Elisa Korenblum, Yonghui Dong, Jedrzej Szymanski, Sayantan Panda, Adam Jozwiak, Hassan Massalha, Sagit Meir, Ilana Rogachev, and Asaph Aharoni

PNAS February 18, 2020 117 (7) 3874-3883

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.

Abstract

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.

See https://www.pnas.org/content/117/7/3874

Figure 1: Linking local-side root microbiome diversity to the chemical composition of systemic root exudation. (A) Schematic representation of the split-root hydroponics experimental design. Local-side roots of the split-root set-up were inoculated with soil microbiome, established using the dilution-to-extinction approach; HD, MD, or LD diversity microbiomes and exudate samples were collected from the systemic side. (B) Alpha diversity indices of root microbiomes (local side) measured 7 d postinoculation. Number of species (richness) or Shannon index gradually decreased among HD, MD, LD microbiomes (asterisks denote difference in alpha diversity indices, *P < 0.05, ***P < 0.0005, ANOVA followed by Tukey’s honestly significant difference (HSD) post hoc multiple comparison). (C) Bar plots of relative abundances of the top four phyla in each root microbiome (HD, MD, and LD) after 7 d of inoculation. Data are the average of six biological replicates. OTU abundance (97% similarity) and assigned taxonomic classifications used to construct this panel can be found in Dataset S1C. The bacterial relative abundance displayed at the phylum level for all individual samples can be found in SI Appendix, Fig. S3B.