even release pollen grains, remaining indehiscent (Gouvêa et al., 2008;Solís et al., 2010;Rosado et al., 2018;Avalos et al., 2019;Zhou et al., 2019). ...
The genus Spondias has a wide variety of sexual systems, with complete monoecious to polygamodioecious species. Spondias macrocarpa (Anacardiaceae) is an endemic species from Brazil, previously described as her-maphroditic, and considered vulnerable due to massive deforestation. However, to our knowledge, no further details on the breeding system or morphological studies are available. Herewith we examine the floral mor-pho-anatomy and breeding system of this species to better understand the sexual function of different floral morphologies and the role of pollinators in its reproduction. We used light and scanning electron microscopy to study the morphology and anatomy of the flowers. Additionally, we carried out experiments on pollen viability, stigmatic receptivity, and controlled pollinations. We found both bisexual and male flowers in the same inflo-rescence, with the staminate flowers presenting cryptic unisexuality. Investment in bisexual flowers was higher than in male ones, although more than 70% of the inflorescence was made up of male flowers. Most male flowers are present in the proximal region of the inflorescence, and there is no temporal separation between male and female functions in bisexual flowers. We show that S. macrocarpa is andromonoecious with cryptic-monoecy and a self-incompatibility system. Under natural conditions, S. macrocarpa is probably a pollinator generalist, with small bees being its main floral visitors. High levels of pollen robbing and low levels of crossing by floral visitors may result in the observed low fruit set. Further studies on the pre-and post-pollination barriers and on the reproductive ecology of extant natural populations should elucidate the reason for such a low fruit set.
Lespedeza davurica (Laxm.) is a leguminous plant with significant ecological benefits, but its embryonic development mechanism remains unclear. We investigated the flower bud differentiation, megaspore and microspore formation, gametophyte development, and embryo and endosperm development in L. davurica. Our aim was to elucidate the relationship between the external morphology and internal development processes of male and female floral organs during growth, as well as the reproductive factors influencing fruiting. The results indicated that although the pistil develops later than the stamen during flower bud differentiation, both organs mature synchronously before flowering. L. davurica pollen exhibits three germination grooves, a reticulate outer wall, and papillary structures on the anther surface. In vivo pollination experiments revealed abnormal spiral growth of L. davurica pollen tubes within the style and the occurrence of callus plugs, which may reduce the seed setting rate. The anther wall development follows the dicotyledonous type, with tetrads formed through microspore meiosis exhibiting both left–right symmetry and tetrahedral arrangements. L. davurica has a single ovule, and the embryo sac develops in the monosporic polygonum type. After dormancy, the zygote undergoes multiple divisions, progressing through spherical, heart-shaped, and torpedo-shaped embryo stages, culminating in a mature embryo. A mature seed comprises cotyledons, hypocotyl, embryo, radicle, and seed coat. Phylogenetic tree analysis reveals a close genetic relationship between L. davurica and other leguminous plants from the genera Lespedeza and Medicago. This study provides valuable insights into the regulation of flowering and hybrid breeding in leguminous plants and offers a new perspective on the development of floral organs and seed setting rates.
Floral features contribute with remarkable additions to morphological studies and are widely used to address questions about the evolution and diversification of several groups of plants. Even though Simaroubaceae are a small monophyletic family, the few detailed structural analyses of reproductive organs and the floral diversity and variations already described in their members stimulate novel structural studies. In this study, we investigate the evolution of reproductive features of Simaroubaceae by means of a combination of original data and a review of the literature, aiming to elucidate which floral characters are most informative for a better understanding of the evolutionary history of the group. We analyzed 21 out of the 23 genera of Simaroubaceae, plus six from Rutaceae and seven from Meliaceae as outgroups. We used a Bayesian method and the Parsimony optimality criterion to reconstruct ancestral reproductive character states using a re-analyzed phylogenetic tree of Sapindales. Here, we combined available molecular sequences to have the largest sample of Simaroubaceae genera. We found that the ancestral flowers of Simaroubaceae were probably polygamous or dioecious plants, with free carpels united only distally, with divergent, elongated stigmas, and with drupaceous, laterally flattened to lenticular fruits. The latter feature plus apocarpous carpels are putative synapomorphies of the family retrieved in this study. Imbricate petals and a diplostemonous androecium were recovered as conditions found in the ancestor of Simaroubaceae but also shared with the ancestors of Meliaceae and Rutaceae. Our findings were mostly in accordance with previous evolutionary studies on genera of Simaroubaceae and with other families of Sapindales. © 2021, The Author(s), under exclusive licence to Botanical Society of Sao Paulo.
COLE TCH, FERRUCCI MS (2023) SAPINDACEAE Phylogeny Poster (SapPP) © COLE, FERRUCCI 2023 (CC-BY) • subfamilies, tribes, and genera with selected features • main tree of genera chiefly based on Buerki et al. 2021 • topology of Sapindales tree based on Joyce et al. 2023 • family of ca. 144 genera (of these 134 listed here) • phylogeny, classification, and features assembled from the References cited here • branch lengths deliberate, not expressing actual time scale • the characters listed do not necessarily apply to all members a clade • for characteristics (family and genera) see: Kubitzki K (ed) (2011) FGVP, Vol. X and APweb
The floral organogenesis and anatomy of Koelreuteria bipinnata and its variety K. bipinnata var. integrifolia (Sapindaceae) has been investigated to clarify the identity of the two taxa in relation to other species of Koelreuteria, and to understand the shift to monosymmetry in the genus. Although the floral development is highly similar, we found a number of striking differences. Flowers arise in thyrses, with lateral branches forming cincinni of 5–9 flowers. Sepals initiate in a spiral sequence. Five petals arise unidirectionally alternating to the sepals. The last formed petal and one stamen between sepals 3 and 5 are strongly delayed, appearing as a common primordium, while this petal is completely suppressed in var. integrifoliola. Eight stamens initiate sequentially, differ in size and partly precede the development of petals. The gynoecium develops as a triangular primordium on which three carpellary lobes become demarcated simultaneously. Placentation is axile. Septal slits occurring within the style are interpreted as a deep-reaching non-nectariferous extension of the stigma. The massive, oblique disk with crenate apex develops in an extrastaminal position, but is interrupted on the radius of the lost petal. Floral developmental evidence supports variety K. bipinnata var. integrifolia rather than being synonym of K. bipinnata. Floral development is compared with K. paniculata and is discussed in the context of floral evolution of Sapindaceae. Our study demonstrates the importance of developmental shifts on floral evolution. The triangular gynoecium has a strong spatial impact in obliquely reorganizing the symmetry of the flower. It is demonstrated that spatial constraints of calyx and ovary are responsible for the reduction in one of the petals, two stamens and a shift in symmetry of the flower.
