Comparative floral development in the tribe Mentheae (Nepetoideae: Lamiaceae) and its bearing on the evolution of floral patterns in asterids

A comparative developmental study of flowers was carried out using epi-illumination light microscopy on four genera of Lamiaceae (Nepeta, Rosmarinus, Salvia, andZiziphora), representing all three subtribes of Mentheae. All species examined share unidirectional (adaxial to abaxial) sepal initiation, except Rosmarinus, which has the reverse unidirectional sequence, starting abaxially. Initiated but suppressed bracteoles were detected only in Rosmarinus. In Rosmarinus, Salvia, and Ziziphora, initiation of petals and stamens proceeds unidirectionally from the abaxial side. Floral initiation of Nepeta has bidirectional inception of petals and unidirectional stamen initiation from the adaxial side. Temporal overlap in organ initiation between petal and stamen whorls occurs in all taxa, though this feature is more prominent in Rosmarinus. Significant structural and developmental features that distinguish the four genera include: (1) polysymmetric calyx tube, highly tomentose corolla and deeply four-partitioned ovary in Nepeta; (2) monosymmetric two-lipped calyx and shallowly four-partitioned ovary in Ziziphora; and (3) suppression of adaxial stamens in Salvia and Rosmarinus. Adaxial stamens are absent from Rosmarinus, but reduced stamens remain as staminodia in Salvia. In a phylogenetic context, the late monosymmetry of Nepeta and very early monosymmetry of Rosmarinus could both be regarded as derived conditions compared with the early monosymmetry ofSalvia and Ziziphora.     

Floral organogenesis and floral evolution of the Lecythidoideae (Lecythidaceae)

The subfamily Lecythidoideae of Lecythidaceae (Brazil nut family) is a dominant group in neotropical forests, especially those of Amazonia. New World members of the family have large showy flowers that are either polysymmetric or monosymmetric. In this study, floral organogenesis of all 10 neotropical genera was examined using SEM. Our observations of floral development are put into the context of a molecular phylogeny based on sequences of the ndhF and trnL-F genes (Am. J. Bot. 94: 289-301). Floral evolution of the subfamily is explained as having undergone four different levels of complexity in regard to floral symmetry. The basal most genera, Grias and Gustavia, have polysymmetric flowers. At level two, represented only by Couroupita, monosymmetry is established through the expression of abaxial dominance and the development of an androecial hood; at this level, abaxial dominance impacts the perianth and androecium, but not the gynoecium. At the third level, monosymmetry is developed in groups of Couratari and Cariniana domestica; but, in the Allantoma/Cariniana decandra lineage, a reversal back to polysymmetric flowers, resulting from a gradual weakening of abaxial dominance, and the loss of the hood has occurred. Finally, in level four, including Bertholletia, Corythophora, Eschweilera, and Lecythis, monosymmetry is so strongly expressed that the gynoecium is also influenced by abaxial dominance. In this group, the hood is complicated in both structure and function, and the floral axis is changed from straight to slightly inclined. This study demonstrates that the development of floral abaxial dominance is the proximate cause of monosymmetry in the Lecythidoideae. We suggest that monosymmetric flowers are more efficiently pollinated, and therefore the bees and bats that pollinate the monosymmetric flowers in this group are ultimately responsible for the monosymmetry.     

Flower ontogeny in Capparis spinosa (Capparaceae) with special emphasis on symmetry expression

The flower ontogeny of Capparis spinosa L. was studied using scanning electron microscopy (SEM) in order to shed light on the early expression of symmetry in a representative member of Capparaceae. Sepals start decussately with the abaxial and adaxial sepals, followed by the lateral ones. Petal appearance proceeds uni‐directionally from the abaxial to the adaxial side. Stamens develop centrifugally on an androecial ring. Five to seven carpel lobes arise on a gynoecial ring. Monosymmetry is established in early development by the uni‐directional petal appearance and is further enhanced by the acquisition of an abaxial nectary appendage and differential development of perianth organs at anthesis. The early monosymmetric pattern found in C. spinosa differs from the early monosymmetric and early disymmetric pathways of Cleomoideae. Our findings are consistent with the hypothesis that the late establishment of monosymmetry is a reflective of symmetry in early development.     

