Evolution of regulatory interactions controlling floral asymmetry

A key challenge in evolutionary biology is to understand how new morphologies can arise through changes in gene regulatory networks. For example, floral asymmetry is thought to have evolved many times independently from a radially symmetrical ancestral condition, yet the molecular changes underlying this innovation are unknown. Here, we address this problem by investigating the action of a key regulator of floral asymmetry, CYCLOIDEA (CYC), in species with asymmetric and symmetric flowers. We show that CYC encodes a DNA-binding protein that recognises sites in a downstream target gene RADIALIS (RAD) in Antirrhinum. The interaction between CYC and RAD can be reconstituted in Arabidopsis, which has radially symmetrical flowers. Overexpression of CYC in Arabidopsis modifies petal and leaf development, through changes in cell proliferation and expansion at various stages of development. This indicates that developmental target processes are influenced by CYC in Arabidopsis, similar to the situation in Antirrhinum. However, endogenous RAD-like genes are not activated by CYC in Arabidopsis, suggesting that co-option of RAD may have occurred specifically in the Antirrhinum lineage. Taken together, our results indicate that floral asymmetry may have arisen through evolutionary tinkering with the strengths and pattern of connections at several points in a gene regulatory network.     

Flower symmetry and shape in Antirrhinum

According to their symmetry, flowers are classified as radially symmetrical or bilaterally symmetrical. Bilateral symmetry, which is thought to have evolved from radial symmetry, results from establishment of asymmetry relative to a dorsoventral axis of flowers. Here we consider developmental genetic mechanisms underlying the generation of this asymmetry and how they relate to controls of petal shape and growth in Antirrhinum. Two genes, CYC and DICH, are expressed in dorsal domains of the Antirrhinum flower and determine its overall dorsoventral asymmetry and the asymmetries and shapes of individual floral organs, by influencing regional growth. Another gene, DIV, influences regional asymmetries and shapes in ventral regions of the flower through a quantitative effect on growth. However, DIV is not involved in determining the overall dorsoventral asymmetry of the flower and its effects on regional asymmetries depend on interactions with CYC/DICH. These interactions illustrate how gene activity, symmetry, shape and growth may be related.     

Diversification and co-option of RAD-like genes in the evolution of floral asymmetry

To understand how changes in gene regulatory networks lead to novel morphologies, we have analysed the evolution of a key target gene, RAD, controlling floral asymmetry. In Antirrhinum, flower asymmetry depends on activation of RAD in dorsal regions of the floral meristem by the upstream regulators CYC and DICH. We show that Arabidopsis, a species with radially symmetric flowers, contains six RAD-like genes, reflecting at least three duplications since the divergence of Antirrhinum and Arabidopsis. Unlike the situation in Antirrhinum, none of the Arabidopsis RAD-like genes are activated in dorsal regions of the flower meristem. Rather, the RAD-like genes are expressed in distinctive domains along radial or ab-adaxial axes, consistent with a range of developmental roles. Introduction of a RAD genomic clone from Antirrhinum into Arabidopsis leads to a novel expression pattern that is distinct from the expression pattern of RAD in Antirrhinum and from the endogenous RAD-like genes of Arabidopsis. Nevertheless, RAD is able to influence developmental targets in Arabidopsis, as ectopic expression of RAD has developmental effects in this species. Taken together, our results suggest that duplication and divergence of RAD-like genes has involved a range of cis- and trans-regulatory changes. It is possible that such changes led to the coupling of RAD to CYC regulation in the Antirrhinum lineage and hence the co-option of RAD had a role in the generation of flower dorsoventral asymmetry.     