Magonia pubescens A.St.-Hil. (Dodonaeaeae, Sapindaceae) is a monoecious species exhibiting two floral morphs, namely staminate flowers, with gynoecium reduced to a pistillode, and morphologically hermaphrodite but functionally pistillate flowers. It presents the basic type of antheral wall development. Microsporogenesis is normal, forming tetrahedral and decussate tetrads. Anatomical differences in anthers between floral morphs become visible at the stage of callose wall degradation and release of tetrads. In staminate flowers, the endothecium develops fibrous thickening, and the two middle layers, the tapetum and the parenchymal septum that separates both locule, are degraded. At dehiscence, permanent calymmate tetrads are released. Magonia is the only genus of the family with this type of pollen unit. In pistillate flowers, the endothecium exhibits fibrous thickening only in three to five cells on the dorsal loculus, and only the inner middle layer collapses. The septum that separates both locules remains unaltered, the stomium is non-functional, mature anthers are indehiscent and show collapsed tetrads. In staminate flowers, the gynoecium is reduced to a tricarpellar pistillode, trilocular, with ovules that degenerate after megasporogenesis. In pistillate flowers, the gynoecium has a tricarpellary ovary, with six to eight ovules per carpel; they are campylotropous, bitegmic, mixed crassinucellate, and exhibit a well-developed obturator. The phylogenetic implications of these embryological characters are discussed in the context of the family.
Se estudió la esporogénesis y gametogénesis de flores estaminadas y pistiladas de Allophylus edulis (Sapindaceae). La anteras jóvenes son similares en ambos tipos de flores, comparten el tipo básico de desarrollo anteral; presentan epidermis, endotecio con células binucleadas, dos capas medias, y tapete de tipo secretor, con células binucleadas. La microsporogénesis es normal, la división de las células madres de las micrósporas es simultánea y las tétrades son tetraédricas y decusadas. La antera madura en flores estaminadas presenta células epidérmicas adelgazadas a nivel del estomio y el endotecio con engrosamientos fibrosos. Se aprecia un único lóculo por teca por disolución del septo y los granos de polen son liberados al estado 2-celular, éstos son triporados o tetraporados. El gineceo está reducido a un pistilodio tricarpelar, trilocular, con un óvulo por lóculo. El óvulo degenera antes de que ocurra la meiosis. La antera madura de las flores pistiladas difiere anatómicamente de la de las flores estaminadas. El endotecio no desarrolla engrosamientos fibrosos, las capas medias y el tapete persisten, y el estomio no es funcional; las anteras son indehiscentes. El gineceo de las flores pistiladas, presentan ovario tricarpelar y trilocular. Cada lóculo contiene un óvulo hemianátropo, bitegumentado y crasinucelado, con obturador desarrollado; el megagametófito es de tipo Polygonum. Se discuten los resultados obtenidos en relación a lo conocido para la familia.
The structure and ultrastructure of the floral nectary of staminate and pistillate flowers of Koelreuteria elegans subsp. formosana (Sapindaceae, Koelreuterieae) were studied. In both floral morphs, the floral nectary is extrastaminal, receptacular, thimble-shaped and persistent. The anatomical analysis revealed a differentiated secretory parenchyma and a less developed, inner non-secretory parenchyma. These anatomical features reveal that the nectary is structured, and is supplied by phloem traces derived from the central stele. In the middle of the floral nectary there are few modified stomata. The nectarostomata were of anomocytic type; they may occur at the level of or sunken below the adjacent epidermal cells. Statistically significant differences were observed between both floral morphs in relation to nectar volume and the different moments of day, whereas the sugar concentration showed no significant differences. Ultrastructural studies showed no difference between staminate and pistillate flowers. At anthesis, amyloplasts and lipid globules were observed in the secretory parenchyma cells, whereas at post-anthesis the secretory parenchyma cells were degenerated. Floral nectar is secreted through nectarostomata and the outer epidermal cell walls. These results are discussed in relation to other species belonging to different tribes within Sapindaceae.
Phylogenetic relationships within Sapindaceae sensu lato are assessed using sequence data from two plastid genes, analyzed separately and together. A total of 46 rbcL sequences (31 of which are new), and 89 matK sequences (75 new) representing 64 genera were subjected to parsimony and Bayesian analysis. The results support three major lineages, relationships between which are only weakly supported. Xanthoceras sorbifolium is not clearly a member of any of these lineages, and there is some support for it being the first lineage to diverge within the entire assemblage. Support for a broadly defined Sapindaceae incorporating Aceraceae, Hippocastanaceae, and Xanthoceras is very robust. A division into four subfamilies is proposed: Sapindoideae (including Koelreuteria and Ungnadia); Hippocastanoideae (including taxa previously referred to Aceraceae and Hippocastanaceae, plus Handeliodendron); a more narrowly defined Dodonaeoideae; and a monotypic Xanthoceroideae. Tribal groupings are critically evaluated in light of the analyses. Although many of the current tribes appear paraphyletic or polyphyletic, there is support for the monophyly of some core groups of genera that suggest realignments of tribal concepts that would render them more informative of relationships.
Anther development, microsporogenesis and microgametogenesis of six species of the genera Corchorus, Heliocarpus, Luehea and Triumfetta were analysed. The genera were found to share the following characters: ontogeny of anther wall of basic type; simultaneous microsporogenesis, resulting mainly in tetrahedral tetrads; secretory tapetum and pollen grains shed at the bicellular stage. Moreover, the characters that differentiate them are: presence of uninucleate tapetal cells in Heliocarpus and Triumfetta; binucleate cells in Corchorus and multinucleate cells in Luehea; differentiation of the thickenings of the endothecium at free microspores stage in Corchorus, Heliocarpus and Triumfetta, whereas in Luehea differentiation occurs at the mature pollen grains stage; late disintegration of sporogenous tissue cell walls in Luehea; and the presence of orbicules, absent only in Corchorus. This is the first embryological report of the Grewioideae subfamily, contributing to the characterization of the genera studied. The results are discussed in relation to the known data for the family.
