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Flower of Tupidanthus calyptratus (Araliaceae; SEM; modified from Sokoloff et al. 2007b). A: Beginning of initiation of calyx and corolla tubes. B: Development of calyx and corolla tubes. C: Oblique view of flower showing corolla tube appressed to floral meristem. D: Flower at stage of stamen initiation; corolla partly removed. E: Part of corolla at nearly the same stage as in D viewed from inside, i.e. from adaxial side. F: Part of developing corolla, top view, with its suture being closed by special hairs along margin. brl, bracteole; ca, calyx; co, corolla; fsb, flower-subtending bract; st, stamen. (Scale bars: A, B = 150 μm, C = 100 μm, D = 400 μm, E = 200 μm, F = 100 μm.)
Source publication
Fusion between floral organs or their parts is believed to have played key roles in the origin and subsequent diversification of angiosperms. Two types of fusion can be recognized: postgenital and congenital. Postgenital fusion is readily observable during flower development: primary morphological surfaces of contacting structures meet and join dur...
Context in source publication
Context 1
... and Erbar 2004;Nicolas and Plunkett 2009;Chaerophyllum of Apiaceae, Erbar and Leins 1997;Nuraliev et al. 2017), total absence of the calyx whorl was reported: no traces of sepal primordia were found in developmental studies. In several species of Araliaceae, such as Schefflera actinophylla, S. subintegra ( Fig. 7A-C) and Tupidanthus calyptratus ( Fig. 8A-D), the calyx is represented only by a tube without any free lobes since its initiation ( Sokoloff et al. 2007b;Nuraliev et al. 2009Nuraliev et al. , 2010Nuraliev et al. , 2011Nuraliev et al. , 2014Nuraliev et al. , 2017; though of course in this case it is espe- cially difficult to demonstrate that this structure is indeed a calyx tube ...
Citations
... Jonker 1938). The conventional nature of distinction between the imperfect postgenital fusion of floral organs and just an appression of their free surfaces was highlighted for angiosperms in general by Sokoloff et al. (2018). ...
Thismia papillata, a new species of Thismiaceae, is described and illustrated. The species was discovered in 2023 in Thanh Hoa Province, northern Vietnam. The new species is readily distinguishable from most of its congeners by the presence of appendages of outer and inner tepals, inner tepals fused into a mitre, absence of a wing-like appendage of supraconnective and absence of interstaminal glands. Thismia papillata is similar to T. abei, T. taiwanensis and T. tuberculata, differing mainly in prominently papillate outer hypanthium surface, appendages of the outer tepals up to 15 mm long, appendages of the inner tepals up to 9 mm long, and column-like placentas. Gaps in understanding of interactions between the inner tepals in Thismia are highlighted that are related to the postgenital tepal fusion and tepal aestivation. Similar uncertainties in determination of fusion between the stamens are also uncovered.
... Sattler [17] distinguished the following processes: zonal growth, heterotopy, meristem extension, and interprimordial growth. Sokoloff et al. [18] (p. 18) equate congenital fusion with zonal growth, which is only one of the processes subsumed under the concept of congenital fusion. ...
Since the 19th century, we have had countless debates, sometimes acrimonious, about the nature of the gynoecium. A pivotal question has been whether all angiosperms possess carpels or if some or all angiosperms are acarpellate. We can resolve these debates if we do not define the carpel as a closed megasporophyll but simply as an appendage that encloses the placenta or a single ovule. This redefinition may, however, lead to confusion because often it may not be clear whether the traditional (classical) definition of the carpel or the redefinition is implied. Therefore, a topographic approach is proposed that is compatible with the redefinition. According to this approach, gynoecia comprise one or more gynoecial appendages and placentas or single ovules that may be formed in different positions. Heterotopy refers to these different positions. In the context of evo-devo, which explores evolutionary changes in development, morpho evo-devo delves into spatial shifts of the placentas and ovules leading to heterotopy. Furthermore, it considers shifts in timing (heterochrony) and other processes leading to heteromorphy. Recognizing spatial shifting of the placentas or a single ovule and other evolutionary processes opens up new vistas in the search for the ancestor(s) of angiosperms and their gynoecia.
