Ontogenetic origins of floral bilateral symmetry in Moringaceae (Brassicales)

Floral morphology of the 13 species of Moringa ranges from actinomorphic flowers with little hypanthium to highly zygomorphic flowers with well-developed hypanthia. Scanning electron and light microscopy were used to identify ontogenetic differences among two actinomorphic and eight zygomorphic species. All species show traces of zygomorphy between petal organogenesis and anther differentiation. At late organogenesis, zygomorphy is manifest by one petal being larger than the others, slight unidirectional maturation of the anthers, and in many species, some staminodes may be missing. At organ differentiation and beyond, the actinomorphic species show a trend toward increasing actinomorphy, whereas the zygomorphic features of early ontogeny are progressively accentuated throughout the ontogeny of the zygomorphic species. Because of the early traces of zygomorphy throughout the family, ontogeny in Moringa does not resemble that known from the sister taxon Caricaceae, which has flowers that are actinomorphic throughout ontogeny. Great intraspecific variation was found in floral plan in the actinomorphic-flowered species in contrast to the zygomorphic species. Each of the main clades in the family is distinguished by at least one feature of floral ontogeny. In general, ontogenetic differences that are congruent with deeper phylogenetic splits tend to occur earlier in ontogeny than those congruent with more recent divergences.     

The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention

Stamens that have lost their primary function of pollen production, or staminodes, occur uncommonly within angiosperms, but frequently fulfill important secondary floral functions. The phylogenetic distribution of staminodes suggests that they typically arise during evolutionary reduction of the androecium. Differences in the genetic control and patterns of stamen loss between actinomorphic and zygomorphic flowers shape staminode development. In clades with actinomorphic flowers, staminodes generally replace an entire stamen whorl and staminode loss seems irreversible. In contrast, in clades with zygomorphic flowers staminodes evolve from a subset of the stamens in a whorl and staminodes can reappear in a lineage after being lost (e.g., Cheloneae, Scrophulariaceae). If staminodes do not adopt new functions during androecium reduction they are lost quickly, so that nonfunctional staminodes appear only in recently derived taxa. Alternatively, when staminodes assume new floral roles, either directly or indirectly after a nonfunctional period, they can become integral floral components which perpetuate within clades (e.g., Orchidaceae). Indirect evolution of staminode function allows greater flexibility of function by allowing staminodes to take over roles not performed by stamens, such as involvement in mechanisms to prevent self-pollination and mechanisms of explosive pollination. Multifunctional staminodes characterize lineages with universal or widespread staminodes.     

Natural selection on Erysimum mediohispanicum flower shape: insights into the evolution of zygomorphy

Paleontological and phylogenetic studies have shown that floral zygomorphy (bilateral symmetry) has evolved independently in several plant groups from actinomorphic (radially symmetric) ancestors as a consequence of strong selection exerted by specialized pollinators. Most studies focused on unraveling the developmental genetics of flower symmetry, but little is known about the adaptive significance of intraspecific flower shape variation under natural conditions. We provide the first evidence for natural selection favoring zygomorphy in a wild population of Erysimum mediohispanicum (Brassicaceae), a plant showing extensive continuous variation in flower shape, ranging from actinomorphic to zygomorphic flowers. By using geometric morphometric tools to describe flower shape, we demonstrate that plants bearing zygomorphic flowers received more pollinator visits and had the highest fitness, measured not only by the number of seeds produced per plant but also by the number of seeds surviving to the juvenile stage. This study provides strong evidence for the existence of significant fitness differences associated with floral shape variation in E. mediohispanicum, thus illuminating a pathway for the evolution of zygomorphy in natural populations.     