Microsporogenesis and microgametogenesis of two species, Cardiospermum grandiflorum Sw. and Urvillea chacoensis Hunz. (Sapindaceae, Paullinieae), were studied using light and transmission electron microscopy. Both species are monoecious, with staminate and hermaphrodite, although functionally pistillate, flowers. A comparative pollen-development study of these two floral morphs is reported. For the present study, five stages of pollen ontogeny were identified. The development of the anther wall is of basic type. Its wall consists of epidermis, endothecium, two middle layers and a uninucleate secretory tapetum. The microspore tetrads are tetrahedral. The mature anther in staminate flowers presents the endothecium with well developed fibrillar thickenings, remains of tapetal cells, a single locule formed in the theca by dissolution of the septum before anther dehiscence and two-celled pollen grains when shed. In functionally pistillate flowers, the mature anthers present remnants of the middle layers, tapetal cells without signs of degradation, the theca with two locules and pollen grains uni- or bicellular, some of them with the cytoplasm collapsed. These anthers are not dehiscent. It can be concluded that male sterility is characterised by failure to produce functional pollen grains, an event that would be associated with the persistence of tapetal cells. Ultrastructural analysis clearly shows the difference in tapetal cells between the two flower morphs.
Next to pollen, stamens of flowering plants often produce microstructures, called orbicules, lining the locules. Although the existence of orbicules has been known since 1865, their function still remains enigmatic. This paper surveys orbicule distribution throughout angiosperms, including +1,500 entries. We show that orbicules are found all over of flowering plants with an evolutionary trend towards orbicule absence in more derived clades. Orbicules are common in the ANITA-grade and 85 % of the monocots studied produce orbicules, with Orchidaceae, Commelinales and Zingiberales as notable exceptions. Within eudicots, asterids are most densely sampled with 61 % orbicule presence. Asteraceae and the majority of Lamiaceae lack orbicules. For 17 angiosperm orders orbicule distribution data are lacking entirely. We demonstrate that the hypothesized correlation of orbicule presence with non-amoeboid tapetum types holds true. The presence of orbicules is therefore a convenient proxy for tapetum characterization. The potential of orbicules as an a-cellular model system for patterned sporopollenin polymerization is discussed and suitable model plants for future functional orbicule-research are identified.
Anther and pollen development in staminate and pistillate flowers of dioecious Melicoccus lepidopetalus (Sapindaceae) were examined by light and electron microscopy. Young anthers are similar in both types of flowers; they consist of epidermis, endothecium, two to four middle layers and a secretory tapetum. The microspore tetrads are tetrahedral. The mature anther in staminate flowers presents compressed epidermal cells and endothecium cells with fibrillar thickenings. A single locule is formed in the theca by dissolution of the septum and pollen grains are shed at two-celled stage. The mature anthers of pistillate flowers differ anatomically from those of staminate flowers. The epidermis is not compressed, the endothecium does not develop fibrillar thickenings, middle layers and tapetum are generally persisting, and the stomium is nonfunctional. Microspore degeneration begins after meiosis of microspore mother cells. At anthesis, uninucleate microspores and pollen grains with vegetative and generative nuclei with no cytokinesis are observed. Some pollen walls display an abnormal exine deposition, whereas others show a well formed exine, although both are devoid of intine. These results suggest that in the evolution towards unisexuality, the developmental differences of anther wall tissues and pollen grains between pistillate and staminate flowers might become more pronounced in a derived condition, such as dioecy.
The Burseraceae are a medium-sized family in which 18 genera are currently recognised. They are the subject of a long-term project to describe the pollen morphology from light, scanning electron and transmission electron microscopy. The pollen morphology of tribe Protieae has been published, as well as an account of the pollen of the African taxa in the family. Pollen data for the other two tribes, Bursereae and Canarieae, are more or less complete. The pollen of all the genera have been examined, with the exception of the recently described Pseudodacryodes Pierlot for which, currently, there is no pollen material available. This paper summarises the results. There is considerable variation in exine and aperture features between, and occasionally within, the genera and 14 major pollen types are defined, including two previously undescribed types: ‘ Canarium oleiferum ' and ‘ Canarium gracile '. The distribution of pollen characteristics throughout the family is compared with previously published tribal and subtribal groupings, as well as with current ideas of generic relationships from molecular analyses. Comparisons show notable congruence of pollen data with molecular data. To some extent pollen morphology is different for each of the subtribes. Nevertheless, there are some notable exceptions, for example, the pollen of Garuga and Boswellia are remarkably similar, although Garuga has been included, somewhat tenuously, in tribe Protieae, and Boswellia is included in tribe Bursereae, subtribe Boswelliinae. In a recent molecular tree Garuga and Boswellia appear to be closely related, and this supports the conclusion, based on several macromorphological characters as well as pollen, that Garuga should be transferred to tribe Bursereae.
Studies on the morphology and anatomy of the flower and anthesis of Metrodorea nigra St. Hill. (Rutaceae) showed perfect flowers, which occurred in panicle. The peak of the flowering was August and September. The anthesis was diurnal and the species presented protandrous flowers. The green sepals and the red petals presented papillose epidermis with stomata and parenchymatic mesophyll. The tetrasporangiate anther presented a papillose epidermis too, endothecium cells with secondary parietal thickenings, two middle layers and binucleate tapetum. The only pistil presented an ovary wall with nectariferous tissue and a meristematic ventral epidermis, a solid style and an inconspicuous stigma. The ovules were anatropous, bitegmic and crassinucelate and presented an obturator of funicular and placentic origin. The nectaries occurred around the ovary as a disk-like structure and in its apex as a number of pillose protuberances.
