Parasitism-evoked horizontal gene transfer between plants as a novel trigger for specialized metabolism evolution

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 made the striking observation that two parasitic dodders, Cuscuta campestris and C. australis, have enzymatically active homologues of SiCYP81Q1, which encodes piperitol/sesamin synthase (PSS), and accumulate their product sesamin as found in the phylogenetically remote plant Sesamum indicum (sesame). Notably, parasitism of sesame plants by C. campestris not only induced expression of SiCYP81Q1 of the host plant at the parasitic interface but also allowed for host-to-parasite transfer of intron-retained SiCYP81Q1 mRNA. Furthermore, sesamin synthase genes in dodders have remnants of poly(A) sequences and are integrated in regions that are otherwise syntenic among related species. These data suggest that PSS genes in Cuscuta spp. have been integrated to their genomes through parasitism-mediated horizontal gene transfer (pHGT) which was tightly associated with the PSS gene transcripts and provide insights into an unexpected role that pHGT might have played in the metabolic evolution of plants.