Angiosperms evolved a great diversity of ways to display their flowers for reproductive success by variation in floral color, size, shape, scent, arrangements, and flowering time. The various innovations in floral forms and the aggregation of flowers into different kinds of inflorescences can drive new ecological adaptations, speciation, and angiosperm diversification. Evolutionary developmental biology (evo-devo) seeks to uncover the developmental and genetic basis underlying morphological diversification. Advances in the developmental genetics of floral display have provided a foundation for insights into the genetic basis of floral and inflorescence evolution. A number of regulatory genes controlling floral and inflorescence development have been identified in model plants (e.g., Arabidopsis thaliana, Antirrhinum majus) using forward genetics and conserved functions of many of these genes across diverse non-model species have been revealed by reverse genetics. Gene-regulatory networks that mediated the developmental progresses of floral and inflorescence development have also been established in some plant species. Meanwhile, phylogeny-based comparative analysis of morphological and genetic character has enabled the identification of key evolutionary events that lead to morphological complexity and diversification. Here we review the recent progress on evo-devo studies of floral display including floral symmetry, petal fusion, floral color, floral scent, and inflorescences. We also review the molecular genetic approaches applied to plant evo-devo studies and highlight the future directions of evo-devo.

Rafflesiaceae, crowned “the greatest prodigy of the vegetable world”, produce the largest flowers in angiosperms. They are also holoparasites residing inside their vine hosts, and emerge only during flowering. The floral gigantism and obligate parasitism of Rafflesiaceae have rendered their structure unrecognizable to most plant biologists. The vegetative body is composed of highly reduced strands of cells embedded in the host tissue, and does not differentiate into leaves, stems, or roots. The flowers look and smell like decaying animal flesh and exhibit numerous features unknown in the vast majority of flowering plants. This unusual combination of characters, alongside their generally elevated rates of molecular evolution among commonly used phylogenetic markers and propensity for host-to-parasite horizontal gene transfer, has obscured the phylogenetic affinities of Rafflesiaceae since their discovery two centuries ago. Here, we review the phylogenetic placement of Rafflesiaceae and how it has informed a deeper understanding of the pattern and magnitude of horizontal gene transfer in parasitic plants. We also examine the vegetative and reproductive morphology of Rafflesiaceae to provide insight into how these unusual plants are constructed, and offer clues on their evolution from tiny flowered ancestors to floral giants.

The abrupt origin and rapid diversification of the flowering plants presents what Darwin called “an abominable mystery”. Floral diversification was a key factor in the rise of the flowering plants, but the molecular underpinnings of floral diversity remain mysterious. To understand the molecular biology underlying floral morphological evolution, genetic model systems are essential for rigorously testing gene function and gene interactions. Most model plants are eudicots, while in the monocots genetic models are almost entirely restricted to the grass family. Likely because grass flowers are diminutive and specialized for wind pollination, grasses have not been a major focus in floral evo-devo research. However, while grass flowers do not exhibit any of the raucous morphological diversification characteristic of the orchids, there is abundant floral variation in the family. Here, we discuss grass flower diversity, and review what is known about the developmental genetics of this diversity. In particular, we focus on three aspects of grass flower evolution: (1) the evolution of a novel organ identity—the lodicule; (2) lemma awns and their diversity; and (3) the convergent evolution of sexual differentiation. The combination of morphological diversity in the grass family at large and genetic models spread across the family provides a powerful framework for attaining deep understanding of the molecular genetics of floral evolution.

This review summarizes inflorescence developmental morphology in the grape order Vitales within a phylogenetic context. Inflorescences in the shrubby Leeaceae are terminal thyrses that appear leaf-opposed once renewal growth begins. Plants of the Vitaceae are mainly tendrilled lianas and form five well-defined clades. Inflorescences develop from the unique, non-leafy, uncommitted primordium which arises opposite a leaf on the flank of the shoot apical meristem, and may mature into an inflorescence, tendril, or a combination of the two. The Ampelopsis-Rhoicissus clade, Cissus antarctica group and Yua have a tendril/inflorescence, with cymose branching on the inflorescence axis. Inflorescences in the core Cissus clade and Cyphostemma-Tetrastigma clade arise on a compressed axillary shoot, and leaf-opposed tendrils arise on the main shoot, resulting in different branch orders. In Parthenocissus, tendrils are leaf-opposed on long shoots, and inflorescences are leaf-opposed on axillary branches on short shoots. In the Ampelocissus-Vitis clade, the leaf-opposed tendrils and thyrse inflorescences are of the same branching order, and are often combined. Terminal inflorescences such as in Leeaceae are common in angiosperms, in contrast to the unique leaf-opposed tendril/inflorescence of Vitaceae. The further separation of the tendrils and inflorescences onto different orders of branching (core Cissus, Cyphostemma-Tetrastigma), or separate short and long shoots (Parthenocissus), have allowed each component to optimize its own function. The Ampelocissus-Vitis clade, however, has returned to a thyrse inflorescence, which may allow for larger or unusual lamellate inflorescences (Pterisanthes), and has reunited tendrils and inflorescences. Thus, each clade has developed its own set of inflorescence morphology.

