Assistant Professor University of California, Davis Davis, California
Plant specialized metabolites are used by humans as medicines, food additives and natural insecticides. Solanaceae family plants synthesize herbivory defensive acylated sugars in the tip cells of glandular trichomes. Acylsugars show striking structural variety within the family, providing an ideal system for investigating the mechanisms of metabolic innovation. Here we explored the common black nightshade (Solanum nigrum) that makes an unusually large number (~100) of different acylsugars in their trichome hairs. We developed methods to structurally analyze acylsugar mixtures by 2D NMR, which led to the insight that the Old World species black nightshade accumulates acylglucoses and acylinositols in the same tissue. Detailed in vitro biochemistry, cross-validated by in vivo virus-induced gene silencing, revealed two unique features of the four-step acylglucose biosynthetic pathway: A trichome-expressed, neofunctionalized invertase-like enzyme, SnASFF1 (S. nigrum acylsucrose fructofuranosidase 1), converts BAHD-produced acylsucroses to acylglucoses, which, in turn, are substrates for a novel acylglucose acyltransferase (SnAGAT1). Requirement of SnASFF1 makes S. nigrum acylglucose biosynthesis superficially similar to wild tomato (Solanum pennellii) acylglucose biosynthesis, where SpASFF1 enzyme converts triacylsucroses to triacylglucoses. However, our results reveal that the S. nigrum pathway evolved independently, with cooption of the neofunctionalized SnASFF1 from a distinct lineage of the invertase gene phylogeny. These results demonstrate the dynamic nature of acylsugar biosynthesis with independent examples of primary metabolic
enzyme cooption and variation in BAHD acyltransferases. These discoveries also warrant investigation of the advantage behind convergent evolution of acylsugar sugar cores.