Gene Duplication and Evolution of the MADS-Box Floral Homeotic, WUSCHEL-RELATED HOMEOBOX, and PIN-FORMED Gene Families in Angiosperms

Abstract

Whole genome duplication (WGD), along with other modes of gene duplication, has been associated with biochemical transitions underlying morphological complexity and adaptive radiation across eukaryotes, including flowering plants. However, comparatively little is known about how the evolution of gene regulatory networks (GRNs) contribute to the diversity of complex organs, such as flowers. Floral organ identities are determined by the interaction of the MIKCC-type MADS-box transcription factors APETALA1 (AP1), APETALA3 (AP3), AGAMOUS (AG), and SEPALLATA1/2/4 (LOFSEP). At the base of the core eudicot clade, which comprises 70% of extant flowering plants, each of these gene lineages appears to have experienced at least one gene duplication event, which gave rise to two or three descendent subclades. In Chapter Two of this dissertation, phylogenetic and synteny analyses are used to examine the simultaneous cluster of MIKCC-type MADS gene duplications that coincide with the γ WGD event. This is dated to between the divergence of the Buxales and the radiation of the core eudicots, which was followed by the establishment of the Core Eudicot Floral Groundplan (CEFG) in the Pentapetalae. In Chapter Three, reconstruction of ancestral character states shows that the confined AP1 expression in sepals and petals observed in Arabidopsis has been evolved multiple times in derived angiosperm lineages, while the gene expression patterns of AP3 (in petals and stamens) and AG (stamens and carpels) are highly conserved in angiosperms. In order to further understand how gene duplications related to the γ event and other WGDs have contributed to the evolution of plant development, the sequences of 1019 WUSCHEL-RELATED HOMEOBOX (WOX) transcription factors and 462 PIN-FORMED (PIN) auxin efflux carrier from 36 genomes and 351 transcriptomes spanning Plantae are compiled for phylogenomic analyses. Chapter Four shows that the WOX gene family may have originated in Plantae and diverged into three ancient superclades and that two duplications of the PIN gene family in the euphyllophytes gave rise to three superclades. The GRNs of WOX and PIN genes may be deeply conserved in Plantae. This study provides the phylogenetic context for elucidating functional evolution of the MADS-box, WOX, and PIN gene families, which is likely to have contributed to the morphological complexity of land plants.