Evolution of the legume flower: case studies in the early-branching papilionoid legumes (Papilionoideae, Leguminosae)

Abstract

Flowers are the reproductive structures of angiosperms and have played an important role in the diversification of land plants. In the legume family (Leguminosae or Fabaceae), the diversity of flower morphology is remarkable across its six subfamilies, but one particular type of architecture is considered the signature of the family: the papilionate flower. This typical pea flower with zygomorphic symmetry, five petals and ten stamens is exclusively found in the Papilionoideae subfamily, but genera with a range of non-papilonate floral morphologies are found across the early-branching lineages nested within papilionate lineages. Investigating the genetic changes in these divergent lineages can shed light on the underlying processes leading to the evolution of novel flower morphology.

CYCLOIDEA (CYC), DIVARICATA (DIV) RADIALIS (RAD) and DIV-and-RAD-Interacting-Factor (DRIF) have been identified as key genes regulating floral symmetry across flowering plants. In typical papilionate flowers, CYC like genes are expressed on the dorsal (upper) side of the flower and are specific to development of the standard petal, whereas DIV, RAD and DRIF activity is not well known. In this thesis, we use new genomic and transcriptomic data to explore the key symmetry-regulating genes in the papilionoid legume genera Andira (typical zygomorphic papilionate flower), Cyathostegia (single petal and multiple stamens), and Cadia (radially symmetrical flower). We produce draft genome assemblies and RNASeq to identify putative orthologs of CYC, DIV, RAD, and DRIF. We quantify the relative abundance of these genes in the different developmental stages and between species. Using these genomic and transcriptomic data in the context of previously published DNA sequence data for these genes from across legumes and other angiosperms we use a phylogenetic approach to understanding their evolution and possible function in Papilionoideae. We find that non-papilionate genera do not differ in copy number of CYC, DIV and RAD, suggesting, in contrast to prior studies, that higher copy number of these genes is not associated with the typical papilionate floral morphology. We identify genes differentially expressed between adaxial and abaxial domains of the Cadia flower, genes upregulated on the floral transition Cadia and Cyathostegia, and gene families differentially expressed between the species. We examine the expression pattern of candidate genes to establish if there is any evidence for neofunctionalisation of the retained paralogs. This work is placed into an ontogenetic developmental context with new data of floral ontogeny and published information from across basal legumes. We focus on petal heterochronical patterns and androecium symmetry because these floral features have been shown to be variable in legumes and have only been studied in isolated fashion in classic ontogenetic studies. We show multiple independent evolutionary changes in both features, which underlines the general evolutionary lability of floral forms, for example overall symmetry, uncovered by prior phylogenetic studies.

This thesis also presents a taxonomic synopsis of Aldina, a genus of Papilionoideae with unusual non-papilionoid flower morphology. Flowers of Aldina are radially symmetrical, with numerous free stamens, unlike its sister genera Andira and Hymenolobium, whose zygomorphic flowers are typically papilionate and with 10 stamens. Aldina taxonomy is in need of a revision since the preliminary taxonomic studies on the genus that date back 70 years. Aldina is also ecologically important in the Amazon basin, but because it is poorly studied, and species boundaries are uncertain. Given the urgent need of filling in the gaps in knowledge in the plant diversity of unexplored regions, this thesis presents a taxonomic synopsis of the genus. Eighteen species are recognized in Aldina, with seven names newly placed in synonymy, new lectotypification of five names, and a new combination, Aldina auyantepuiensis, is proposed.