Evolution of perianth and stamen characteristics with respect to floral symmetry in Ranunculales

BACKGROUND AND AIMS: Floral symmetry presents two main states in angiosperms, namely polysymmetry and monosymmetry. Monosymmetry is thought to have evolved several times independently from polysymmetry, possibly in co-adaptation with specialized pollinators. Monosymmetry commonly refers to the perianth, even though associated androecium modifications have been reported. The evolution of perianth symmetry is examined with respect to traits of flower architecture in the Ranunculales, the sister group to all other eudicots, which present a large diversity of floral forms. METHODS: Characters considered were perianth merism, calyx, corolla and androecium symmetry, number of stamens and spurs. Character evolution was optimized on a composite phylogenetic tree of Ranunculales using maximum parsimony. KEY RESULTS: The ancestral state for merism could not be inferred because the basalmost Eupteleaceae lack a perianth and have a variable number of stamens. The Papaveraceae are dimerous, and the five other families share a common trimerous ancestor. Shifts from trimery to dimery (or reverse) are observed. Pentamery evolved in Ranunculaceae. Ranunculales except Eupteleaceae, present a polysymmetric ancestral state. Monosymmetry evolved once within Papaveraceae, Ranunculaceae and Menispermaceae (female flowers only). Oligandry is the ancestral state for all Ranunculales, and polyandry evolved several times independently, in Papaveraceae, Menispermaceae, Berberidaceae and Ranunculaceae, with two reversions to oligandry in the latter. The ancestral state for androecium symmetry is ambiguous for the Ranunculales, while polysymmetry evolved immediately after the divergence of Eupteleaceae. A disymmetric androecium evolved in Papaveraceae. The ancestral state for spurs is none. Multiple spurs evolved in Papaveraceae, Berberidaceae and Ranunculaceae, and single spurs occur in Papaveraceae and Ranunculaceae. CONCLUSIONS: The evolution of symmetry appears disconnected from changes in merism and stamen number, although monosymmetry never evolved in the context of an open ground plan. In bisexual species, monosymmetry evolved coincidently with single spurs, allowing us to propose an evolutionary scenario for Papaveraceae.     

The Immense Diversity of Floral Monosymmetry and Asymmetry Across Angiosperms

Floral monosymmetry and asymmetry are traced through the angiosperm orders and families. Both are diverse and widespread in angiosperms. The systematic distribution of the different forms of monosymmetry and asymmetry indicates that both evolved numerous times. Elaborate forms occur in highly synorganized flowers. Less elaborate forms occur by curvature of organs and by simplicity with minimal organ numbers. Elaborate forms of asymmetry evolved from elaborate monosymmetry. Less elaborate form come about by curvature or torsion of organs, by imbricate aestivation of perianth organs, or also by simplicity. Floral monosymmetry appears to be a key innovation in some groups (e.g., Orchidaceae, Fabaceae, Lamiales), but not in others. Floral asymmetry appears as a key innovation in Phaseoleae (Fabaceae). Simple patterns of monosymmetry appear easily “reverted” to polysymmetry, whereas elaborate monosymmetry is difficult to lose without disruption of floral function (e.g., Orchidaceae). Monosymmetry and asymmetry can be expressed at different stages of floral (and fruit) development and may be transient in some taxa. The two symmetries are most common in bee-pollinated flowers, and appear to be especially prone to develop in some specialized biological situations: monosymmetry, e.g., with buzz-pollinated flowers or with oil flowers, and asymmetry also with buzz-pollinated flowers, both based on the particular collection mechanisms by the pollinating bees. Floral monosymmetry has developed into a model trait in evo-devo studies, whereas floral asymmetry to date has not been tackled in molecular genetic studies.     

