Duplications and functional specialization force distinct evolution of isoflavonoid biosynthetic genes in legumes

Abstract

Isoflavonoids are specialized plant metabolites, almost exclusive to legumes, and synthesized by the phenylpropanoid pathway. Leguminous plants produce 5-deoxyflavonoids and 5-deoxyisoflavonoids that act in symbiosis with nitrogen-fixing bacteria and involved in plant pathogen and stress response. However, little is known about evolutional origin of legume-specific isoflavonoid biosynthesis pathway. Here, we explored the genome-wide analysis of key genes: chalcone synthase (CHS), chalcone reductase (CHR), isoflavone synthase (IFS) and isoflavone reductase (IFR), encoding enzymes involved in the biosynthesis of (iso) flavonoids in legumes and nonlegumes. Among them, CHS, CHR and IFR comprise multigene families, underling the significant role of gene duplication in the evolutionary. Most duplications of CHS were highly the conventional leguminous type, whereas some were grouped with nonleguminous CHS genes. We also found that CHR homologs in soybean and Sesbania rostrata previously reported were ambiguous and should be re-identified. Phylogenetic analysis and protein sequences alignment indicated that IFSs in legumes are highly conserved. Intriguingly, unlike other IFRs in legumes, IFR-like homologs in Sophora flavescens and Lupinus angustifolius shared high sequence similarity and protein structures with homologs in nonlegumes. Overall, these results offer reasonable gene annotations and comparative analysis and also provided a glimpse into evolutional route of legume-specific isoflavonoid biosynthesis.\n\nHighlightIsoflavonoids are specialized plant metabolites, almost exclusive to legumes. We firstly provide evidence that evolutional origin of legume-specific isoflavonoid biosynthesis may be driven by gene duplications and functional specialization.