... In theory, initiation as two free primordia, taken in isolation from all other arguments, cannot be regarded as a necessary or sufficient condition of recognition of two congenitally united organs. In so-called early congenital fusion, free parts of united organs become visible after the initiation of their common part (Sokoloff et al., 2018). There are even cases when one and the same organ initiates as two distinct primordia. ...
Introduction
Understanding the complex inflorescence architecture and developmental morphology of common buckwheat (Fagopyrum esculentum) is crucial for crop yield. However, most published descriptions of early flower and inflorescence development in Polygonaceae are based on light microscopy and often documented by line drawings. In Fagopyrum and many other Polygonaceae, an important inflorescence module is the thyrse, in which the primary axis never terminates in a flower and lateral cymes (monochasia) produce successively developing flowers of several orders. Each flower of a cyme is enclosed together with the next-order flower by a bilobed sheathing bract-like structure of controversial morphological nature.
Methods
We explored patterns of flower structure and arrangement in buckwheat and its wild relatives, using comparative morphology, scanning electron microscopy and X-ray microtomography.
Results
Our data support interpretation of the sheathing bract as two congenitally fused phyllomes (prophylls), one of which subtends a next-order flower. In tepal-like bract, a homeotic mutant of F. esculentum, the bilobed sheathing bract-like organ acquires tepal-like features and is sometimes replaced by two distinct phyllomes. Wild representatives of F. esculentum (ssp. ancestrale) and most cultivars of common buckwheat possess an indeterminate growth type with lateral thyrses produced successively on the primary inflorescence axis until cessation of growth. In contrast, determinate cultivars of F. esculentum develop a terminal thyrse after producing lateral thyrses. In contrast to F. esculentum, the occurrence of a terminal thyrse does not guarantee a determinate growth pattern in F. tataricum. The number of lateral thyrses produced before the terminal thyrse on the main axis of F. tataricum varies from zero to c. 19.
Discussion
The nine stages of early flower development formally recognized here and our outline of basic terminology will facilitate more standardized and readily comparable descriptions in subsequent research on buckwheat biology. Non-trivial relative arrangements of tepals and bracteoles in Fagopyrum and some other Polygonaceae require investigation using refined approaches to mathematical modelling of flower development. Our data on inflorescence morphology and development suggest contrasting evolutionary patterns in the two main cultivated species of buckwheat, F. esculentum and F. tataricum. The genus Fagopyrum offers an excellent opportunity for evo-devo studies related to inflorescence architecture.
... Further reading: Weberling (1989); Verbeke (1992); Endress (1994Endress ( , 2011Endress ( , 2015; Leins and Erbar (2010); Sokoloff et al. (2018);and Phillips et al. (2020). 1974a). ...
... This interpretation is complementary to ideas on carpel dimorphism outlined above. Although of very different evolutionary origin, the grass gynoecium and the behaviour of its stigmas approach the condition of mixomery found in Cyperaceae (Reynders et al., 2012;Sokoloff et al., 2018). ...
The grass family (Poaceae) includes cereal crops that provide a key food source for the human population. The food industry uses the starch deposited in the cereal grain, which develops directly from the gynoecium. Morphological interpretation of the grass gynoecium remains controversial. A bistigmatic grass gynoecium has two sterile carpels, each producing a stigma, and a fertile carpel that lacks a stigma. To date, studies of grass developmental genetics and developmental morphology have failed to fully demonstrate the composite nature of the grass gynoecium because its complex evolutionary history is hidden by extreme organ integration. We reexamine earlier hypotheses and studies of morphology and development in the context of more recent analyses of grass phylogenetics and developmental genetics. Taken in isolation, data on gynoecium development in bistigmatic grasses do not contradict its interpretation as a solitary ascidiate carpel. Nevertheless, in the context of other data, this interpretation is untenable. Broad comparative analysis in a modern phylogenetic context clearly demonstrates that the grass gynoecium is pseudomonomerous. It is problematic to interpret the gynoecium of grasses in terms of normal angiosperm gynoecium typology. Even the concept of carpel becomes misleading in grasses; instead, we recommend the term pistil for descriptive purposes.
