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.

Spatially Restricted Immune Responses Are Required for Maintaining Root Meristematic Activity upon Detection of Bacteria

“…It has been reported that some commensal bacteria are able to attenuate MAMP-triggered immune responses, either broadly or only the branches of the response that causes root growth inhibition, 53,54 which could explain this observation. Indeed, Ma et al 55 were unable to observe any growth phenotype of WER::FLS2 plants grown in non-sterile soil, which they explain by their finding that 41% of root commensals can suppress MAMP-triggered root growth inhibition in mono-associations. 55 Article suggesting that suppression of root growth inhibition can be achieved without full suppression of all transcriptional responses.…”

“…Indeed, Ma et al 55 were unable to observe any growth phenotype of WER::FLS2 plants grown in non-sterile soil, which they explain by their finding that 41% of root commensals can suppress MAMP-triggered root growth inhibition in mono-associations. 55 Article suggesting that suppression of root growth inhibition can be achieved without full suppression of all transcriptional responses.…”

Toward understanding microbiota homeostasis in the plant kingdom

“…In addition to defense hormones, recent studies have begun to show a critical role of pattern-triggered immunity (PTI) in regulating modulating microbiota homeostasis in plants [17,35,36]. PTI is a major form of plant immunity initiated by plant recognition of common microbial patterns by pattern-recognition receptors (PRRs) [37].…”

Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field

“…Although MAMP-detecting PRRs clearly regulate the interactions of many plant-microbe pairs, how they sculpt the complex plant microbiome is less clear. In a complex community, the effect of the plant immune system on a given microbe may depend on the activity of other community members, including immunosuppression (Ma et al, 2021;Teixeira et al, 2021). Furthermore, plants respond in a distinct manner to particular types of MAMPs (Vetter et al, 2016).…”