The Neotropical genus Averrhoidium (Sapindaceae) is classified in Doratoxyleae (Radlkofer 1934) and comprises four species with disjunct distribution: Averrhoidium dalyi is found in east Peru and northwest Brazil, Averrhoidium gardnerianum in east Brazil, Averrhoidium paraguaiense in Paraguay, and Averrhoidium spondioides in west Mexico. All species are dioecious subcanopy trees. Here we present for the first time observations on living material and detailed morphological and anatomical data of leaves, flowers, and dehisced fruits of A. dalyi. This information contributes to a more complete circumscription of the genus Averrhoidium. The type of seed presentation observed for Averrhoidium is found to be unique and remarkable for Sapindaceae: the one-seeded capsules dehisce, allowing the placenta and parts of the septa to turn outward like a tongue, while the single seed, with a conspicuous white sarcotesta, is still fixed to the placenta. It is dangling between neighboring undehisced red capsules and presumably attracts birds. Comparison of the structural features of the four Averrhoidium species shows that they are morphologically closely related, differing only in leaf characters (size, leaflet number, margin, secondary vein number, anatomy) and in their distribution area. A cladistic analysis of morphological data derived from literature and herbarium specimens confirms the position of Averrhoidium within Dodonaeoideae-Doratoxyleae as proposed by Radlkofer (1934). However, Doratoxyleae sensu Radlkofer (1934) appear to be paraphyletic, including two sapindoid taxa.
Premise of the study:
Koelreuteria (Sapindaceae) has four extant deciduous tree species, disjunctly distributed in eastern Asia and the Fiji Islands. While K. paniculata is widely cultivated, the biogeographic origin and evolutionary history of Koelreuteria remain unclear.
Methods:
Fruits, pollen, wood, and leaves of closely related extant taxa were examined in comparison with fossil remains to evaluate the fossil record and biogeographic history of Koelreuteria.
Key results:
Overall, characters of capsular fruits are more diagnostic than other organs for this genus. We describe two new species of fruit remains from the Eocene, K. taoana sp. nov. (northeastern China and far eastern Russia) and K. dilcheri sp. nov. (western United States), and give emended descriptions of three species: K. allenii (Lesq.) W. N. Edwards (early-late Eocene of the United States), K. macroptera (Kováts) W. N. Edwards (late Oligocene-early Pliocene of Europe), and K. miointegrifoliola Hu et R. W. Chaney (Miocene of eastern Asia).
Conclusions:
Reliable fossil records of capsules and ring-porous wood indicate that Koelreuteria may have originated in North Pacific-Rim area of the northern hemisphere by the early Eocene, representing an early temperate lineage in Sapindaceae adapted for wind dispersal. The fossils herein place a minimum age (ca. 52 Ma) for the divergence of Koelreuteria from tropical genera that appear more basal in the molecular phylogeny of Sapindaceae. Regional extinctions after the Eocene in North America and the Pliocene in Europe, reduced the range of Koelreuteria to eastern Asia, where three species occur today. The present distribution of another species in the Southern Pacific may be explained by long-distance dispersal.
Despite an emphasis on fruit characters in Paullinieae taxonomy, few detailed morphological and anatomical studies of the gynoecia, fruits and seeds exist. The aims of the present study were (1) to provide a detailed documentation of gynoecium, fruit and seed structure and ontogeny in selected Paullinieae taxa; (2) to determine whether the gynoecium, seed and seedling provide additional characters of systematic value within the tribe; and (3) to relate the structural findings to mechanisms of fruit dehiscence and dispersal within these taxa. Newly described characters of systematic value within Paullinieae are shape and surface of the obturator, type of pollen tube transmitting tract, indumentum of the inner and outer surface of the carpels, ovary wall anatomy, aril anatomy, pseudo-hilum form, seedling germination mode and structure of first leaves. The fruits of Paullinia are septifragal, and conspicuous colour contrasts between the pericarp, aril and seed in most species of this genus are suggestive of a bird dispersal syndrome. Interestingly, it appears that relatively minor structural changes are associated with switches to rodent dispersal in Paullinia sphaerocarpa and water dispersal in P. clathrata and P. hystrix. Anemochorous fruits are septifragal (Cardiospermum and Urvillea) or schizocarpic (Houssayanthus, Lophostigma, Serjania). They are structurally similar and Cardiospermum with septifragal capsules may also show septicidal dehiscence. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 159–189.
A survey of our own comparative studies on several larger clades of rosids and over 1400 original publications on rosid flowers
shows that floral structural features support to various degrees the supraordinal relationships in rosids proposed by molecular
phylogenetic studies. However, as many apparent relationships are not yet well resolved, the structural support also remains
tentative. Some of the features that turned out to be of interest in the present study had not previously been considered
in earlier supraordinal studies. The strongest floral structural support is for malvids (Brassicales, Malvales, Sapindales),
which reflects the strong support of phylogenetic analyses. Somewhat less structurally supported are the COM (Celastrales,
Oxalidales, Malpighiales) and the nitrogen-fixing (Cucurbitales, Fagales, Fabales, Rosales) clades of fabids, which are both
also only weakly supported in phylogenetic analyses. The sister pairs, Cucurbitales plus Fagales, and Malvales plus Sapindales,
are structurally only weakly supported, and for the entire fabids there is no clear support by the present floral structural
data. However, an additional grouping, the COM clade plus malvids, shares some interesting features but does not appear as
a clade in phylogenetic analyses. Thus it appears that the deepest split within eurosids–that between fabids and malvids -
in molecular phylogenetic analyses (however weakly supported) is not matched by the present structural data. Features of ovules
including thickness of integuments, thickness of nucellus, and degree of ovular curvature, appear to be especially interesting
for higher level relationships and should be further explored. Although features of interest are not necessarily stable at
the level of a large clade, they do show a considerable concentration in particular clades and are rare or lacking in others.
This may be viewed as a special trend for this feature to evolve in this group or to be conserved as a synapomorphy (or a
combination of both).
The black maple ( Acer saccharum Marsh, ssp. nigrum [Michx. f.] Desm.) gynoecium displays classical involute carpel development; carpels form, in mid‐ to late‐summer, as two separate, opposite, hood‐shaped primordia bearing naked megasporangia on inrolled carpel margins. Megasporogenesis, integument initiation, and carpel closure occur in spring; carpels fuse, forming a biloculate ovary with a short, hollow style and two divergent, dry, unicellular papillose stigmas. Transmitting tissues consist of developmentally and morphologically similar trichomes that form along the apparent carpel margins. The path from stigma to micropyle is open, but pollen tubes do not grow entirely ectotrophically. Germinating at the tip of a stigma papilla, a tube grows, apparently under the cuticle, to the papilla base. It then grows between stigma cells to the style, emerging to grow ectotrophically through the style to the compitum, where it passes into one of the locules. Within a locule, the tube grows over placenta and obturator to the micropyle, then between megasporangium cells to the female gametophyte, spreading over the surface near the egg. This study adds to our sparse understanding of gynoecium development and transmitting tissue in relation to pollen tube growth in naturally pollinated woody plants.
