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Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling

Elisa Korenblum,Yonghui Dong,J. Szymański,S. Panda,A. Jozwiak,H. Massalha,S. Meir,I. Rogachev,A. Aharoni

Published 2020 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Root exudation of metabolites is an important mediator of plant interactions with soil microbes. Here we demonstrate that the tomato rhizosphere microbiome affects the chemical composition of root exudation through a systemic root–root signaling mechanism. We termed this process SIREM (systemically induced root exudation of metabolites) and showed that specific microbial colonization of the “local-side” root modulates the exudate composition at the “systemic side.” For example, Bacillus subtilis modulates systemic exudation of the renowned acylsugars insecticides. We also discovered that glycosylated azelaic acid is microbiome induced and might act in SIREM. The results suggest that microbiome-reprogrammed systemic root exudation promotes soil conditioning and pave the way for deeper understanding of how microbiota modulate root metabolism and secretion. 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 plants fine tune this complex belowground web of interactions. Here we show 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.

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