Evolutionary correlation between floral monosymmetry and corolla pigmentation patterns in <Emphasis Type="Italic">Rhododendron</Emphasis>

Floral symmetry and pigmentation are features of flowers that are believed to be associated due to their shared influence on pollinator behaviour. However, the evolution of such associations has so far not been examined. We analysed variation in Rhododendron flowers, in a phylogenetic context, to test whether the evolution of floral symmetry types and pigment patterns are correlated. Variation in floral symmetry due to variation in corolla form, stamen flexion, stamen arrangement, pistil flexion, as well as corolla pigment patterns was documented in 98 species of Rhododendron. Phylogenetic relations among these species were estimated using maximum likelihood (ML) and Bayesian methods, building on a published molecular dataset of sequences of RNA Polymerase II subunit (RPB2-I). Evolution of the floral traits was studied using phylogenetic correlation tests and ancestral state reconstructions (maximum parsimony, MP and ML methods). Significant correlations were found between corolla pigment pattern and type of floral symmetry at the level of corolla form, stamen flexion or arrangement, and pistil flexion. As expected from their similar roles in enhancing attractability to pollinator, monosymmetric corollas and presence of pigment pattern are correlated; in addition, monosymmetry involving other whorls too shows such a relationship with pigment patterns, and with each other. Multiple evolutionary shifts were detected between monosymmetry and polysymmetry of floral traits in Rhododendron. The relationship between floral monosymmetry attributes and presence of corolla pigment patterns, and additionally, frequent evolutionary shifts in these traits suggest pollinator-mediated selective pressures in Rhododendron.     

Phylogenetic relationships within Senna (Leguminosae, Cassiinae) based on three chloroplast DNA regions: patterns in the evolution of floral symmetry and extrafloral nectaries

Senna (Leguminosae) is a large, widespread genus that includes species with enantiostylous, asymmetric flowers and species with extrafloral nectaries. Clarification of phylogenetic relationships within Senna based on parsimony analyses of three chloroplast regions (rpS16, rpL16, and matK) provides new insights on the evolution of floral symmetry and extrafloral nectaries. Our results support the monophyly of only one (Psilorhegma) of the six currently recognized sections, while Chamaefistula, Peiranisia, and Senna are paraphyletic, and monotypic Astroites and Paradictyon are nested within two of the seven major clades identified by our molecular phylogeny. Two clades (I, VII) include only species with monosymmetric flowers, while the remaining clades (II-VI) contain species with asymmetric, enantiostylous flowers, in which either the gynoecium alone or, in addition, corolla and androecium variously contribute to the asymmetry. Our results further suggest that flowers were ancestrally monosymmetric with seven fertile stamens and three adaxial staminodes, switched to asymmetry later, and reverted to monosymmetry in clade VII. Fertility of all 10 stamens is a derived state, characterizing the Psilorhegma subclade. Extrafloral nectaries evolved once and constitute a synapomorphy for clades IV-VII ("EFN clade"). These nectaries may represent a key innovation in plant defense strategies that enabled Senna to undergo large-scale diversification.     

Comparative floral development in Lamioideae (Lamiaceae): Marrubium,Phlomis, and Stachys

A comparative study of floral ontogeny and development was carried out on three genera (Marrubium L., Phlomis L., Stachys L.), representing three tribes of Lamioideae (Marrubieae, Phlomideae, Stachydeae) using epi-illumination light microscopy. The sequence of organ whorl appearance in all three genera is sepals, petals plus stamens, and carpels. Sepal appearance is reversed unidirectional starting from the adaxial side in all except Phlomis, which is unidirectional. Order of petal appearance is bidirectional in Marrubium and Stachys, and simultaneous in Phlomis. Stamens appear unidirectionally starting from the adaxial side in all except in Phlomis, which has an abaxial to adaxial unidirectional sequence. Significant developmental features distinguishing the three genera from each other include (1) weakly monosymmetric, elongated calyx tube, five-lobed corolla, divergent anthers with thecae transverse to the filament, unequally bifid stigma and ovary with glandular hairs in Marrubium; (2) actinomorphic hairy calyx, four-lobed corolla and unequally bifid stigma in Phlomis; and (3) glabrous calyx, equally bifid stigma and symmetric disc nectary in Stachys. Our results indicate some potential for floral ontogenetic features in delimiting the different tribes. The hypothetical evolutionary pathway of organogenesis sequences is discussed.     