... We focused on mesangiosperms because Ceratophyllum represents one of the five well-supported clades composing mesangiosperms; its relationships with the four other clades (eudicots, monocots, magnoliids and Chloranthaceae) remain insufficiently resolved. Sauquet et al. (2017) did not differentiate between gynoecia with congenital and postgenital carpel fusion, which differ fundamentally in their development (Endress, 2006;Sokoloff et al., 2018b). Congenital and postgenital fusions are apparently governed by different gene regulatory networks. ...
... The family Chloranthaceae has received special attention as the potential sister group of Ceratophyllum because of several shared morphological characters (Endress and Doyle, 2009;Endress and Doyle, 2015;Doyle and Endress, 2018). Among the four extant genera of Chloranthaceae (Ascarina, Chloranthus, Hedyosmum, Sarcandra), the ovary is inferior in pistillate flowers of Hedyosmum, where there are three perianth organs (Endress, 1971;Endress, 1987b;Doyle and Endress, 2014;Sokoloff et al., 2018b). In Ascarina, the gynoecium is the only organ of the pistillate flower, so the condition of ovary position is unknown relative to other organs (Endress, 1987b;Doyle and Endress, 2014). ...
... Angiosperm flowers that show the degree of unequal maturation that is observed in staminate reproductive units Ceratophyllum are apparently unknown (Endress and Doyle, 2015), though this feature could represent a highly specialized pollination mode that is extremely uncommon among angiosperms. Staminate reproductive units of Hedyosmum that are morphologically similar to those of Ceratophyllum are not characterized by prolonged proliferation (Sokoloff et al., 2018b). ...
Molecular phylogenetic analyses have revealed a superclade of mesangiosperms with five extant lineages: monocots, eudicots, magnoliids, Ceratophyllum and Chloranthaceae. Both Ceratophyllum and Chloranthaceae are ancient lineages with a long fossil record; their precise placement within mesangiosperms is uncertain. Morphological studies have suggested that they form a clade together with some Cretaceous fossils, including Canrightia, Montsechia and Pseudoasterophyllites. Apart from Canrightia, members of this clade share unilocular gynoecia commonly interpreted as monomerous with ascidiate carpels. Alternatively, the gynoecium of Ceratophyllum has also been interpreted as syncarpous with a single fertile carpel (pseudomonomerous). We investigate patterns of morphological, anatomical and developmental variation in gynoecia of three Ceratophyllum species to explore the controversial interpretation of its gynoecium as either monomerous or pseudomonomerous. We use an angiosperm-wide morphological data set and contrasting tree topologies to estimate the ancestral gynoecium type in both Ceratophyllum and mesangiosperms. Gynoecia of all three Ceratophyllum species possess a small (sometimes vestigial) glandular appendage on the abaxial side and an occasionally bifurcating apex. The ovary is usually unilocular with two procambium strands, but sometimes bilocular and/or with three strands in C. demersum. None of the possible phylogenetic placements strongly suggest apocarpy in the stem lineage of Ceratophyllum. Rescoring Ceratophyllum as having two united carpels affects broader-scale reconstructions of the ancestral gynoecium in mesangiosperms. Our interpretation of the glandular appendage as a tepal or staminode homologue makes the Ceratophyllum ovary inferior, thus resembling (semi)inferior ovaries of most Chloranthaceae and potentially related fossils Canrightia and Zlatkocarpus. The entire structure of the flower of Ceratophyllum suggests strong reduction following a long and complex evolutionary history. The widely accepted notion that apocarpy is ancestral in mesangiosperms (and angiosperms) lacks robust support, regardless of which modes of carpel fusion are considered. Our study highlights the crucial importance of incorporating fossils into large-scale analyses to understand character evolution.
... The inferior ovary is trilocular from its inception proximally (synascidiate zone) and secondarily trilocular distally (symplicate zone). Along the most symplicate zone, the lines of postgenital closure of ventral slits are undetectable in the cross section, i.e., the postgenital fusion is of perfect type (sensu Sokoloff et al., 2018). In the distal part of the symplicate zone of B. disticha (Figures 3E,F) the tissue in the gynoecium center is lignified to form a central column ( Supplementary Figures 2A-D, 3A-E). ...
