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Chemical signalling in the plant microbiome can have drastic effects on microbial community structure, and on host growth and development. Previously, we demonstrated that the auxin metabolic signal interference performed by the bacterial genusVariovoraxvia an auxin degradation locus was essential for maintaining stereotypic root development in an ecologically relevant bacterial synthetic community. Here, we dissect theVariovoraxauxin degradation locus to define the genesiadDEas necessary and sufficient for indole-3-acetic acid (IAA) degradation and signal interference. We determine the crystal structures and binding properties of the operon’s MarR-family repressor with IAA and other auxins. Auxin degradation operons were identified across the bacterial tree of life and we define two distinct types on the basis of gene content and metabolic products:iac-like andiad-like. The structures of MarRs from representatives of each auxin degradation operon type establish that each has distinct IAA-binding pockets. Comparison of representative IAA-degrading strains from diverse bacterial genera colonizingArabidopsisplants show that while all degrade IAA, only strains containingiad-like auxin-degrading operons interfere with auxin signalling in a complex synthetic community context. This suggests thatiad-like operon-containing bacterial strains, includingVariovoraxspecies, play a key ecological role in modulating auxins in the plant microbiome.

ABSTRACT Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were performed in open systems or agricultural fields, which include a higher diversity of soil microorganisms. Here, we investigated how microbes affect the hormesis induced by low doses of glyphosate. To this end, we used Arabidopsis thaliana and a well-characterized synthetic bacterial community of 185 strains (SynCom) that mimics the root-associated microbiome of Arabidopsis . We found that a dose of 3.6 × 10 −6 g acid equivalent/liter (low dose of glyphosate, or LDG) produced an ∼14% increase in the shoot dry weight (i.e., hormesis) of uninoculated plants. Unexpectedly, in plants inoculated with the SynCom, LDG reduced shoot dry weight by ∼17%. We found that LDG enriched two Firmicutes and two Burkholderia strains in the roots. These specific strains are known to act as root growth inhibitors (RGI) in monoassociation assays. We tested the link between RGI and shoot dry weight reduction in LDG by assembling a new synthetic community lacking RGI strains. Dropping RGI strains out of the community restoredmore »growth induction by LDG. Finally, we showed that individual RGI strains from a few specific phyla were sufficient to switch the response to LDG from growth promotion to growth inhibition. Our results indicate that glyphosate hormesis was completely dependent on the root microbiome composition, specifically on the presence of root growth inhibitor strains. IMPORTANCE Since the introduction of glyphosate-resistant crops, glyphosate has become the most common and widely used herbicide around the world. Due to its intensive use and ability to bind to soil particles, it can be found at low concentrations in the environment. The effect of these remnants of glyphosate in plants has not been broadly studied; however, glyphosate 1,000 to 100,000 times less concentrated than the recommended field dose promoted growth in several species in laboratory and greenhouse experiments. However, this effect is rarely observed in agricultural fields, where complex communities of microbes have a central role in the way plants respond to external cues. Our study reveals how root-associated bacteria modulate the responses of Arabidopsis to low doses of glyphosate, shifting between growth promotion and growth inhibition.« less

Plants have an innate immune system to fight off potential invaders that is based on the perception of nonself or modified-self molecules. Microbe-associated molecular patterns (MAMPs) are evolutionarily conserved microbial molecules whose extracellular detection by specific cell surface receptors initiates an array of biochemical responses collectively known as MAMP-triggered immunity (MTI). Well-characterized MAMPs include chitin, peptidoglycan, and flg22, a 22-amino acid epitope found in the major building block of the bacterial flagellum, FliC. The importance of MAMP detection by the plant immune system is underscored by the large diversity of strategies used by pathogens to interfere with MTI and that failure to do so is often associated with loss of virulence. Yet, whether or how MTI functions beyond pathogenic interactions is not well understood. Here we demonstrate that a community of root commensal bacteria modulates a specific and evolutionarily conserved sector of theArabidopsisimmune system. We identify a set of robust, taxonomically diverse MTI suppressor strains that are efficient root colonizers and, notably, can enhance the colonization capacity of other tested commensal bacteria. We highlight the importance of extracellular strategies for MTI suppression by showing that the type 2, not the type 3, secretion system is required for the immunomodulatory activitymore »of one robust MTI suppressor. Our findings reveal that root colonization by commensals is controlled by MTI, which, in turn, can be selectively modulated by specific members of a representative bacterial root microbiota.

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