Floral Morphology and Organogenesis in Tinantia pringlei, Along with a Review of Floral Developmental Variation in the Spiderwort Family, Commelinaceae

Floral organogenesis had previously been investigated thoroughly in 11 species from three of nine subtribes or their equivalent in the Commelinaceae. Here flower morphology and development is described from a member of a fourth subtribe, Tinantia pringlei from the Thyrsantheminae, and comparisons are made. Although the calyx is only weakly monosymmetric at maturity, development is of the monosymmetric-type known from or resembling that of the monosymmetric flowers of Cochliostema, Dichorisandra, and Plowmanianthus (subtribe Dichorisandrinae; tribe Tradescantieae) and Commelina (tribe Commelineae). Whereas the corolla also is weakly monosymmetric at maturity, development is of the polysymmetric-type known from the polysymmetric flowers of Callisia, Gibasis, and Tradescantia (subtribe Tradescantiinae). In the androecium, the long, inconspicuous blue stamens of the lower floral hemisphere emerge first during development, while the shorter, showy yellow, upper stamens emerge last. The overall pattern of stamen development is centripetal, thereby resembling that reported for the majority of confamilial taxa, and contrasting with the centrifugal pattern known from Callisia and Tradescantia. Relative to the majority of confamilial taxa investigated, the carpels emerge relatively late in development, resembling the timing known for the carpels of Callisia and Tradescantia. Overall, however, carpel emergence in Tinantia pringlei is unique in the comparatively small size of the remnant floral apical primordium on which the carpels emerge. Other variations in floral development are discussed and further such studies within the family are encouraged based on the potential for using such developmental variations in the assessment of morphological homologies and phylogenetic relationships within the Commelinaceae.     

Comparative inflorescence and floral ontogeny in the genus Mentha (Mentheae: Nepetoideae: Lamiaceae): variable sequences of organ appearance and random petal aestivation

The genus Mentha is a taxonomically complex genus, characterized by large morphological variations. Only a few, frequently overlapping, characters are of value in taxonomy. Comparative floral developmental studies provide an opportunity for better understanding the systematic relationships among different species. The inflorescence and floral ontogeny of three Mentha L. species (M. piperita L., M. pulegium L. and M. suaveolens Ehrh.) were investigated using epi-illumination light microscopy. All three species studied have thyrses with the same developmental pathway. The lack of higher order bracts and the monochasial branching of the higher order inflorescence apices were found as special features of inflorescence ontogeny. Sepals appear unidirectionally from the adaxial side in all except for M. pulegium which shows a modified unidirectional sequence. Variable sequences of petal and stamen appearance from unidirectional to reversed unidirectional sequence are present in all. Significant ontogenetic features include (1) appearance of the corolla as a rim before petal lobes become visible and (2) instability in petal aestivation. Morphological features including densely hairy calyx, five-lobed corolla tube, smaller adaxial stamens and hairy ovary with included style distinguish M. pulegium from the other species. On the basis of our results floral ontogenetic features could be considered important characters for delimiting or diagnosing different sections in the genus Mentha. Variable sequences of petal lobe appearance and instability in petal aestivation were found as unusual developmental characters.     

马先蒿属花冠无喙类的花器官发生

对花冠无喙类密穗马先蒿(Pedicularis densispica)和大王马先蒿(P．rex)的花器官电镜扫描发现,两种不同花冠型(无齿和具齿)的马先蒿花部器官发生和发育初期十分相似,表现为明显的单轴对称。2个萼片原基首先发生于花顶的近轴侧位,然后沿花顶边缘向远轴端发育形成--马蹄形结构。密穗马先蒿在近轴中部又出现1枚萼片原基,随后马蹄形结构分化出4枚萼片,并与近轴中部的原基愈合后构成5齿萼片;而大王马先蒿的2齿萼片直接由马蹄形结构发育而成。5枚独立的花瓣原基随后发生,但发育相对滞后;除近轴中部位置1枚空缺外,4枚雄蕊原基与花瓣原基位置呈交互发生;2个心皮原基同时在拱形花顶的近轴和远轴端发生,剩余的花顶形成中间的隔膜,并与2个心皮形成中轴胎座。对马先蒿与金鱼草(Antirrhinum majus)和毛地黄(Digitalis purpurea)花器官发生和发育初期的特征进行了比较,讨论了马先蒿属花冠对称性变化的意义。     