... A tube in a flower that bears all the floral elements except for the gynoecium fits the idea of a hypanthium (Leins and Erbar, 2010;Ronse De Craene, 2010). In most cases, it is impossible to prove the axial or appendicular nature of such a tube, and for this reason the morphological nature is currently not taken into account in definition of a hypanthium (Sokoloff et al., 2018). In Burmannia, the stamens are usually attached distinctly below the apex of the floral tube, and therefore only a part of the floral tube corresponds to the hypanthium (i.e., from the tube base to the level of stamen attachment). ...
Species of the genus Burmannia possess distinctive and highly elaborated flowers with prominent floral tubes that often bear large longitudinal wings. Complicated floral structure of Burmannia hampers understanding its floral evolutionary morphology and biology of the genus. In addition, information on structural features believed to be taxonomically important is lacking for some species. Here we provide an investigation of flowers and inflorescences of Burmannia based on a comprehensive sampling that included eight species with various lifestyles (autotrophic, partially mycoheterotrophic and mycoheterotrophic). We describe the diversity of inflorescence architecture in the genus: a basic (most likely, ancestral) inflorescence type is a thyrsoid comprising two cincinni, which is transformed into a botryoid in some species via reduction of the lateral cymes to single flowers. Burmannia oblonga differs from all the other studied species in having an adaxial (vs. transversal) floral prophyll. For the first time, we describe in detail early floral development in Burmannia. We report presence of the inner tepal lobes in B. oblonga, a species with reportedly absent inner tepals; the growth of the inner tepal lobes is arrested after the middle stage of floral development of this species, and therefore they are undetectable in a mature flower. Floral vasculature in Burmannia varies to reflect the variation of the size of the inner tepal lobes; in B. oblonga with the most reduced inner tepals their vascular supply is completely lost. The gynoecium consists of synascidiate, symplicate, and asymplicate zones. The symplicate zone is secondarily trilocular (except for its distal portion in some of the species) without visible traces of postgenital fusion, which prevented earlier researchers to correctly identify the zones within a definitive ovary. The placentas occupy the entire symplicate zone and a short distal portion of the synascidiate zone. Finally, we revealed an unexpected diversity of stamen-style interactions in Burmannia. In all species studied, the stamens are tightly arranged around the common style to occlude the flower entrance. However, in some species the stamens are free from the common style, whereas in the others the stamen connectives are postgenitally fused with the common style, which results in formation of a gynostegium.
... However, in particular cases, the contacting epidermal cells can dedifferentiate [11], resulting in a situation histologically indistinguishable from true congenital fusion. Taking into account all these difficulties, Sokoloff et al. [12] discriminated between perfect (when the original epidermal layers dedifferentiate) and imperfect (when separate epidermal tissues persist) types of postgenital fusion. Authors of the cited paper [12] (p. ...
... Taking into account all these difficulties, Sokoloff et al. [12] discriminated between perfect (when the original epidermal layers dedifferentiate) and imperfect (when separate epidermal tissues persist) types of postgenital fusion. Authors of the cited paper [12] (p. 18) admitted a difficulty 'to draw a clear boundary between imperfect postgenital fusion of the units and mere appression of their free surfaces' and suggested the recognition of postgenital fusion in cases 'when organs or their parts join each other and remain united by the end of all developmental processes'. ...
The vast majority of highly valuable species of the Leguminosae in temperate latitudes belong to the Inverted Repeat-Lacking Clade (IRLC). Despite having a generally conserved monosymmetric floral morphology, members of this group are remarkable with a pronounced diversity of floral sizes, modes of staminal fusion, and pollination strategies. This paper examined androecia and floral nectaries (FNs) in selected genera of the IRLC. External morphology was investigated using stereomicroscopy and scanning electron microscopy. In some cases, the pattern of staminal fusion was additionally examined in transverse sections using light microscopy. Androecia of all selected genera fell into one of four types, viz., monadelphous, pseudomonadelphous, diadelphous or diadelphous reduced (with inner stamens converted into sterile staminodes). However, there was significant variation in the stamens’ mode of contact, as well as the shape and size of the fenestrae providing access to FNs. Some types seemed to arise independently in different genera, thus providing a high level of homoplasy. FNs were more conserved and comprised areas of secretory stomata in the abaxial part of the receptacle and/or hypanthium. Nectariferous stomata could be found in very miniaturized flowers (Medicago lupulina) and could even accompany monadelphy (Galega). This indicates that preferential self-pollination may nevertheless require visitation by insects.
