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.     

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.     

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     

Floral development in Astragalus caspicus Bieb. (Leguminosae: Papilionoideae: Galegeae)

Floral organogenesis and development of the bushy perennial legume Astragalus caspicus were studied using epi-illumination light microscopy techniques. Based on our observations, flowers are in axillary two-flowered racemes, initiate all 21 floral organs and show precocious appearance of zygomorphy. The order of floral organ initiation is unidirectional in whorls starting from the abaxial position of the flower with a high degree of overlap. Another important ontogenetic feature is the existence of two successive common primordial stages categorized as primary and secondary. The primary common primordia produce antesepalous stamens and secondary common primordia. In contrast, the five secondary common primordia subdivide into a petal and an antepetalous stamen primordia. Our findings on floral ontogeny of A. caspicus provide new evidence for the complex and variable floral initiation and development in legumes. The floral apex with strong overlapping initiation of different organs illustrates a paradox in which different capabilities must be presumed to exist simultaneously. Moreover, two extraordinary types of common primordia represent possibly an advanced evolutionary trend where time intervals between the initiations of different floral organs in Papilionoideae are shortened.     

Specific Duplication and Dorsoventrally Asymmetric Expression Patterns of Cycloidea-Like Genes in Zygomorphic Species of Ranunculaceae

Floral bilateral symmetry (zygomorphy) has evolved several times independently in angiosperms from radially symmetrical (actinomorphic) ancestral states. Homologs of the Antirrhinum majus Cycloidea gene (Cyc) have been shown to control floral symmetry in diverse groups in core eudicots. In the basal eudicot family Ranunculaceae, there is a single evolutionary transition from actinomorphy to zygomorphy in the stem lineage of the tribe Delphinieae. We characterized Cyc homologs in 18 genera of Ranunculaceae, including the four genera of Delphinieae, in a sampling that represents the floral morphological diversity of this tribe, and reconstructed the evolutionary history of this gene family in Ranunculaceae. Within each of the two RanaCyL (Ranunculaceae Cycloidea-like) lineages previously identified, an additional duplication possibly predating the emergence of the Delphinieae was found, resulting in up to four gene copies in zygomorphic species. Expression analyses indicate that the RanaCyL paralogs are expressed early in floral buds and that the duration of their expression varies between species and paralog class. At most one RanaCyL paralog was expressed during the late stages of floral development in the actinomorphic species studied whereas all paralogs from the zygomorphic species were expressed, composing a species-specific identity code for perianth organs. The contrasted asymmetric patterns of expression observed in the two zygomorphic species is discussed in relation to their distinct perianth architecture.     

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.     

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.     

Towards unlocking the deep nodes of Leguminosae: Floral development and morphology of the enigmatic Duparquetia orchidacea (Leguminosae, Caesalpinioideae)

Duparquetia orchidacea (Caesalpinioideae-Cassieae-Duparquetiinae) is a monotypic liana from tropical West Africa. Its highly unusual, zygomorphic flowers, the unique pollen morphology, and the lack of vestured pits in the wood correspond with previous phylogenetic studies that resolved the position of the species to an isolated position among the early-branching Leguminosae. Here we present a detailed analysis of floral morphology and development to clarify open questions of its floral organization. We provide new data that can be useful in clarifying phylogenetic relationships among early branching Leguminosae and improve our understanding of floral evolution in this large and important plant family. For comparison, we also present developmental data for other Fabales. Our analysis reveals some unusual and in parts unique developmental patterns, such as strict acropetal organ formation, loss and suppression of floral organs, and early petal enlargement. We interpret alternating left-right symmetries in floral development as clues to a spiral organ formation in ancestral taxa. Early asymmetry of the young carpel helps to interpret enantiostyly of other Leguminosae as an example of imprinted shape. Finally, we show that cochlear-descending petal aestivation in Duparquetia and in Papilionoideae is based on different ontogenetic patterns and therefore is most probably nonhomologous.     

花对称性的研究进展

花对称性(floral symmetry)是被子植物花部结构的典型特性之一,主要有辐射对称和两侧对称两种形式。被子植物初始起源的花为辐射对称,而两侧对称的花则是由辐射对称的花演变而来。两侧对称的花部结构是被子植物进化过程中的一个关键的革新,被认为是物种形成和分化的关键推动力之一。近年来有关花对称性的形成和进化机制的研究在植物学科的不同领域均取得了长足的进展。本文综述了花对称性在发育生物学、传粉生物学、生殖生态学及分子生物学等方面的研究进展。两侧对称形成于被子植物花器官发育的起始阶段,随后贯穿整个花器官发育过程或者出现在花器官发育后期的不同阶段。花器官发育过程中一种或多种类型器官的败育以及特异性花器官结构的形成是两侧对称形成的主要原因。研究表明,在传粉过程的不同阶段,花对称性均会受到传粉昆虫介导的选择作用。相比辐射对称的花,两侧对称的花提高了特异性传粉者的选择作用,增加了花粉落置的精确性,进而确保了其生殖成功。花对称性的分子机理已经在多种双子叶植物中进行了深入的研究。现有的证据表明,CYC同源基因在花对称性的分子调控方面起着非常重要的作用。花对称性在被子植物进化过程中是如何起源,与其他花部构成之间是否协同作用,一些不符合一般模式的科属其花对称性的形成机制等都是今后要进一步研究的命题。     

Floral Development and Anatomy ofMoringa oleifera(Moringaceae): What is the Evidence for a Capparalean or Sapindalean Affinity?

