Multiple lineages of FRUITFULL exhibit dynamic patterns of gene evolution after genome triplication in the Brassiceae tribe (Brassicaceae)

Abstract

Phylogenetic analyses of important development genes are necessary to identify trends in sequence divergence and gene retention/loss that underlie diversification after polyploidization. We investigated the evolution of FRUITFULL (FUL) in the tribe Brassiceae (Brassicaceae), where a recent genome triplication allows investigation into the fate of paralogs. Many Brassiceae members possess a unique fruit type exhibiting segmentation and variable dehiscence called heteroarthrocarpy, providing a case study to compare with FUL’s evolution, as a single copy is known to control fruit dehiscence in Arabidopsis. We constructed a phylogeny containing all major species lineages to investigate the number of retained FUL paralogs, trends in selective pressure and intron evolution, and their relationship to heteroarthrocarpy. We recovered four well-supported lineages that likely correspond to three FUL copies from hexaploidization. Rates of selection varied across lineages and comparatively relaxed selection was associated with fruit indehiscence. However, stabilizing selection predominated all lineages, indicating that paralogs retain functionality. Longer introns were correlated with relaxed selection on exons and, on average, heteroarthrocarpic taxa had longer introns and retained different FUL paralogs than nonheteroarthrocarpic taxa, although correlations were complex. The dynamic pattern of FUL evolution invites investigation into the role of upstream regulators in the dehiscence of heteroarthrocarpic fruits.