Chemical communication in the root microbiome

Abstract

The outcome of root-microbiome interactions determines the health and yield of crop plants. Besides detrimental pathogens, the root microbiome also harbors beneficial members that promote plant growth or stimulate plant health. For example some beneficial microbes can trigger an induced systemic resistance (ISR), a state in which plants are more resistant against a broad range of foliar pathogens and insect herbivores. Free-living beneficial rhizobacteria were previously found to suppress certain immune responses in Arabidopsis roots. We investigated such root immune modulation by the ISR‐eliciting rhizobacterium Pseudomonas capeferrum WCS358 (WCS358). We found that WCS358 requires the genes pqqF and cyoB for this immune suppression, both of which are involved in the oxidation of glucose to gluconic acid. Gluconic acid production lowers environmental pH in which the bacterium resides and this effectuates root immune suppression. Moreover, the mutation of pqqF reduced the rhizosphere colonization by WCS358, indicating that suppression of root immune responses enables the root colonization by WCS358. Root exudates also play a major role in shaping root microbiome. The root‐specific transcription factor MYB72 and the MYB72‐controlled β‐glucosidase BGLU42 had previously emerged as important regulators of ISR and iron uptake responses. Arabidopsis roots synthesize and secrete fluorescent phenolic compounds in a MYB72/BGLU42‐dependent manner when growing under iron deficiency. We investigated root exudates and found that coumarins are the dominant phenolic compounds produced under iron deficiency. Coumarins can have selective antimicrobial activity, but the ISR‐eliciting rhizobacteria Pseudomonas simiae WCS417 (WCS417) and WCS358 were highly insensitive. Moreover, coumarin‐deficient f6’h1 mutant plants assembled a distinct root microbiome, indicating that coumarins can shape the root microbiome and select tolerant microorganisms. We found that also WCS417 strongly affects the root metabolome, and that production of the coumarins scopolin, scopoletin and esculin was increased. We therefore hypothesize that by inducing coumarin exudation by the roots, coumarin-tolerant ISR-eliciting organisms promote their own colonization. We then studied the responses of WCS417 in response to coumarins in root exudates. We found that transport and metabolism of carbohydrates, amino acids, and nucleotides were induced, while cell motility, the bacterial mobilome, and energy production and conversion were repressed by coumarin containing root exudates. Moreover, these root exudates repressed the expression of cell‐motility related genes, likely by repressing flagellar biosynthesis. We speculate on how repression of motility might be part of a motility-to-biofilm-formation switch that could promote colonization of the plant root.