Floral zygomorphy, the recurring evolution of a successful trait

The flowers of the primitive angiosperm plants were radially symmetrical (actinomorphic). Flowers with bilateral symmetry (zygomorphic) evolved in several clades independently as an adaptation to specialized methods of pollination and played an important role in the diversification of flowering plants. In the model species Antirrhinum majus (snapdragon), the related genes CYCLOIDEA (CYC) and DICHOTOMA (DICH) are key in the development of this trait. This raises the question of whether they played a role in the evolution of floral bilateral symmetry. To address this, the evolution of CYC in relation to the evolution of zygomorphy is being investigated. Phylogenetic and functional analyses of CYC-like genes are being carried out in groups either closely related to Antirhinum or in families where zygomorphy evolved as an independent event. In addition, the origin of zygomorphy is being studied by comparing the function of CYC-like genes in species with zygomorphic flowers with their function in species with radially symmetrical flowers.     

Support for the predictions of the pollinator-mediated stabilizing selection hypothesis

Aims Floral traits are frequently used in traditional plant systematics because of their assumed constancy. One potential reason for the apparent constancy of flower size is that effective pollen transfer between flowers depends on the accuracy of the physical fit between the flower and pollinator. Therefore, flowers are likely to be under stronger stabilizing selection for uniform size than vegetative plant parts. Moreover, as predicted by the pollinator-mediated stabilizing selection (PMSS) hypothesis, an accurate fit between flowers and their pollinators is likely to be more important for specialized pollination systems as found in many species with bilaterally symmetric (zygomorphic) flowers than for species with radially symmetric (actinomorphic) flowers.Methods In a comparative study of 15 zygomorphic and 13 actinomorphic species in Switzerland, we tested whether variation in flower size, among and within individuals, is smaller than variation in leaf size and whether variation in flower size is smaller in zygomorphic compared to actinomorphic species.Important findings Indeed, variation in leaf length was significantly larger than variation in flower length and width. Within-individual variation in flower and leaf sizes did not differ significantly between zygomorphic and actinomorphic species. In line with the predictions of the PMSS, among-individual variation in flower length and flower width was significantly smaller for zygomorphic species than for actinomorphic species, while the two groups did not differ in leaf length variation. This suggests that plants with zygomorphic flowers have undergone stronger selection for uniform flowers than plants with actinomorphic flowers. This supports that the relative uniformity of flowers compared to vegetative structures within species, as already observed in traditional plant systematics, is, at least in part, a consequence of the requirement for effective pollination.     

Floral development and evolution of capitulum structure in Anacyclus (Anthemideae,Asteraceae)

Background and Aims

Most of the diversity in the pseudanthia of Asteraceae is based on the differential symmetry and sexuality of its flowers. In Anacyclus, where there are (1) homogamous capitula, with bisexual, mainly actinomorphic and pentamerous flowers; and (2) heterogamous capitula, with peripheral zygomorphic, trimerous and long-/short-rayed female flowers, the floral ontogeny was investigated to infer their origin.

Methods

Floral morphology and ontogeny were studied using scanning electron microscope and light microscope techniques

Key Results

Disc flowers, subtended by paleae, initiate acropetally. Perianth and androecium initiation is unidirectional/simultaneous. Late zygomorphy occurs by enlargement of the adaxial perianth lobes. In contrast, ray flowers, subtended by involucral bracts, initiate after the proximal disc buds, breaking the inflorescence acropetal pattern. Early zygomorphy is manifested through the fusion of the lateral and abaxial perianth lobes and the arrest of the adaxials. We report atypical phenotypes with peripheral ‘trumpet’ flowers from natural populations. The peripheral ‘trumpet’ buds initiate after disc flowers, but maintain an actinomorphic perianth. All phenotypes are compared and interpreted in the context of alternative scenarios for the origin of the capitulum and the perianth identity.

Conclusions

Homogamous inflorescences display a uniform floral morphology and development, whereas the peripheral buds in heterogamous capitula display remarkable plasticity. Disc and ray flowers follow different floral developmental pathways. Peripheral zygomorphic flowers initiate after the proximal actinomorphic disc flowers, behaving as lateral independent units of the pseudanthial disc from inception. The perianth and the androecium are the most variable whorls across the different types of flowers, but their changes are not correlated. Lack of homology between hypanthial appendages and a calyx, and the perianth double-sided structure are discussed for Anacyclus together with potential causes of its ray flower plasticity.     