Floral development and anatomy ofMoringahave been investigatedin the context of the disputed view of a capparalean affinity.Flowers arise in terminal or axillary panicles. Sepals arisesequentially and petals simultaneously. Antepetalous stamensarise simultaneously and precede the antesepalous staminodes,which emerge sequentially. Within their respective whorls, thepetals and stamens become twisted along different orientations.The gynoecium develops as a ring primordium on which three carpellarylobes become demarcated simultaneously. A saccate ovary bearsnumerous ovules on a parietal placentation and is topped bya hollow style. The interpretation of laminal placentation isdenied. Monothecal anthers are formed by the failure of onehalf to initiate. The flowers present a peculiar form of zygomorphyrunning transversally from the petal between sepals 3 and 5to sepal 4. The shape and position of petals and stamens isrelated to a pollen presentation mechanism with bowl-shapedanthers on different levels. The floral anatomy also reflectsthe zygomorphy of the flower. AlthoughMoringashares importantmorphological features with certain members of the Sapindalesand Capparales, differences in ontogeny make a close relationshipwith either Capparales or certain Sapindales appear uncertain.Copyright1998 Annals of Botany Company Moringa,Moringaceae, Capparales, Sapindales, floral ontogeny, floral anatomy.     

Genetic analysis of floral symmetry in Van Gogh's sunflowers reveals independent recruitment of CYCLOIDEA genes in the Asteraceae

The genetic basis of floral symmetry is a topic of great interest because of its effect on pollinator behavior and, consequently, plant diversification. The Asteraceae, which is the largest family of flowering plants, is an ideal system in which to study this trait, as many species within the family exhibit a compound inflorescence containing both bilaterally symmetric (i.e., zygomorphic) and radially symmetric (i.e., actinomorphic) florets. In sunflower and related species, the inflorescence is composed of a single whorl of ray florets surrounding multiple whorls of disc florets. We show that in double-flowered (dbl) sunflower mutants (in which disc florets develop bilateral symmetry), such as those captured by Vincent van Gogh in his famous nineteenth-century sunflower paintings, an insertion into the promoter region of a CYCLOIDEA (CYC)-like gene (HaCYC2c) that is normally expressed specifically in WT rays is instead expressed throughout the inflorescence, presumably resulting in the observed loss of actinomorphy. This same gene is mutated in two independent tubular-rayed (tub) mutants, though these mutations involve apparently recent transposon insertions, resulting in little or no expression and radialization of the normally zygomorphic ray florets. Interestingly, a phylogenetic analysis of CYC-like genes from across the family suggests that different paralogs of this fascinating gene family have been independently recruited to specify zygomorphy in different species within the Asteraceae.     

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.     

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.     

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。     

HETEROMORPHIC FLOWER DEVELOPMENT IN NEPTUNIA PUBESCENS,A MIMOSOID LEGUME

The characteristic of heteromorphic inflorescences in some mimosoid legumes such as Neptunia is a puzzling one which can be approached developmentally. Each spicate inflorescence of Neptunia pubescens includes three types of flowers: perfect in the upper half, functionally male just below the middle, and sterile or neuter at the base. Developmental studies of the inflorescence show that order of initiation of bracts on the inflorescence is acropetal, but that order of subsequent development of flowers is both acropetal and basipetal on the axis. Bract growth and initiation of the axillary floral apices at the base are inhibited or retarded, while those in the middle and upper levels continue development without interruption. The three types of floral primordia are similar during initiatory stages of organ formation and through early development. At mid-development, differences arise in floral symmetry, petal form, stamen form, and size and shape of the carpel. The functionally male flowers become strongly dorsiventral and zygomorphic while the other two morphs remain actinomorphic or nearly so. Heteromorphy arises from a combination of early suppression of organogeny plus mid-stage innovations of zygomorphy and lateral expansion of stamen primordia. These divergent developmental pathways in one inflorescence can be interpreted in part using Gould's concept of heterochrony: changes in timing of developmental events to produce different structures. Other changes in Neptunia cannot be explained by this concept, however; such changes as omission of processes (i.e., meiosis) in some organs, or addition of processes not normally present (i.e., blade formation in stamen primordia which become staminodia). It is becoming evident from work on this and other legume flowers that actual loss of organs is rare, compared to initiation followed by suppression or modification.     

Pentamerous flowers in the genus Phytolacca have been derived from trimerous flowers—New evidence from the floral organogenesis of Phytolacca dodecandra

The floral organogenesis of Phytolacca dodecandra L′Her. (Phytolaccaceae) has been observed under both scanning electron microscope (SEM) and light microscope. The primordia of the floral appendage are arranged according to a pentamerous pattern and acropetal succession. Five sepal primordia arise in a 2/5 sequence, and no petal primordia have been observed. The stamen primordia arise centrifugally. The first two pairs arise successively opposite sepal one and two. In the subsequent initiation of inner and outer stamens, P. dodecandra differs from other species in the genus Phytolacca. The four or five carpel primordia arise in rapid succession, usually equal in number and alternating with the inner stamens. The effects of temporal and spatial factors during the floral organogenesis of P. dodecandra are discussed. The data on the androecial ontogeny in P. dodecandra refute the existence of diplostemony in Phytolaccaceae, in which P. dodecandra occupies a pivotal systematic position. The androecial ontogeny in P. dodecandra supports the viewpoint that in the genus Phytolacca pentamerous flowers have been derived from trimerous flowers.