Floral symmetry affects speciation rates in angiosperms

Despite much recent activity in the field of pollination biology, the extent to which animal pollinators drive the formation of new angiosperm species remains unresolved. One problem has been identifying floral adaptations that promote reproductive isolation. The evolution of a bilaterally symmetrical corolla restricts the direction of approach and movement of pollinators on and between flowers. Restricting pollinators to approaching a flower from a single direction facilitates specific placement of pollen on the pollinator. When coupled with pollinator constancy, precise pollen placement can increase the probability that pollen grains reach a compatible stigma. This has the potential to generate reproductive isolation between species, because mutations that cause changes in the placement of pollen on the pollinator may decrease gene flow between incipient species. I predict that animal-pollinated lineages that possess bilaterally symmetrical flowers should have higher speciation rates than lineages possessing radially symmetrical flowers. Using sister-group comparisons I demonstrate that bilaterally symmetric lineages tend to be more species rich than their radially symmetrical sister lineages. This study supports an important role for pollinator-mediated speciation and demonstrates that floral morphology plays a key role in angiosperm speciation.     

The Arabidopsis SUPERMAN Gene Mediates Asymmetric Growth of the Outer Integument of Ovules

Arabidopsis superman (sup, also referred to as floral mutant10) mutants have previously been shown to have flowers with supernumerary stamens and reduced carpels as a result of ectopic expression of the floral homeotic gene APETALA3 (AP3). Here, we report that sup mutations also cause specific alterations in ovule development. Growth of the outer integument of wild-type ovules occurs almost exclusively on the abaxial side of the ovule, resulting in a bilaterally symmetrical hoodlike structure. In contrast, the outer integument of sup mutant ovules grows equally on all sides of the ovule, resulting in a nearly radially symmetrical tubular shape. Thus, one role of SUP is to suppress growth of the outer integument on the adaxial side of the ovule. Genetic analyses showed that the effects of sup mutations on ovule development are independent of the presence or absence of AP3 activity. Thus, SUP acts through different mechanisms in its early role in ensuring proper determination of carpel identity and in its later role in asymmetric suppression of outer integument growth.     

被子植物花对称性的遗传控制

简要评述了被子植物花对称性遗传控制研究的最新进展。金鱼草中控制花背腹轴不对称性基因Cy cloidea(Cyc)和Dichotama(Dich)的克隆 ,为研究单对称花的遗传控制机理和进化历程提供了可能。在唇形目(Lamialess .l.)中的研究表明 ,在与金鱼草 (Antirrhinummajus)近缘的物种中 ,Cyc基因的同源基因可以采用相似的机制控制背腹轴上花器官的不对称性发育。最新的研究结果显示 ,在同金鱼草远缘的豆科植物 (Legu minosae)中 ,不仅存在Cyc基因的同源基因 ,而且它们也参与花背腹轴上不对称性的形成。参与花对称性控制的基因属于植物中一个新发现的基因家族———TCP结构域基因     

Floral symmetry and nectar guides: ontogenetic constraints from floral development, colour pattern rules and functional significance

The accord between symmetries of flower shape (external contours) and nectar guides (internal contours) was examined using the bulbous flora of South Africa, and in the general floras of Britain, Alpine Colorado, Canadian Arctic and Israel. It was found that radially symmetrical flowers have radially symmetrical nectar guides whereas bilaterally symmetrical flowers have bilaterally symmetrical nectar guides. It is suggested that the complementarity between the external and the internal contours of the flower increases the probability that, and efficiency with which, a bee moves into the flower's centre and towards the sporophylls and access to floral rewards, regardless of the flower's form and the bee's previous experience. Patterns of coloration of tepals against background and nectar guides against tepals also accord with behavioural and sensory characteristics of pollinators. It is suggested that the complementarity of contours is probably constrained by floral development, but patterns of coloration of tepals against background and nectar guides against tepals is constrained by pollinators' sensory physiology.     

A duplication of gcyc predates divergence within tribe Coronanthereae (Gesneriaceae): Phylogenetic analysis and evolution

Recent investigations in Gesneriaceae have indicated that the cycloidea homolog, gcyc, remains functional at the DNA level and rates of sequence divergence in this gene are not statistically different across all taxa regardless of floral symmetry. A duplication of gcyc has been detected within Coronanthereae, a tribe that has phylogenetic affinities to subfamily Gesnerioideae and includes two genera with radially symmetrical corollas. Duplication of gcyc has been detected in all Coronanthereae except Sarmienta. All paralogs appear functional at the DNA level. Likewise, there is no increased sequence divergence between the two copies, nor between species with radially symmetrical flowers to those with bilateral symmetry. The duplication of gcyc in Coronanthereae is most likely a result of polyploidy since Coronanthereae have the highest chromosome counts of all Gesneriaceae.     

