Parasitism-mediated horizontal transfer of a functional cytochrome P450 gene entails transposon colonization in newly gained introns

Abstract

Plants produce a wide variety of specialized metabolites that are typically present only in specific lineages. However, some specialized metabolites are found sporadically across distantly related plant species. While the latter cases have been explained as outcomes of convergent evolution, the molecular mechanism behind such metabolic evolution has remained largely elusive. Here, we report that parasitic dodders belonging to the genus Cuscuta accumulate sesamin, and that this accumulation may be attributed to the acquisition of enzymatically active homologs of Sesamum indicum CYP81Q1, which encodes piperitol/sesamin synthase (PSS). Phylogenetic analysis of CYP81Q homologs in Cuscuta and Grammica subgenera supports a trajectory in which ancestral Cuscuta species acquired CYP81Q from an ancestral host plant of Lamiales through horizontal gene transfer (HGT), and that the gene has been maintained during the speciation of Cuscuta. The evolution of the CYP81Q genes was accompanied by sequential intron gains, which likely involved the colonization of transposons. Experiments involving C. campestris and S. indicum suggested that expression of the host CYP81Q gene could be induced by parasitism, and physical connection to the host plant allowed the transfer of genetic elements to Cuscuta. These data suggest that parasitism-mediated HGT contributed to the transfer of a gene encoding a key enzyme in specialized lignan metabolism to Cuscuta, and that the acquired metabolic gene underwent structural modification while retaining its enzymatic function in dodders.