Phylogenomic Synteny Network Analysis Reveals an Ancient MADS-Box Transcription Factor Tandem Duplication and Lineage-Specific Transpositions

Abstract

Conserved genomic context (or synteny) provides critical information for comparative evolutionary analysis, such as the inference of ancient polyploidy events, recurrent genomic rearrangements across species and gene ancestry. With the increase of sequenced and assembled plant genomes, we now have the opportunity to use synteny to analyze the dynamics of gene family expansion and contraction across broad phylogenetic groups. Here we present an integrated approach to organize plant kingdom-wide gene synteny networks using k-clique percolation. As an example, we analyzed the gene synteny network of the MADS-box transcription factor family based on fifty-one completed plant genomes. We conclude from two massive gene clusters that one of the two Type II MADS-box gene clades evolved from an ancient tandem gene duplication likely predating the radiation of seed plants, which then expanded by polyploidy events and sub-functionalization. This gene clade now contains key regulators of major phenotypes of angiosperms including flower development. Moreover, we find lineage-specific gene clusters derived from transposition events. For example, lineage-specific clusters in the Brassicales containing genes that are well-known for their function in controlling flower morphology (AP3 and PI). Our phylogenomic synteny network approach can be applied to any group of species to gain new insights into the evolution and dynamics of any set of genes.