Additional notes on the floral biology of neotropical Lecythidaceae

Observations on the floral biology of seven species of New World Lecythidaceae, including the first report of bat pollination for neotropical members of the family, are presented. The shift from actinomorphic flowers with many stamens to zygomorphic flowers with fewer stamens and the concomitant change from pollen to nectar as the pollinator reward are discussed and related to the respective pollinators. Several mechanisms which operate to reduce competition for pollinators between sympatric species of the family are suggested.     

The influence of floral symmetry,dependence on pollinators and pollination generalization on flower size variation

Background and Aims

The pollinator-mediated stabilizing selection hypothesis suggests that the specialized pollination system of zygomorphic flowers might cause stabilizing selection, reducing their flower size variation compared with actinomorphic flowers. However, the degree of ecological generalization and of dependence on pollinators varies greatly among species of both flower symmetry types and this may also affect flower size variation.

Methods

Data on 43 species from two contrasting communities (one alpine and one lowland community) were used to test the relationships and interactions between flower size phenotypic variation, floral symmetry, ecological pollination generalization and species'' dependence on pollinators.

Key Results

Contrary to what was expected, higher flower size variation was found in zygomorphic than in actinomorphic species in the lowland community, and no difference in flower size variation was found between symmetry types in the alpine community. The relationship between floral symmetry and flower size variation depended on ecological generalization and species'' dependence on pollinators, although the influence of ecological generalization was only detected in the alpine community. Zygomorphic species that were highly dependent on pollinators and that were ecologically specialized were less variable in flower size than ecologically generalist and selfing zygomorphic species, supporting the pollinator-mediated stabilizing selection hypothesis. However, these relationships were not found in actinomorphic species, probably because they are not dependent on any particular pollinator for efficient pollination and therefore their flower size always shows moderate levels of variation.

Conclusions

The study suggests that the relationship between flower size variation and floral symmetry may be influenced by population-dependent factors, such as ecological generalization and species'' dependence on pollinators.     

大叶铁线莲大小孢子发生及雌雄配子体发育

铁线莲属植物在花部形态和结构方面存在较大差异, 遗传背景相对复杂。因此, 在杂交育种前对其进行胚胎学研究具有重要意义。利用石蜡切片技术对大叶铁线莲(Clematis heracleifolia)大小孢子发生及雌雄配子体发育过程进行研究, 结果显示, 大叶铁线莲具雄株和两性花植株。雄花中, 雄配子体发育偶见败育现象; 而两性花中多数花粉发育异常, 形成功能性雌花。正常发育的两性花中, 雄蕊较雌蕊先发育完全。花药4室, 具腺质绒毡层, 偶见变形绒毡层。胞质分裂为同时型, 以四面体型四分体为主, 偶见左右对称型。成熟花药中, 花药壁由纤维状加厚的表皮及药室内壁构成, 花粉粒为2-细胞型, 近球状, 散沟型。子房1室, 内含少量退化胚珠及1个发育正常的胚珠, 倒生, 单珠被, 薄珠心, 蓼型胚囊, 具线形大孢子四分体及双核反足细胞。大叶铁线莲可能处于相对进化的过渡地位。在杂交育种中, 建议以雄花植株作为父本, 两性花植株仅用作母本; 在两性花花芽大小为0.5-0.8 cm时进行去雄处理。     

辣椒R2R3-MYB转录因子家族的全基因组鉴定与比较进化分析

MYB转录因子作为植物中最大的转录因子家族之一,参与植物的生长、代谢、抵御生物和非生物胁迫等多种生理生化过程。R2R3-MYB是MYB转录因子家族的主要存在形式。辣椒是具有重要经济价值的蔬菜作物,其R2R3-MYB转录因子缺乏系统的研究。从一年生辣椒(Capsicum annuum)、浆果状辣椒(C. baccatum...     