The floral development and vascular anatomy of Nitraria retusa were investigated in order to understand its characteristic androecium of 15 stamens and to clarify the systematic position of the genus relative to Zygophyllaceae. Sepals arise in a helical sequence and are relatively small at maturity. Petals are initiated almost simultaneously or in a rapid helical sequence. Five stamen primordia arise opposite the sepals. Next, two other antesepalous primordia are incepted centrifugally to the first primordia on the remaining receptacular surface. The outer stamens tend to be squeezed between the petals and upper stamens and appear to make up an antepetalous whorl of stamens. Three carpels arise from a low ringwall and grow into a hairy trilocular pistil. In each locule a single pendulous ovule is present. Disclike nectarial tissue is initiated in pits between the stamens and petals. Long trichomes develop on its surface. It is concluded that the androecium is linked with a haplostemonous condition because the stamens of each triplet develop on strictly localized sectors. The distinction between stamens arising on complex primordia and the inception of three independent units is explained by the “principle of variable proportions.” The vasculature also tends to confirm that the outer stamen pairs belong to antesepalous triplets.
Premise of research.?The comparative development of staminate and pistillate flowers in Pseuduvaria trimera (Annonaceae) was investigated for the first time to understand its sexual differentiation and developmental processes. The morphological and anatomical features of mature stamens and staminodes were also compared to clarify anther dehiscence and to understand the mechanism underlying staminode sterility.
Methodology.?Flowers at different developmental stages as well as mature stamens and staminodes were examined using SEM and LM.
Pivotal results.?Similar to other Annonaceae, the flowers of Pseuduvaria trimera have a complex whorled phyllotaxis. They have double positions in the outermost whorl of reproductive organs and variable numbers of stamens and carpels per whorl. The stomium region of each theca is composed of the septum and the stomium. The septum and stomium cells of stamens degenerate and facilitate anther opening, whereas those of staminodes remain intact and form indehiscent anthers.
Conclusions.?The data suggest that staminate flowers are unisexual from their inception while pistillate flowers are morphologically hermaphroditic but nevertheless functionally pistillate. The anthers are indehiscent, and the structural andromonoecy of P. trimera actually functions as monoecy. The mechanism underlying the sterility of the indehiscent staminodes and the delayed dehiscence of the outer stamens might promote xenogamy. The presence of the staminodes is closely correlated with the evolution of functional unisexual flowers in the genus Pseuduvaria.
Maple trees are known for their varied sexual and floral systems. One such system, andromonoecy, has generated considerable interest in terms of sexual system and evolution in angiosperms. In Acer oblongum three different flowering morphs were present on each individual: Staminate type I (Male type I), hermaphrodite and Staminate type II (Male type II) flowers. Staminate type I flowers bloom early in the season followed by hermaphrodite and Staminate type II. The objective of this study was to elucidate sexual system in A. oblongum by comparing male and female organ performance of different floral morphs and assess its adaptive significance. Phenology, morphometry, resource allocation patterns, and pollen and pistil performance of three morphs were compared in order to elucidate the sexual system. Significant differences were observed in resource allocation patterns of different floral morphs. The variation was mainly because of androecium and gynoecium weight. Anthers of hermaphrodite morphs remain indehiscent while number and size of anthers were less than that of staminate types. The number of pollen per flower in case of hermaphrodite flowers was smaller and their pollen showed lower viability when compared with staminate types. Although pollen from hermaphrodite flowers failed to germinate on the receptive stigmas, it yielded positive FCR viability test. Morphologically hermaphrodite flowers of A. oblongum do not possess male function and are functionally female, although a relict function of attracting pollinators cannot be ignored. Acer oblongum is cryptically monoecious while functionally andromonoecious.
The developmental morphology of the obturator and micropyle and the pathway of the pollen tubes in the ovarian locule in Phellodendron amurense Rupr. have been investigated by scanning electron microscopy and light microscopy. The obturator of the ovule is of funicular origin. As the ovule is fully developed, the obturator becomes considerably large and closely covers the micropyle. When the pistillate flower reaches the receptive phase, the morphology of the obturator is greatly modified, and its cells on the surface are radially expanded and appear to be columnar, semi-papillar or papillar. Following fertilization the obturator reduces in size and degenerates. The pollen tubes need not necessarily traverse the obturator. Whether the pollen tubes pass the obturator or not depends on the sites at which they enter the ovarian locule. This observation does not support the idea that the obturator mainly serves the function of mechanical guidance for the growth of pollen tubes. Our investigations indicate that the structure of the micropyle changes with the different stages of the reproductive process, and becomes asymmetrical during pollination. The development of the obturator and the micropyle correlates with that of the female gametophyte in P. amurense.
Orbicules or Ubisch bodies are corpuscles of sporopollenin that appear in the anther locule during pollen grain development. Their size ranges from 0.14 μm to 20 μm. They present different shapes with a smooth or ornamented surface. Orbicules often form aggregates and sometimes have a plaque-like appearance. Ultrastructurally, they may present a central core with different degree of transparency to electrons. Those that do not have a central core are observed completely solid. Orbicules are resistant to acetolisis, autofluorescent when irradiated with ultraviolet light and have the same reaction to colorants that the exine of pollen grains. Their presence is generally associated with a tapetal membrane in species with secretor type tapetum and with a peritapetal membrane in species with intermediate or plasmodial type tapetum. Although the shed of orbicules out of the anther along with the pollen grains is cited, they are usually attached to the inner surface of the locule when the anther opens. Investigations suggest that orbicules appear in approximately 80 families of Angiosperms and Gimnosperms. It is not certain whether orbicules are not developed in the rests of the families or are just not informed. Researches on ontogeny and ultrastructure of orbicules are rare. However, their tapetal origin and their simultaneous formation with the pollen grain wall are well established. The systematic value of orbicules is known and considered in a few families, such as Loganiaceae, Gentianaceae, Apocynaceae, Rubiaceae and Oxalidaceae. Evolutionary studies on these bodies or on its relationship with the different modes of pollination are lacking. Even though orbicules are so common among angiosperms, their function is unknown and only speculations are made. On this report a review on orbicules is made and an analysis of their presence, ontogeny and morphology is presented. Our aim is to supply information that will help understand orbicules function. Therefore, the orbicules morphology in relation with the pollination mode is studied.