Production of multiple flowers in inflorescences allows the reproductive phenotypes of individual plants to include systematic among-flower variation, which could be adaptive. Systematic trait variation within inflorescences could arise from resource competition among flowers, or be a developmentally determined feature of flower position, regardless of resource dynamics. The latter, architectural effect typically manifests as continuous floral variation within inflorescences. For architectural effects to be adaptive, floral trait variation among individuals must covary with reproductive performance and be heritable. However, heritability and phenotypic selection on gradients of variation cannot be estimated readily with traditional statistical approaches. Instead, we advocate and illustrate the application of two functional data analysis techniques with observations of Delphinium glaucum (Ranunculaceae). To demonstrate the parameters-as-data approach we quantify heritability of variation in anthesis rate, as represented by the regression coefficient relating daily anthesis rate to inflorescence age. SNP-based estimates detected significant heritability (h² = 0.245) for declining anthesis rate within inflorescences. Functional regression was used to assess phenotypic selection on anthesis rate and a floral trait (lower sepal length). The approach used spline curves that characterize within-inflorescence variation as functional predictors of a plant's fruit set. Selection on anthesis rate varied with inflorescence age and the duration of an individual's anthesis period. Lower sepal length experienced positive selection for basal and distal flowers, but negative selection for central flowers. These results illustrate the utility and power of functional-data analyses for studying architectural effects and specifically demonstrate that these effects are subject to natural selection and hence adaptive.

In mature buds of the dwarf dogwood lineage (DW) of Cornus, petals and filaments form an “x”-like box containing mechanical energy from the filaments to allow explosive pollen dispersal. As a start to understand the molecular mechanisms responsible for the origin of this unique structure in Cornus, we cloned and characterized the sequences of APETALA3 (AP3) homologs from Cornus canadensis of the DW lineage and five other Cornus species, given the function of AP3 on petal and stamen development in Arabidopsis, and tested the function of CorcanAP3 using a stable Agrobacterium-mediated transformation system. The cloned CorAP3s (AP3-like genes in Cornus) were confirmed to belong to the euAP3 lineage. qRT-PCR analysis indicated strong increase of CorcanAP3 expression in floral buds of wildtype C. canadensis. A hairpin construct of CorcanAP3 was successfully introduced into wild type plants of C. canadensis, resulting in significant reduction of CorcanAP3 expression and abnormal floral development. The abnormal floral buds lost the “x” form and opened immaturely due to delay or retard of petal and stamen elongation and the push of style elongation. The results suggested CorcanAP3 may function to regulate the coordinated rate of development of petals and stamens in C. canadensis, necessary for the x-structure formation, although the exact molecular mechanism remains unclear. Comparison among six Cornus species indicated a greater ratio of stamen to petal and style growth in C. canadensis, suggesting an evolutionary change of CorAP3 expression pattern in the DW lineage, leading to the greater growth of filaments to form the “x”-box.

In Solanaceae, a group dominated by actinomorphic-flowered species, floral zygomorphy is frequently observed among the early-branching clades. Morphological studies indicated that a zygomorphic androecium is much more common than a zygomorphic corolla in the family. Ontogenic studies suggested the evolution of floral zygomorphy in these two whorls is independent. Here, we have examined the evolution of floral symmetry in the androecium and corolla in Solanaceae. The character states of floral symmetry were assembled for androecium and corolla separately, and ancestral state reconstructions were carried out at both the genus and species levels for Solanaceae and its outgroups. Correlation tests were performed to determine whether the presence of floral zygomorphy in the androecium and corolla is correlated. The ancestral state reconstructions suggest the flower of the most recent common ancestor of Solanaceae is likely zygomorphic in the androecium but actinomorphic in the corolla. Multiple losses and gains of floral zygomorphy in androecium and corolla explain the existing pattern of floral symmetry in Solanaceae. A significant positive correlation between the possession of floral zygomorphy in the androecium and corolla of Solanaceae was detected. Floral zygomorphy likely has evolved in androecium and corolla along separate evolutionary trajectories, and zygomorphy in the androecium may be a precursor for the many gains of zygomorphy in the corolla in Solanaceae.