Phylogenomic and synteny analysis of BAHD and SCP/SCPL gene families reveal their evolutionary histories in plant specialized metabolism

Plant chemical diversity is largely owing to a number of enzymes which catalyse reactions involved in the assembly, and in the subsequent chemical modifications, of the core structures of major classes of plant specialized metabolites. One such reaction is acylation. With this in mind, to study the deep evolutionary history of BAHD and the serine-carboxypeptidase-like (SCPL) acyltransferase genes, we assembled phylogenomic synteny networks based on a large-scale inference analysis of orthologues across whole-genome sequences of 126 species spanning Stramenopiles and Archaeplastida, including Arabidopsis thaliana , tomato ( Solanum lycopersicum ) and maize ( Zea mays ). As such, this study combined the study of genomic location with changes in gene sequences. Our analyses revealed that serine-carboxypeptidase (SCP)/serine-carboxypeptidase-like (SCPL) genes had a deeper evolutionary origin than BAHD genes, which expanded massively on the transition to land and with the development of the vascular system. The two gene families additionally display quite distinct patterns of copy number variation across phylogenies as well as differences in cross-phylogenetic syntenic network components. In unlocking the above observations, our analyses demonstrate the possibilities afforded by modern phylogenomic (syntenic) networks, but also highlight their current limitations, as demonstrated by the inability of phylogenetic methods to separate authentic SCPL acyltransferases from standard SCP peptide hydrolases. This article is part of the theme issue ‘The evolution of plant metabolism’.