The tapetum of the anther or microsporangium in flowering plants has evolved functions related to the needs of the seed habit in addition to that of nourishing the microspore. A tapetum is available to megaspores where they are subsequently shed from the plant, as in Selaginella and Isoetes. Where the megaspore is retained, as in the seed plants, the typically transient tapetum is replaced by a more sustained nutrient supply, of which the so-called “integumentary tapetum” is a component. In flowering plants, in order from the exterior to the interior of the anther, are the epidermis, endothecium, middle layers, tapetum, and sporogenous tissue. The sporogenous tissue provides the contents of the pollen chamber and to which the tapetum forms a lining. At meiosis the four microspores are encased in the callose wall of the pollen mother cell for a period. If pollen development, including wall deposition, is well advanced before the callose wall is broken down, the direct tapetal contribution is smaller than where the breakdown happens earlier. Glandular and amoeboid tapeta remove the callose wall relatively earlier and later, respectively. Pollen therefore, surrounded by a glandular tapetum, derives more of its wall-forming precursors directly from the tapetum.
This volume provides a comprehensive overview of tropical flower diversity, thereby forming an indication of evolutionary trends. An introductory chapter provides an evolutionary context and introduces tropical flowers. Six chapters then deal with general structural and biological features of flowers and illustrate facets of their diversity: floral organization (structural units and floral symmetry, perianth, androecium, gynoecium, and floral phyllotaxis); floral construction/architecture; adaptation to different pollinators; differentiations associated with pollinator attraction (for example - nectaries, resin glands/flowers, optical displays, and tactile guides); differentiations associated with breeding systems (for example - sex expression, dichogamy, herkogamy, heterostyly, and agamospermy); and the process of anthesis. Chapter eight then outlines floral diversity and evolution of selected tropical systematic groups: Magnoliales (Magnoliidae); Laurales (Magnoliidae); Aristolochiales (Magnoliidae); Lecythidales (Dilleniidae); Violales (Dilleniidae); Fabales (Rosidae); Gentianales (Asteridae); Scrophulariales (Asteridae); Zingiberales (Zingiberidae); and Orchidales (Liliidae). Next, the salient aspects of flower evolution are reviewed. To conclude, the author underlines the need for research synthesis at all levels. -S.R.Harris
In order to investigate the embryological characteristics of Delavaya toxocarpa and provide a basis for further understanding the phylogeny within Sapindaceae s.l., we studied the sporogenesis and gametogenesis of D. toxocarpa by using the conventional paraffin section method. The results are as follows: anthers are tetrasporangium; tapetum is typically secretory type; cytokinesis in the microsporecyte meiosis is of the simultaneous type and microspore tetrads are tetrahedral; mature pollen contains two cells; the ovary is bilocular with two ovules per locule; placentation is axial; the ovule is amphitropous, bitegmic and crassinucellate; the chalazal megaspore in a linear tetrad becomes functional; the development of megaspore is of the polygonum type. Most similarities shared by the species observed suggest that the species and genera of Sapindaceae s.l. have phylogenetic consistency. The distinctive trait, lacking hypostase, indicates Delavaya (and Handeliodendron) might be more primitive than other genera in Sapindaceae. Moreover, some characters, such as opposite palmate compound leaf, apical thyrse, rounded seed without wing, 2 hemitropous ovules per locule, lacking aril, indicate the close relationship among Delavaya, Aceraceae and Hippocastanaceae. The preliminary data about embryological and morphological characteristics in Delavaya might justify the basic systematic position of this genus in the family Sapindaceae s.s.
Biebersteinia, a perennial herb of five species distributed from Greece to Central Asia, was long considered to be placed in, or near Geraniaceae. Recent molecular analyses, however, have shown that the genus is the sole member of the family Biebersteiniaceae in Sapindales (not including Geraniaceae). Here, we report the embryological features of Biebersteinia and provide embryological corroboration for the molecular sapindalean affinities of the genus. We compared its embryology with those of eight other families of Sapindales, as well as with those of the related orders Huerteales, Malvales, and Brassicales. Overall comparisons showed that Biebersteinia fits in Sapindales because of the presence of anther tapetal cells with polyploid nuclear mass and non-fibrous exotegmen. Further, the genus is characterized by three-celled pollen grains, tetrasporic 16-nucleate Penaea-type female gametophyte, unitegmic ovules, pseudoporogamy, and the chalaza shifting its position near the concave side in the post-fertilization stage. A considerable number of autapomorphies, combined with the lack of synapomorphies with other sapindalean families, supports placing Biebersteinia in its own family. Biebersteiniaceae appear to represent an early divergent lineage of Sapindales. Previous descriptions of seed coats, which were considered to have developed from "bitegmic" ovules, were revised.
Acer stigmas were said by Heslop-Harrison and Shivanna (Ann. Bot. 41: 1232-1258. 1977) to be dry and non-papillate, a statement supported by unillustrated observations on two unnamed species. We report here that the earlier literature, and our own observations on six species, show instead that Acer has a papillate stigma. Rudimentary pistils of staminate flowers, common in Acer, could result in erroneous observations of stigmas. Presence of papillate stigmas in Acer is consistent with the presence of papillate stigmas in closely related groups. Increase in papillae development allows increase in stigma surface area, thereby contributing to more efficient wind pollination, a mode which has evolved in a number of maple species.