苦苣苔科大叶石上莲CYC类基因RT-PCR表达模式研究

CYC类基因的分子系统学研究已经在苦苣苔科Gesneriaceae中展开,但是还缺乏对这些基因表达和功能的研究。因此,我们选择苦苣苔科大叶石上莲Oreocharis benthamii作为实验材料,分离出了CYC类基因的两个拷贝,经过分子系统学分析这两个基因分别属于苦苣苔科GCYC1和GCYC2两个分支,故命名为ObCYC1和ObCYC2。分区的RT-PCR实验结果显示这两个基因拥有不同的时间空间表达模式。ObCYC1与模式植物金鱼草Antirrhinum majus中的CYC基因类似,集中在花冠背部区域表达,这与它们拥有保守的功能区TCP和R相一致。但是,ObCYC1与CYC表达模式仍有区别,即,和CYC相比ObCYC1在花冠背部区域的表达提前减弱。这可能和大叶石上莲花冠微弱的两侧对称性相关。另外,由于大叶石上莲的背部花瓣较两侧和腹部花瓣小,因此,在功能上ObCYC1可能起抑制背部花瓣生长作用而CYC基因则促进背部花瓣生长。与ObCYC1不同,ObCYC2的保守功能区有更多的氨基酸位点变化,而且在RT-PCR实验中也没有检测到它的表达。因此,需要开展更深入的实验研究分析ObCYC2的基本功能,这将有助于了解GCYC2类基因在苦苣苔科及其近缘科中的功能和进化途径。     

Roles of synorganisation,zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots

A gynostemium, comprising stamen filaments adnate to a syncarpous style, occurs in only threc groups of monocots: the large family Orchidaceae (Asparagales) and two small genera Pauridia (Hypoxidaceae: Asparagales) and Corsia (Corsiaceae, probably in Liliales), all epigynous taxa. Pauridia has actinomorphic (polysymmetric) flowers, whereas those of Corsia and most orchids are strongly zygomorphic (monosymmetric) with a well-differentiated labellum. In Corsia the labellum is formed from the outer median tepal (sepal), whereas in orchids it is formed from the inner median tepal (petal) and is developmentally adaxial (but positionally abaxial in orchids with resupinate flowers). Furthermore, in orchids zygomorphy is also expressed in the stamen whorls, in contrast to Corsia. In Pauridia a complete stamen whorl is suppressed, but the 'lost' outer whorl is fused to the style. The evolution of adnation and zygomorphy are discussed in the context of the existing phylogenetic framework in monocotyledons. An arguably typological classification of floral terata is presented, focusing on three contrasting modes each of peloria and pseudopeloria. Dynamic evolutionary transitions in floral morphology are assigned to recently revised concepts of heterotopy (including homeosis) and heterochrony, seeking patterns that delimit developmental constraints and allow inferences regarding underlying genetic controls. Current evidence suggests that lateral heterotopy is more frequent than acropetal heterotopy, and that full basipetal heterotopy does not occur. Pseudopeloria is more likely to generate a radically altered yet functional perianth, but is also more likely to cause acropetal modification of the gynostemium. These comparisons indicate that there are at least two key genes or sets of genes controlling adnation, adaxial stamen suppression and labellum development in lilioid monocots; at least one is responsible for stamen adnation to the style (i.e. gynostemium formation), and another controls adaxial stamen suppression and adaxial labellum formation in orchids. Stamen adnation to the style may be a product of over-expression of the genes related to epigyny (i.e. a form of hyper-epigyny). If, as seems likely, stamen-style adnation preceded zygomorphy in orchid evolution, then the flowers of Pauridia may closely resemble those of the immediate ancestors of Orchidaceae, although existing molecular phylogenetic data indicate that a sister-group relationship is unlikely. The initial radiation in Orchidaceae can be attributed to the combination of hyper-epigyny, zygomorphy and resupination, but later radiations at lower taxonomic levels that generated the remarkable species richness of subfamilies Orchidoideae and Epidendroideae are more likely to reflect more subtle innovations that directly influence pollinator specificity, such as the development of stalked pollinaria and heavily marked and/or spur-bearing labella.     