... Investigations of the vascular anatomy of flowers was introduced by van Tieghem (1871), and is still successfully applied in the investigation of monocots (Dyka, 2018;Novikoff & Kazemirska, 2012;Remizowa et al., 2010;Zalko & Deroin, 2018). Because of its evolutionary conservation, the floral vascular system can serve not only for direct comparison of different taxa, but also for the elucidation of fused organs and analysis of floral evolution and morphogenesis (Joshi, 1940;Novikoff & Jabbour, 2014;Nuraliev et al., 2021;Silva et al., 2016;Sokoloff et al., 2018). Similarly, the principles of the gynoecium vertical zonality were developed by Leinfellner (1950) and Baum (1952), but are still useful in solving phylogenetic and taxonomic issues, in combination with morphological and molecular data (Heigl et al., 2020;Odintsova et al., 2013;Oliveira et al., 2020;Silva et al., 2020). ...
... Interpretation of vertical zonality of syncarpous gynoecia can be complicated for many reasons, including the fusion of perigon with carpels or different levels of postgenital fusion of carpels (Sokoloff et al., 2018). Hence, it is crucial to reconstruct the primary structure of the gynoecium and determine its secondary transformations. ...
Flowers of the five species from the four sections of the genus Gagea (that is, G. lutea , G. pusilla , G. reticulata , G. fragifera , and G. serotina (syn. Lloydia serotina ) were investigated by light microscopy. All investigated species had similar flower organization, vertical zonality of the gynoecium, and floral vascularization. In all species, the flowers were trimerous, with the superior ovary and short complete or semicomplete syntepalous zone at the base. The presence of the syntepalous zone allows consideration of such flowers as an intermediate between hypogynous and perigynous.
All investigated species had nectaries at the base of the tepals. However, in Gagea s. str., they were represented by relatively small nectariferous areas of the tepals located at the beginning of the synascidiate zone of the gynoecium. In contrast, the nectaries in G. serotina were represented by elongated tepalar outgrowths located higher, at the level of the fertile symplicate zone of the gynoecium. Considering reports on the potential peltate origin of the nectaries in G. serotina , it is probably incorrect to interpret them as homologous to the nectaries in Gagea s. str.
The gynoecium in the studied species demonstrated identical vertical zonality with synascidiate, symplicate, and asymptomatic zones, and corresponded to type C of the syncarpous gynoecium. At the base of the ovary, three carpels were congenitally isolated (primary synascidiate zone); however, they were isolated only postgenitally (secondary synascidiate zone). This secondary synascidiate zone originated from a symplicate zone due to the fusion of the carpelar margins. Although it looks like a synascidiate zone, for correct interpretation of the gynoecium’s vertical structure, it should be considered symplicate.
The vascularization of the flower in all investigated species was similar, with the participation of lateral vascular bundles in the supply of placentas.
... Floral developmental studies help us to understand the ontogenetic bases that have led to key innovations in different groups of angiosperms (e.g. Endress, 2006Endress, , 2011Remizowa et al., 2010;Sokoloff et al., 2018). The floral bauplan is genetically controlled and under strong developmental constraints, but other factors can also influence development, such as available space in floral buds, size of organ primordia, timing of organ initiation and rate of organ growth (Rudall, 2010;Ronse De Craene, 2016. ...
• Background and Aims. Floral developmental studies are crucial for understanding the evolution of floral structures and sexual systems in angiosperms. Within the monocot order Poales, both subfamilies of Eriocaulaceae have unisexual flowers bearing unusual nectaries. Few previous studies have investigated floral development in subfamily Eriocauloideae, which includes the large, diverse and widespread genus Eriocaulon. To understand floral variation and the evolution of the androecium, gynoecium and floral nectaries of Eriocaulaceae, we analysed floral development and vasculature in Eriocaulon and compared it with that of subfamily Paepalanthoideae and the related family Xyridaceae in a phylogenetic context.
• Methods. Thirteen species of Eriocaulon were studied. Developmental analysis was carried out using scanning electron microscopy, and vasculature analysis was carried out using light microscopy. Fresh material was also analysed using scanning electron microscopy with a cryo function. Character evolution was reconstructed over well-resolved phylogenies.
