Dysfunction of histone demethylase IBM1 in Arabidopsis causes autoimmunity and reshapes the root microbiome

Root microbiota is important for plant growth and fitness. Little is known about 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 (INCREASE IN BONSAI METHYLATION 1) in Arabidopsis thaliana substantially reshaped the root microbiota, with the majority of the significant amplicon sequence variants (ASVs) being decreased. 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 several important defense regulators. Consistently, ibm1 mutants showed increased resistance to the pathogen Pseudomonas syringae DC3000 with stronger immune responses. In addition, ibm1 showed substantially impaired plant growth-promotion in response to beneficial bacteria; the impairment was partially mimicked by exogenous application of SA to wild type plants, and by a null mutation of AGP19 that is important for cell expansion and that is repressed with DNA hyper methylation in ibm1. IBM1-dependent epigenetic regulation imposes strong and broad impacts on plant-microbe interactions and thereby shapes the assembly of root microbiota. Overall design: BS-seq: soil-grown plants of ibm1-1 was compared with the Col-0, each genotype has 2 biological replicates; RNA-seq in soil: soil-grown plants of ibm1-1 was compared with the Col-0, and each genotype has 3 biological replicates; RNAseq in medium: MS-medium-grown seedlings of ibm1-1 was compared with Col-0, and each genotype has 2 biological replicates