Black maple [Acer saccharum Marsh. subsp. nigrum (Michx. f.) Desm.] anthers overwinter in the microsporocyte stage. The microsporocytes are surrounded by a tapetal layer, two middle layers, an endothecium, and an epidermis. In the spring, tapetal cells become binucleate or multinucleate as microsporogenesis proceeds basipetally through the entire inflorescence and its individual branches. Development is nearly synchronous within all locules of individual anthers. As microsporogenesis progresses, middle layers become crushed and the glandular (secretory) tapetum degenerates. Tetrahedral tetrads are formed by simultaneous cytokinesis, followed by dissolution of callose and release of microspores. After microspore mitosis, pollen is shed at the two-celled stage. In functionally pistillate flowers, pollen maturity is delayed until after anthesis, yet filament elongation and anther dehiscence do not occur. Endothecial wall thickenings are present in the anthers of pistillate flowers and show no differences that appear to contribute to the lack of anther dehiscence. In both staminate and pistillate flowers, mature endothecial cells are radially elongate with fibrous thickenings forming a cage of more-or-less parallel bands along each cell's anticlinal walls. On the inner periclinal cell face, the bands anastomose into a central baseplate; on the outer periclinal face, bands are continuous, though often attenuated. This paper presents the first photographically documented observations of microsporogenesis and the first description of endothecial wall thickenings for the Aceraceae. Observations presented confirm and supplement previous scattered observations of anther and pollen development in Acer
Recent molecular analyses found the Chinese monotypic genus Xanthoceras to be either a sister genus to the rest of a broadly defined Sapindaceae sensu lato (s.l.) including Aceraceae and Hippocastanaceae or the only genus of the Xanthoceraceae. Here we investigate for the first time the embryology of Xanthoceras and compare the embryological data with related taxa to aid in understanding the phylogenetic relationships of this genus. The results indicate that Xanthoceras shares many embryological features with Sapindaceae sensu stricto (s.s.), Aceraceae, and Hippocastanaceae, including a glandular tapetum, simultaneous microsporogenesis, three-colporate pollen grains, a bitegmic and crassinucellate ovule, Polygonum type of embryo sac development, endosperm formation of the nuclear type, and exalbuminous mature seeds. The wide range of similarities in embryological features suggests that Xanthoceras is closely related to other members of Sapindaceae s.l. However, Xanthoceras differs from other Sapindaceae in several morphological characteristics, for instance, five to eight ovules in each locule in Xanthoceras versus one to two ovules in each locule in other Sapindaceae s.l., and five golden horn-like appendages present on both staminate and hermaphrodite flowers of Xanthoceras versus absent on the flowers of other Sapindaceae s.l. We propose that Xanthoceras merits recognition at the subfamily level as Xanthoceroideae, rather than at the family level as Xanthoceraceae. The present study also reveals that late-acting ovarian self-incompatibility (OSI) occurs in X. sorbifolium and that postzygotic OSI contributes to the self-sterility of the species.
HA, C. O., SANDS, V. E., SOEPADMO, E. & JONG, K., 1988. Reproductive patterns of selected understorey trees in the Malaysian rain forest: the sexual species. Investigations were carried out on the floral, fruit and seed biology, and the embryology of representatives of the Sapindaceae and Bombacaceae which occur in the lower canopy of the lowland rain forest of Peninsular Malaysia. Pollination studies indicated cross-compatibility and outbreeding in all species examined, associated with self-compatibility in the polygamous monecious Pometia pinnata and Allophylus cobbe and, to a limited extent, in the effectively dioecious Xerospermum intermedium. In these sapindaceous species, together with the self-incompatible androdioecious Nephelium lappaceum, the structurally hermaphrodite flowers were determined embryologically to be functionally female with no anther dehiscence. The self-incompatible Durio griffithii of the Bombacaceae, and X. intermedium, N. lappaceum and P. pinnata were shown by embryological studies to form a sexual zygote. The observations on these outcrossing species are considered in relation to their potential for gene exchange and their contribution to the maintenance of species diversity in the lowland rain forest.
This paper reports upon a study of the characteristics of the receptive surfaces of angiosperm stigmas, covering almost 1000 species of about 900 genera of some 250 families. In both monocotyledons and dicotyledons the major subdivision is into those stigmas which are ‘dry’ at maturity, having a hydrated, proteinaceous extracuticular layer or pellicle but no free-flowing secretion, and those which are ‘wet’ bearing such a fluid secretion when in the receptive state. Further subdivision may be made talcing into account the nature of the surface cells—whether or not the receptive surface is papillate or smooth, and if papillate, whether the papillae are unicellular or multicellular. When the genera are classified according to these criteria, various taxonotnic regularities emerge. Many families are homogeneous in stigma type, but some prove to be diverse. Among these are families such as the Liliaceae, a fact that may have phylogenetic significance.
The physiological importance of stigma type is shown by the correlations that exist between the characteristics of the receptive surface and self-incompatibility system. Sporophytic self-incompatibility systems are associated with dry, papillate stigmas; most gametophytic systems with wet stigmas. Further relationships exist with pollen type and physiology. Trinucleate pollen, not readily germinated in vitro, tends to be associated with dry stigmas, while wet-stigma forms tend to have binucleate pollen, easily germinated in liquid or semi-solid media; binucleate pollen, however, occurs with both wet and dry stigmas.
The black maple (Acer saccharum Marsh. ssp. nigrum [Michx. f.] Desm.) gynoecium displays classical involute carpel development; carpels form, in mid- to late-summer, as two separate, opposite, hood-shaped primordia bearing naked megasporangia on inrolled carpel margins. Megasporogenesis, integument initiation, and carpel closure occur in spring; carpels fuse, forming a biloculate ovary with a short, hollow style and two divergent, dry, unicellular papillose stigmas. Transmitting tissues consist of developmentally and morphologically similar trichomes that form along the apparent carpel margins. The path from stigma to micropyle is open, but pollen tubes do not grow entirely ectotrophicaly. Germinating at the tip of a stigma papilla, a tube grows, apparently under the cuticle, to the papilla base. It then grows between stigma cells to the style, emerging to grow ectotrophically through the style to the compitum, where it passes into one of the locules. Within a locule, the tube grows over placenta and obturator to the micropyle, then between megasporangium cells to the female gametophyte, spreading over the surface near the egg. This study adds to our sparse understanding of gynoecium development and transmitting tissue in relation to pollen tube growth in naturally pollinated woody plants.
The pendulous, bitegmic, anatropous ovulr with dorsal raphe is suspended at the tip of a massive funicle. A group of nurellar cells with intensively staining cell walls, the hypostase sensu stricto, is present. The initially plate-like tanniniferous chalazal-nucellar tissue, with suberin and lignin impregnated cell walls represents a hypostase sensu lato. The mature seed-coat is formed by the raphe, extensive chalaza, adjacent, well-developed, cup-like hypostase sensu lato, remnants of the two integuments and a cuticular layer. The exalbuminous seed of Sclerocarya birrea suhsp. caffra (the Marula), is regarded to he a derived and phylogenetically advanced type. The undifferentiated seed-roat is very similar to that found in Lannea discolor which, like the marula, belongs to the tribe Spondieae. The similarities in the structure of the seed-coat and seed of the marula and L. discolor confirm their proposed close phylogenetir relationship.