• Key Results. Perianth reductions can occur due to delayed development that can also result in loss of the vascular bundles of the median sepals. Nectariferous petal glands cease development and remain vestigial in some species. In staminate flowers, the inner stamens can emerge before the outer ones, and carpels are transformed into nectariferous carpellodes. In pistillate flowers, stamens are reduced to staminodes and the gynoecium has dorsal stigmas.
• Conclusions. Floral morphology is highly diverse in Eriocaulon, as a result of fusion, reduction or loss of perianth parts. The nectariferous carpellodes of staminate flowers originated first in the ancestor of Eriocaulaceae; petal glands and nectariferous branches of pistillate flowers originated independently in Eriocaulaceae through transfer of function. We present a hypothesis of floral evolution for the family, illustrating a shift from bisexuality to unisexuality and the evolution of nectaries in a complex monocot family, which can contribute to future studies on reproductive biology and floral evolution in other groups.
... However, numerous elaborations have led to the extraordinary appearance of the flowers of Thismia. These include a prominent hypanthium enclosing stamens and stigmas [also called a floral tube (for terminology, see Caddick, Rudall & Wilkin, 2000;Nuraliev et al., 2014;Sokoloff et al., 2018)], a fleshy massive ring-like structure called an annulus at the top of the hypanthium bearing stamens hanging down in the hypanthium chamber, more or less long appendages of inner and/or outer tepals, a roof-like structure formed by inner tepals (a so-called mitre or a loose dome), a stamen tube resulted from postgenital fusion, long prolongations of stamen connectives, and various hairs and appendages on the stamen surface. ...
... The growing mass of tissue extends towards the floral centre, so that this process does not alter the position of the tepals on the hypanthium, but forms a structure to which the stamens are attached. Thus, the annulus fits the idea of a stamen tube (or, more precisely, a filament tube) with late congenital fusion (Erbar, 1991;Leins & Erbar, 1997Sokoloff et al., 2018). In our opinion, it would be incorrect to consider the annulus as a hypanthium outgrowth, because the hypanthium expansion never takes place between the perianth and the androecium according to the definition of the hypanthium (e.g. ...
... However, Thismiaceae differ from many other angiosperms with free-central placentas, as the true free-central placentas are attached only at the base of the locule, and not at its top (see explanation by Ickert-Bond, Gerrath & Wen, 2014). Although the free-central placenta in its strict sense develops directly from the carpel meristem and has an intact primary morphological surface, the column-like placenta cannot develop without an event of either postgenital fusion or schizogeny for geometrical reasons (Sokoloff et al., 2018). According to our results and some earlier observations (Pfeiffer, 1914;Rübsamen, 1986), in Thismia, the second type of event is found, i.e. its placentas are of a schizogenous nature. ...
Thismia is characterized by an exceptionally complicated floral morphology that is currently not understood properly. In the taxonomic literature, descriptive rather than morphological terms are often applied to parts of the flower in Thismia, relating to the general appearance of the floral organs instead of their precise homologies. Precise understanding of the floral structure is complicated by the rarity of Thismia spp. and the paucity of appropriate material. Here we provide a comprehensive study of reproductive organs of three Thismia spp. (T. annamensis, T. javanica and T. mucronata) including the first investigation of inflorescence architecture and early floral development in Thismiaceae. We found a hitherto unknown diversity of the reproductive shoots in the genus, manifested in the number of floral prophylls (two or three, in contrast to a single prophyll in the vast majority of monocots) and in the branching plane resulting in two distinct inflorescence types, a drepanium and a bostryx. We report the non-acropetal sequence of initiation of floral whorls (with stamens being the last elements to initiate), never previously described in monocots, and the gynoecium composed of completely plicate carpels, also a rare feature for monocots. Floral vasculature is relatively uniform in Thismia, but significant interspecific differences are found in tepal innervation, including the number of tepal traces; some of these differences are not immediately related to the external tepal morphology. We argue that the annulus, which acts as a roof of the hypanthium, possesses an androecium nature and represents congenitally fused bases of stamen filaments. We describe the stamens as laminar structures, which are also shortly tubular in the distal part of the supraconnective with the adaxial tubular side forming a skirt-like appendage. Finally, the placentas, which are column-like when mature, are initially parietal, becoming secondarily similar to free-central placentas through schizogenous separation from the ovary wall.
