Multi-omics of the nasturtium (Tropaeolum majus) and the parallel evolution of the erucic acid biosynthesis in angiosperms.

Erucic acid is a widely used raw material in industry, and it can be synthesized in the seeds of a number of plants, including Tropaeolum majus (nasturtium), an herbaceous vine in Tropaeolaceae. In this study, using a newly assembled chromosome-level nasturtium genome, we screened candidate genes encoding the rate-limiting enzymes involved in the nasturtium erucic acid biosynthesis. After genome-wide identification and expression profiling, nine out of 25 3-ketoacyl-CoA synthase (KCS) genes were found to be expressed in nasturtium seed, while further expression pattern clustering divided the nine genes into three categories based on their preferential expression in five different seed developmental stages. The yeast transformation experiments of selected candidates validated the functional roles of TmKCS11, TmFAE and TmKCS19 in erucic acid biosynthesis. These three KCS genes putatively involved in erucic acid production showed higher expression during seed development. Finally, phylogenetic and comparative genomic analyses indicate that WGD and local tandem duplication events have contributed to KCS family expansion in nasturtium and have served as recurrent evolutionary drivers across diverse plant lineages, repeatedly facilitating the independent acquisition of erucic acid biosynthetic capacity. The parallel evolution of this enzymatic activity through gene family reuse across angiosperms highlights a recurring metabolic strategy and provides insights into the general mechanisms underlying lineage-specific specialized metabolite evolution.