Insect preference for symmetrical artificial flowers

An insect preference for floral symmetry may be maintained because plants with symmetrical flowers, which are able to control developmental processes under given environmental conditions, also are able to provide more pollinator rewards than plants with asymmetrical flowers. Alternatively, insects may have an inherent preference for symmetrical structures and thereby impose selection for the maintenance of symmetry in flowers even in the absence of any pollinator rewards. We tested for an insect preference for radially symmetrical flowers by using horizontally placed units of four circular coloured flower models varying in size and symmetry. The shape and colour of the model flowers did not resemble any naturally occurring flowers in the environment. Insects and Hymenoptera, respectively (five species of Diptera and one species of Coleoptera) that visited the flower models clearly preferred symmetrical models over asymmetrical ones, and the ranking of visits to the models reflected a preference for large, symmetrical flowers. These results provide evidence for a preference for symmetrical flower models, even in the absence of pollinator rewards. Received: 11 September 1997 / Accepted: 2 November 1997     

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.     

Patterns of fluctuating asymmetry in flowers: Implications for sexual selection in plants

Characters in animals used in signalling and subjected to strong directional selection often demonstrate (i) an elevated level of fluctuating asymmetry (small random deviations from bilateral symmetry) and (ii) a negative relationship between the degree of individual fluctuating asymmetry and the size of a given character. We tested these two predictions in plants since flowers are subjected to strong directional selection and are involved in signalling to pollinators, whereas leaves are supposed not to be directly involved in signalling. The overall level of fluctuating asymmetry in a number of plant species with bilaterally or radially symmetric flowers was not generally higher in floral traits than in leaves. The level of fluctuating asymmetry in plants was sometimes significantly consistent within individuals. The absolute degree of individual fluctuating asymmetry in floral traits was generally negatively related to the size of the trait, while there was a positive relationship for leaves. The degree of individual fluctuating asymmetry in floral traits was marginally negatively related to the degree of individual fluctuating asymmetry in leaf traits. These patterns of fluctuating asymmetry in plants suggest that (i) the degree of asymmetry in flowers signals different aspects of quality than does the degree of asymmetry in leaves, and that (ii) fluctuating asymmetry in flowers often reflects the phenotypic quality of individual plants.     

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.     

Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). 1. Radially symmetrical taxa lacking organ suppression

Flowers in detarioid legume taxa (Isoberlinia angolensis, Microberlinia brazzavillensis, M. bisulcata, Hymenostegia klainii) initiate all 21 floral organs, are radially symmetrical, and have little or no organ suppression. All share a narrow, "Omega"-shaped floral apex and massive bracteoles at initiation. All have helical sepal initiation, starting abaxially. They differ in whether the first sepal initiates medianly (Microberlinia brazzavillensis, M. bisulcata) or nonmedianly (Isoberlinia angolensis, Hymenostegia klainii), and in petal order: helical (I. angolensis) or unidirectional (M. brazzavillensis, M. bisulcata, H. klainii). Stamens initiate in unidirectional order in each whorl except in M. brazzavillensis, which has a bidirectional outer whorl. An unusual feature is the ring meristem in M. bisulcata, on which petals and stamens are initiated. Overlap in time of organ initiation between whorls occurs in I. angolensis, M. brazzavillensis, and M. bisulcata but not in H. klainii. The carpel initiates concurrently with petals in all except H. klainii, in which it initiates with the outer stamens. The carpel remains open at ovule initiation in both species of Microberlinia. These detarioid taxa represent elements of the tribe having essentially radially symmetrical flowers, with all organs initiated and persisting to anthesis, but their specialized "Omega" character-state complex is shared with specialized taxa that have zygomorphic flowers and some organs suppressed.     

