Coordination of microbe-host homeostasis via a crosstalk with plant innate immunity

Abstract Asymptomatic plants grown in natural soil are colonized by phylogenetically structured communities of microbes known as the microbiota. Individual microbes can activate microbe-associated molecular pattern (MAMP)-triggered immunity (MTI), which limits pathogen proliferation but curtails plant growth, a phenomenon known as the growth-defense trade-off. We report that in mono-associations, 41% (62/151) of taxonomically diverse root bacterial commensals suppress Arabidopsis thaliana root growth inhibition (RGI) triggered by immune-stimulating MAMPs or damage-associated molecular patterns. Amplicon sequencing of bacteria 16S rRNA genes reveal that immune activation alters the profile of synthetic communities (SynComs) comprised of RGI-non-suppressive strains, while the presence of RGI-suppressive strains attenuates this effect. Root colonization by SynComs with different complexities and RGI-suppressive activities alters the expression of 174 core host genes with functions related to root development and nutrient transport. Further, RGI-suppressive SynComs specifically downregulate a subset of immune-related genes. Pre-colonization with RGI-suppressive SynComs, or mutation of one commensal-downregulated transcription factor, MYB15, render plants more susceptible to opportunistic Pseudomonas pathogens. Our results suggest that RGI-non-suppressive and suppressive root commensals modulate host susceptibility to pathogens by either eliciting or dampening MTI responses, respectively. This interplay buffers the plant immune system against pathogen perturbation and defense-associated growth inhibition, ultimately leading to commensal-host homeostasis.