Evolution of flower shape in <Emphasis Type="Italic">Plantago lanceolata</Emphasis>

Plantago lanceolata produces small actinomorphic (radially symmetric), wind-pollinated flowers that have evolved from a zygomorphic, biotically pollinated ancestral state. To understand the developmental mechanisms that might underlie this change in flower shape, and associated change in pollination syndrome, we analyzed the role of CYC-like genes in P. lanceolata. Related zygomorphic species have two CYC-like genes that are expressed asymmetrically in the dorsal region of young floral meristems and in developing flowers, where they affect the rate of development of dorsal petals and stamens. Plantago has a single CYC-like gene (PlCYC) that is not expressed in early floral meristems and there is no apparent asymmetry in the pattern of PlCYC expression during later flower development. Thus, the evolution of actinomorphy in Plantago correlates with loss of dorsal-specific CYC-like gene function. PlCYC is expressed in the inflorescence stem, in pedicels, and relatively late in stamen development, suggesting a novel role for PlCYC in compacting the inflorescence and retarding stamen elongation in this wind pollinated species.     

Altered expression patterns of TCP and MYB genes relating to the floral developmental transition from initial zygomorphy to actinomorphy in Bournea (Gesneriaceae)

The shift from zygomorphy to actinomorphy has been intensively studied in molecular genetic model organisms. However, it is still a key challenge to explain the great morphological diversity of derived actinomorphy in angiosperms, since different underlying mechanisms may be responsible for similar external morphologies. Bournea (Gesneriaceae) is of particular interest in addressing this question, as it is a representative of primarily derived actinomorphy characteristic of a unique developmental transition from zygomorphy to actinomorphic flowers at anthesis. Using RNA in situ hybridization, the expression patterns were investigated of three different Bournea orthologues of TCP and MYB genes that have been shown to control floral symmetry in model species. Here, it is shown that the initial zygomorphic pattern in Bournea is likely a residual zygomorphy resulting from conserved expression of the adaxial (dorsal) identity gene BlCYC1. As a key novel event, the late downregulation of BlCYC1 and BlRAD and the correlative changes in the late specific expression of the abaxial (ventral) identity gene BlDIV should be responsible for the origin of the derived actinomorphy in Bournea. These results further indicate that there might be diverse pathways in the origin and evolution of derived actinomorphy through modifications of pre-existing zygomorphic developmental programs under dynamics of regulatory networks.     

Evolutionary change in flowers and inflorescences: evidence from naturally occurring terata

Records of naturally occurring, heritable floral abnormalities considerably enhance our understanding of floral evolution. Peloric mutants, frequent in natural populations of orchids and mints, have radially symmetric flowers but occur in species characterized by bilaterally symmetric flowers. Three distributions of peloric flowers across an inflorescence are: (1) complete (all flowers peloric, as in the cycloidea mutant of Antirrhinum), (2) scattered (with both peloric and zygomorphic flowers, as in the epigenetic cycloidea mutant of Linaria), and (3) terminal (only the terminal flower peloric, as in the centroradialis mutant of Antirrhinum). Genetic relationships between lateral and terminal peloria, and between peloric and pseudopeloric flowers, remain ambiguous. Complete peloria probably caused occasional evolutionary reversals from zygomorphy to actinomorphy, whereas the 'terminal-flower effect' is a less likely cause of floral evolution.     

