The Root, the Microbiome and the Secreted Metabolome in-between

Microbial communities associated with roots confer specific functions to their hosts, thereby modulating plant growth, health and productivity. Yet, seminal questions remain largely unaddressed including whether and how the rhizosphere microbiome modulates root metabolism and exudation and, consequently, how do plants fine-tune this complex belowground web of interactions? We found that, through a process termed Systemically Induced Root Exudation of Metabolites (SIREM), different microbial communities induce specific systemic changes in tomato root exudation. For instance, systemic exudation of acylsugars secondary metabolites is triggered by local colonization of bacteria affiliated with the genus Bacillus. Moreover, both leaf and systemic root metabolomes and transcriptomes change according to the rhizosphere microbial community structure. Analysis of the systemic root metabolome points to glycosylated azelaic acid as a potential microbiome-induced signaling molecule that is subsequently exuded as free azelaic acid. Our results demonstrate that rhizosphere microbiome assembly drives the SIREM process at the molecular and chemical levels. It highlights a thus far unexplored long-distance signaling phenomenon that may regulate soil conditioning.