The apocarpous gynoecia of three separate groups of higher advanced dicotyledons show postgenital fusion of their apical parts. In this fused region the pollen tube transmitting tissue of the carpels is united into a compitum, which provides advantages of a syncarpous to the apocarpous gynoecium. It is supposed that in at least some of these groups the general evolutionary trend of the angiosperms from apocarpy towards syncarpy is reversed.
Pistacia atlantica, P. palaestina, P. lentiscus and P. saportae, were found to have great similarity in their embryology and fruit development. The anatropous, pendulous and crassinucellate ovule was initially unitegmic; later, the integument split close to the micropyle, forming a partial second integument. After anthesis there was a development of a hypostase and an obturator. The development of the Polygonum-type embryo sac followed division of a megaspore mother cell, giving a tetrad or triad of megaspores. The functional megaspore was the chalazal one. The ovary developed into a mature pericarp after anthesis, even when pollination was prevented, and before the zygote divided. Therefore, the fruit can be parthenocarpic. The ovule started to grow after initiation of embryo development until it filled the cavity within the pericarp. The zygotes were dormant for 4–18 weeks after pollination. In P. saportae reproduction became arrested during the development of the embryo sac; only very few abnormal embryos were found. No fixed pattern of embryo development could be discerned. The endosperm was initially nuclear, becoming cellular when the embryo started to develop. The seed coat was derived from the integument and the remnants of the nucellus.
Anacardiaceae and Burseraceae are traditionally distinguished by the number of ovules (1 vs. 2) per locule and the direction of ovule curvature (syntropous vs. antitropous). Recent molecular phylogenetic studies have shown that these families are sister groups in Sapindales after having been separated in different orders for a long time. We present a comparative morphological study of the flower structure in both families. The major clades, usually supported in molecular phylogenetic analyses, are well supported by floral structure. In Anacardiaceae, there is a tendency to gynoecium reduction to a single fertile carpel (particularly in Anacardioideae). The single ovule has a long and unusually differentiated funicle, which connects with the stylar pollen tube transmitting tract in all representatives studied. In Anacardiaceae–Spondiadoideae, there is a tendency to form an extensive synascidiate zone, with a massive remnant of the floral apex in the centre; these features are also present in Beiselia (Burseraceae) and Kirkiaceae (sister to Anacardiaceae plus Burseraceae) and may represent a synapomorphy or apomorphic tendency for the three families. In core Burseraceae, gynoecium structure is much less diverse than in Anacardiaceae and has probably retained more plesiomorphies. Differences in proportions of parts of the ovules in Anacardiaceae and Burseraceae are linked with the different direction of ovule curvature. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 499–571.
WANNAN, B. S. & QUINN, C. J, 1991. Floral structure and evolution in the Anacardiaceae. Carpel morphology and anatomy is investigated in 17 genera and carpellode morphology in 12 genera. There is an evolutionary sequence in the family from poorly differentiated, nearly apocarpous gynoecia towards syncarpous gynoecia with clearly defined stigmata, styles and ovaries. There has also been marked reduction culminating in pseudomonomery. The carpellodes of the male flowers appear more conservative, and provide evidence of affinities between genera with quite different fertile gynoecia. The characters have been polarized using Burseraceae as a sister group. Data from these sources, as well as from pericarp anatomy, wood anatomy and biflavonoid content indicate that the long standing intrafamilial classification into five tribes is artificial, and that the two small satellite families, Blepharocaryaceae and Julianiaceae should be included in the family. A large monophyletic group is recognized comprised of essentially four of the existing tribes (Anacardiëae, Dobineëae, Semecarpeae, Rhoëae), as well as the two satellite families. This group incorporates two subgroups of more closely allied genera. The remaining genera (mostly Spondiadeae) are very diverse, and for the present are placed in an artificial group characterised by a set of plesiomorphs. Relationships within this group must be resolved before a satisfactory taxonomy of the family can be achieved.
Phylogenetic relationships in a Malagasy clade of Sapindaceae, encompassing Molinaea (with members also in the Mascarene Islands), Neotina, Tina and Tinopsis, were inferred by expanding a previous nuclear and plastid DNA data set for the family. The circumscription of these morphologically similar genera has remained problematic since the first family-wide treatment. To investigate this situation, representative taxa were analysed to: (1) test the monophyly of the genera; (2) investigate their phylogenetic relationships; and (3) explore alternative circumscriptions that reflect phylogeny and yield genera that are morphologically coherent and easily characterized. Phylogenetic inferences supported the monophyly of the group and its subdivision into three clades. All species of Molinaea sampled belong to a clade (Clade I) that is sister to a clade comprising Neotina, Tina and Tinopsis, within which one clade (Clade II) encompasses Tinopsis and Neotina (with the latter nested within the former) and another (Clade III) comprises all taxa of Tina. These three genera can be easily distinguished from Molinaea by having two rather than three carpels, which represents an unambiguous synapomorphy. Given the paraphyly of Tinopsis with regard to Neotina and the strong support for the monophyly of Tina, two potentially viable options are available for the generic delimitation of the taxa in this clade: (1) to recognize two genera corresponding, respectively, to Clades II and III; or (2) to place all of the taxa in a single genus encompassing both clades. Based on a review of morphological evidence the second option is favoured and consequently a broad generic concept is applied. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 165, 223–234.
It appears that the tapetum is universally present in land plants, even though it is sometimes difficult to recognize, because it serves mostly as a tissue for meiocyte/spore nutrition. In addition to this main function, the tapetum has other functions, namely the production of the locular fluid, the production and release of callase, the conveying of P.A.S. positive material towards the loculus, the formation of exine precursors, viscin threads and orbicules (= Ubisch bodies), the production of sporophytic proteins and enzymes, and of pollenkitt/tryphine. Not all these functions are present in all land plants:Embryophyta. Two main tapetal types are usually distinguished in theSpermatophyta: the secretory or parietal type and the amoeboid or periplasmodial type; in lower groups, however, other types may be recognized, with greater or lesser differences. A hypothetical phylogenesis of the tapetum is proposed on the basis of its morphological appearance and of the nutritional relations with meiocytes/spores. The evolutionary trends of the tapeta tend towards a more and more intimate and increasingly greater contact with the spores/pollen grains. Three evolutionary trends can be recognized: 1) an intrusion of the tapetal cells between the spores, 2) a loss of tapetal cell walls, and 3) increasing nutrition through direct contact in narrow anthers.