Corolla tube formation in four species of solanaceae

Corolla tube formation inSolanum nigrum, Salpichroa rhomboidea, Datura stramonium var.chalybea andNicotiana tabacum cv. Xanthi nc was investigated anatomically. InSolanum, the formation of the lower portion of the corolla tube, including the portion below the stamen insertion and the inserted zones, begins with the extension of the bases of the petal primordia toward the interprimordial regions. The extension of the petal bases is caused by the successive incorporation of the interprimordial regions just beside the bases into the petal primordia by means of the upward growth at those regions. The extending petal bases reach the lower portions of stamen primordia and connect with them resulting in formation of a short tube, which later develops into the lower portion of a corolla tube accompanied by epipetalous stamens. The petal bases extend further, and connect with each other outside the stamen primordia. The upward growth occurs also at the connected regions resulting in formation of the upper portion of a corolla tube. Marginal meristems of the petal primordium differentiate not later than the connection of petal bases. After the connection, marginal meristems and meristems of connected regions become continuous with each other and develop in a similar pattern. In the other three species, the corolla tube is formed in a similar manner as in the species mentioned above. However, the connection of the petal primordia occurs much earlier than the differentiation of their marginal meristems. InSalpichroa andNicotiana, the developmental patterns of the connected region and the corolla lobe margin are different.     

'Living stones' reveal alternative petal identity programs within the core eudicots

Petals, defined as the showy laminar floral organs in the second floral whorl, have been shown to be under similar genetic control in distantly related core eudicot model organisms. On the basis of these findings, it is commonly assumed that the petal identity program regulated by B-class MADS-box gene homologs is invariant across the core eudicot clade. However, the core eudicots, which comprise >70% of angiosperm species, exhibit numerous instances of petal and sepal loss, transference of petal function between floral whorls, and recurrent petal evolution. In the face of these complex patterns of perianth evolution, the concept of a core eudicot petal identity program has not been tested. We therefore examined the petal identity program in the Caryophyllales, a core eudicot clade in which perianth differentiation into sepals and petals has evolved multiple times. Specifically, we analyzed the expression patterns of B- and C-class MADS-box homologs for evidence of a conserved petal identity program between sepal-derived and stamen-derived petaloid organs in the 'living stone' family Aizoaceae. We found that neither sepal-derived nor stamen-derived petaloid organs exhibit gene expression patterns consistent with the core eudicot petal identity program. B-class gene homologs are not expressed during the development of sepal-derived petals and are not implicated in petal identity in stamen-derived petals, as their transient expression coincides with early expression of the C-class homolog. We therefore provide evidence for petal development that is independent of B-class genes and suggest that different genetic control of petal identity has evolved within this lineage of core eudicots. These findings call for a more comprehensive understanding of perianth variation and its genetic causes within the core eudicots--an endeavor that will have broader implications for the interpretation of perianth evolution across angiosperms.     

Floral Developmental Evidence for the Systematic Relationships of Tropaeolum(Tropaeolaceae)

The floral ontogeny of three species of Tropaeolum was studiedusing scanning electron microscopy to find morphological evidencefor discussing the systematic position of the family. The initiationof the androecium is highly unusual: there are always eightstamens which arise (1) either in a spiral sequence startingwith the stamen opposite sepal four, running in a directionopposite to the sequence of the sepals, and with reversals inthe direction of the spiral, or (2) as a sequence of pairedand unpaired stamens. The floral symmetry changes twice duringthe development of the flower, from polysymmetrical at sepaland petal initiation, through oblique monosymmetry at stameninitiation, and ending with median monosymmetry in later developmentalstages. The occurrence of median monosymmetry is a late-developmentalevent and is caused by the initiation of a hypanthial spur,and the unequal growth of the petals and styles. The originfor the unusual sequence of stamen initiation reflects a trendaffecting the whole flower which is linked with the changingpatterns of floral symmetry. Octandry is enhanced by multiplecauses, such as the loss of two stamens in an originally diplostemonousandroecium and the regulating pressure of the gynoecium. Thechange in symmetry during ontogeny is significant for discussingthe systematic position of Tropaeolaceae in comparison withthe glucosinolate-producing taxa and the Sapindales. The combinationof an androecium with eight stamens and oblique monosymmetryis either a single event in evolution and links Tropaeolum withthe Sapindales, or it has evolved at least twice, once in theSapindales, and once in a clade comprising Tropaeolaceae, Akaniaceaeand Bretschneideraceae. Morphological data support a sistergroup relationship of the three latter families, which is inline with macromolecular studies. Copyright 2001 Annals of BotanyCompany Tropaeolum, Tropaeolaceae, Glucosinolate clade, Sapindales, oblique monosymmetry, androecium, octandry, floral development, phylogeny