Zygomorphy evolved from disymmetry in Fumarioideae (Papaveraceae,Ranunculales): new evidence from an expanded molecular phylogenetic framework

Background and Aims Fumarioideae (20 genera, 593 species) is a clade of Papaveraceae (Ranunculales) characterized by flowers that are either disymmetric (i.e. two perpendicular planes of bilateral symmetry) or zygomorphic (i.e. one plane of bilateral symmetry). In contrast, the other subfamily of Papaveraceae, Papaveroideae (23 genera, 230 species), has actinomorphic flowers (i.e. more than two planes of symmetry). Understanding of the evolution of floral symmetry in this clade has so far been limited by the lack of a reliable phylogenetic framework. Pteridophyllum (one species) shares similarities with Fumarioideae but has actinomorphic flowers, and the relationships among Pteridophyllum, Papaveroideae and Fumarioideae have remained unclear. This study reassesses the evolution of floral symmetry in Papaveraceae based on new molecular phylogenetic analyses of the family.Methods Maximum likelihood, Bayesian and maximum parsimony phylogenetic analyses of Papaveraceae were conducted using six plastid markers and one nuclear marker, sampling Pteridophyllum, 18 (90 %) genera and 73 species of Fumarioideae, 11 (48 %) genera and 11 species of Papaveroideae, and a wide selection of outgroup taxa. Floral characters recorded from the literature were then optimized onto phylogenetic trees to reconstruct ancestral states using parsimony, maximum likelihood and reversible-jump Bayesian approaches.Key Results Pteridophyllum is not nested in Fumarioideae. Fumarioideae are monophyletic and Hypecoum (18 species) is the sister group of the remaining genera. Relationships within the core Fumarioideae are well resolved and supported. Dactylicapnos and all zygomorphic genera form a well-supported clade nested among disymmetric taxa.Conclusions Disymmetry of the corolla is a synapomorphy of Fumarioideae and is strongly correlated with changes in the androecium and differentiation of middle and inner tepal shape (basal spurs on middle tepals). Zygomorphy subsequently evolved from disymmetry either once (with a reversal in Dactylicapnos) or twice (Capnoides, other zygomorphic Fumarioideae) and appears to be correlated with the loss of one nectar spur.     

大叶铁线莲大小孢子发生及雌雄配子体发育

铁线莲属植物在花部形态和结构方面存在较大差异, 遗传背景相对复杂。因此, 在杂交育种前对其进行胚胎学研究具有重要意义。利用石蜡切片技术对大叶铁线莲(Clematis heracleifolia)大小孢子发生及雌雄配子体发育过程进行研究, 结果显示, 大叶铁线莲具雄株和两性花植株。雄花中, 雄配子体发育偶见败育现象; 而两性花中多数花粉发育异常, 形成功能性雌花。正常发育的两性花中, 雄蕊较雌蕊先发育完全。花药4室, 具腺质绒毡层, 偶见变形绒毡层。胞质分裂为同时型, 以四面体型四分体为主, 偶见左右对称型。成熟花药中, 花药壁由纤维状加厚的表皮及药室内壁构成, 花粉粒为2-细胞型, 近球状, 散沟型。子房1室, 内含少量退化胚珠及1个发育正常的胚珠, 倒生, 单珠被, 薄珠心, 蓼型胚囊, 具线形大孢子四分体及双核反足细胞。大叶铁线莲可能处于相对进化的过渡地位。在杂交育种中, 建议以雄花植株作为父本, 两性花植株仅用作母本; 在两性花花芽大小为0.5-0.8 cm时进行去雄处理。     

Establishment of zygomorphy on an ontogenic spiral and evolution of perianth in the tribe Delphinieae (Ranunculaceae)

Background and Aims

Ranunculaceae presents both ancestral and derived floral traits for eudicots, and as such is of potential interest to understand key steps involved in the evolution of zygomorphy in eudicots. Zygomorphy evolved once in Ranunculaceae, in the speciose and derived tribe Delphinieae. This tribe consists of two genera (Aconitum and Delphinium s.l.) comprising more than one-quarter of the species of the family. In this paper, the establishment of zygomorphy during development was investigated to cast light on the origin and evolution of this morphological novelty.

