A novel triterpene biosynthetic network mediates Arabidopsis root microbiota assembly

lant secondary metabolites mediate plant-microbe interactions, yet the vast number of uncharacterized genes with predicted functions in specialized metabolism present in plant genomes suggests that such processes remain poorly understood. Here, we use biosynthetic gene cluster and co-expression analysis to uncover a hitherto undescribed triterpene biosynthetic network that operates in the roots of Arabidopsis thaliana. This network consists of functionally divergent biosynthetic gene clusters, connected by scattered (peripheral) genes encoding promiscuous acyltransferases and alcohol dehydrogenases. Collectively the network furnishes three new linked multi-step pathways for the previously unknown triterpenes thalianin and thalianyl medium-chain fatty acid esters, and the recently identified arabidin. A. thaliana mutants affected in the biosynthesis of these compounds have altered root microbiota composition that is enriched or depleted for specific bacteria from different taxonomic groups. In vitro bioassays with 14 pathway metabolites reveal that these compounds show selective growth promoting and inhibitory activities towards different bacterial isolates and have subtle structure-activity relationships, consistent with a role for this biosynthetic network in directly modulating the A. thaliana root microbiota.