Visual discrimination of radial cues by the honeybee (Apis mellifera)

This is a systematic study of the discrimination of black radially symmetrical patterns presented on a white vertical background and subtending 45 degrees or 50 degrees at the point of choice in a Y-maze apparatus. Before discrimination can occur, the ability to fixate is promoted by any radial pattern irrespective of the number of symmetry axes. A ring of spots can also stabilize the eye before the positions of the spots are discriminated.Cues for discrimination are of two main types. First, with fixed patterns of sectors or spots, the cue is the location of an area of black relative to the fixation point, and the particular number of axes is less important than the size of the individual areas. Secondly, evidence is presented for a family of filters with large fields and coarse tuning that detect patterns of radially symmetrical edges. These filters become more evident when the patterns are made of thin black radial bars or when they are rotated at random during the training. An angular shift of one radial pattern relative to the other, or a difference between numbers of bars, is best discriminated when one of the patterns but not the other has angles of 30 degrees, 60 degrees, or 120 degrees between radial edges, and least when the angles are 90 degrees. Baffles in the apparatus make the bees pause and fixate so that discrimination is improved. When targets are rotated during the learning process, radial cues for discriminations must be presented as edges, not as spots or areas. Besides detecting and fixating flowers, this system could be useful to estimate the perfection of their symmetry.     

Floral ontogeny, pattern formation, and evolution in Hibbertia and Adrastaea (Dilleniaceae)

Floral development was compared with scanning electron microscopy in 12 Australian species of Hibbertia representing most of its morphological variation, and in the related Adrastaea (Dilleniaceae). Calyx and corolla arise in quincuncial helices in radially symmetrical species, while the petals initiate unidirectionally from one side in zygomorphic species. Stamen number (3-200+) proliferates by centrifugal addition of individual primordia or by innovations of common primordia and ring meristems. Common primordia arise in single-stamen positions alternately with petals, and each produces one to several stamens centrifugally that remain attached to a shared base and form a stamen fascicle. A ring meristem in Adrastaea initiates a whorl of five stamens, alternate with the first stamens but outside their whorl. In radially symmetrical species of Hibbertia, a first ring of stamens is supplemented centrifugally by additional stamens on a meristem ring. The first stamens in zygomorphic species of Hibbertia initiate as a terminal ridge on the floral apex, with subsequent stamens added centrifugally on one side and two carpels initiated on the opposite side. The carpels arise as a simultaneous ring in radially symmetrical flowers, or as a simultaneous pair in zygomorphic species. Staminodial presence is viewed as of minor significance. Four pollinator syndromes are proposed for Hibbertia, related to differing floral architecture.     

Traits and phylogenetic history contribute to network structure across Canadian plant–pollinator communities

Interaction webs, or networks, define how the members of two or more trophic levels interact. However, the traits that mediate network structure have not been widely investigated. Generally, the mechanism that determines plant-pollinator partnerships is thought to involve the matching of a suite of species traits (such as abundance, phenology, morphology) between trophic levels. These traits are often unknown or hard to measure, but may reflect phylogenetic history. We asked whether morphological traits or phylogenetic history were more important in mediating network structure in mutualistic plant-pollinator interaction networks from Western Canada. At the plant species level, sexual system, growth form, and flower symmetry were the most important traits. For example species with radially symmetrical flowers had more connections within their modules (a subset of species that interact more among one another than outside of the module) than species with bilaterally symmetrical flowers. At the pollinator species level, social species had more connections within and among modules. In addition, larger pollinators tended to be more specialized. As traits mediate interactions and have a phylogenetic signal, we found that phylogenetically close species tend to interact with a similar set of species. At the network level, patterns were weak, but we found increasing functional trait and phylogenetic diversity of plants associated with increased weighted nestedness. These results provide evidence that both specific traits and phylogenetic history can contribute to the nature of mutualistic interactions within networks, but they explain less variation between networks.