Methods

The floral developmental sequence of six species of Ranunculaceae, three actinomorphic (Nigella damascena, Aquilegia alpina and Clematis recta) and three zygomorphic (Aconitum napellus, Delphinium staphisagria and D. grandiflorum), was compared. A developmental model was elaborated to break down the successive acquisitions of floral organ identities on the ontogenic spiral (all the species studied except Aquilegia have a spiral phyllotaxis), giving clues to understanding this complex morphogenesis from an evo-devo point of view. In addition, the evolution of symmetry in Ranunculaceae was examined in conjunction with other traits of flowers and with ecological factors.

Key Results

In the species studied, zygomorphy is established after organogenesis is completed, and is late, compared with other zygomorphic eudicot species. Zygomorphy occurs in flowers characterized by a fixed merism and a partially reduced and transformed corolla.

Conclusions

It is suggested that shifts in expression of genes controlling the merism, as well as floral symmetry and organ identity, have played a critical role in the evolution of zygomorphy in Delphinieae, while the presence of pollinators able to exploit the peculiar morphology of the flower has been a key factor for the maintenance and diversification of this trait.Key words: Delphinieae, development, evolution, evo-devo, nectar spurs, ontogenic spiral, Ranunculaceae, zygomorphy     

Pollination biology in Roepera (Zygophyllaceae): How flower structure and shape influence foraging activity

The foraging behavior of bees is a complex phenomenon that depends on numerous physical features of flowers. Of particular importance are accessibility of floral rewards, floral proportions, symmetry and orientation. The flowers of Roepera are characterized by the presence of staminal scales (SS), which play an important role in nectar protection. We studied two species of Roepera with different symmetry and flower orientation, which are mainly visited by honeybees (Apis mellifera). We aimed to show how the foraging behavior of honey bees is affected by the function of SS, floral symmetry and orientation. The foraging behavior was documented by video photography. Handling time, access to nectar, percentage of pollen/nectar foraging, percentage of pollen contact and pollen deposition site on the honey bee's body were assessed. The morphometric features of the honey bees and flowers were analyzed. We found that the SS restricted pollinator access to nectar. Our results indicated consistency of visitation patterns in zygomorphic, laterally oriented flowers of R. fuscata versus random patterns in actinomorphic, diversely oriented flowers of R. leptopetala. The relative proportions of SS and proboscis length appear to be crucial for the success of pollinators. The directionality of the honey bees' movement, together with the different positioning of reproductive organs, plays an important role in the accuracy of pollen transfer and pollination efficiency.     

非洲紫罗兰两侧与辐射对称花中两个CYC类完整基因的分离和序列分析

在已知GCYC基因部分序列基础上, 通过改进的mTAIL-PCR方法克隆非洲紫罗兰Saintpaulia ionantha两侧对称栽培种中CYC类基因的5′未知序列, 并进而从两侧与辐射对称栽培种中分离得到苦苣苔科Gesneriaceae中第一组完整基因: SiCYC1A与SiCYC1B。对以上基因的核酸和氨基酸序列比较发现, SiCYC1A与SiCYC1B序列同源性很高, 均含有完整的功能调控区域(即TCP domain和R domain)并与模式植物金鱼草Antirrhinum majus中CYC基因同源。因此, 这两个基因应具有正常功能, 是功能上互补的冗余基因。令人意外的是在辐射对称花栽培品种中的这两个基因和两侧对称花栽培品种中对应基因的序列完全相同。经过对金鱼草以及相关类群辐射对称花突变体中CYC类基因序列的比较分析, 推论在非洲紫罗兰中, SiCYC1A与SiCYC1B基因可能受上游未知的共同调控因子调控, 该调控因子的改变是导致栽培品种中花对称性发生变化的主要原因。另外, 对改进后的TAIL-PCR(mTAIL-PCR)的方法和过程进行了详细叙述, 并对其技术特征和优势开展了简单的论述。