Dysfunction of the histone demethylase IBM1 in Arabidopsis causes autoimmunity and reshapes the root-associated bacteria community

Root microbiota, the root-associated microbial community, is important for plant growth and fitness. It has been elusive whether and how the assembly of root microbiota may be controlled by epigenetic regulation, which is crucial for gene transcription and genome stability. Here we show that dysfunction of the histone demethylase IBM1 in Arabidopsis thaliana substantially reshaped the root microbiota in the rhizosphere and the endosphere, with the majority of the abundant community members (ACM) becoming less enriched in the mutants than the wild type plants. Transcriptome analyses of plants grown in soil and in sterile growth-medium jointly disclosed salicylic acid (SA)-mediated autoimmunity and production of the defense metabolite camalexin in the ibm1 mutants. Analyses of genome-wide histone modifications and DNA methylation highlighted epigenetic modifications permissive for transcription at the loci of a group of key defense regulators, including OM66, RLP23, CRK45, PNP-A, ADR1, and RMG1, which are concomitantly induced by IBM1 dysfunction. Compared to the wild type plants, ibm1 mutants showed increased resistance to the pathogen Psedomonas syringae DC3000, consistent with stronger immune responses including phosphorylation of MPK3 and MPK6 in response to the pathogen molecular pattern flg22. In addition, ibm1 showed substantially impaired beneficial-bacteria-induced plant growth-promotion; the impairment was partially mimicked by exogenous application of SA to wild type plants, as well as by a null mutation of AGP19 that is important for cell expansion and that is repressed with DNA hyper methylation in ibm1. Our findings demonstrate that IBM1-dependent epigenetic regulation imposes strong and broad impacts on plant-microbe interactions and thereby shapes the assembly of root microbiota.