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 hypermethylation in ibm1. IBM1-dependent epigenetic regulation imposes strong and broad impacts on plant-microbe interactions and thereby shapes the assembly of root microbiota.

根系微生物群对植物生长和健康很重要。关于根系微生物群的组装是否以及如何受到表观遗传调控的控制知之甚少，这对于基因转录和基因组稳定性至关重要。在这里，我们显示拟南芥中组蛋白去甲基化酶 IBM1（BONSAI 甲基化 1 增加）的功能障碍显着重塑了根部微生物群，大多数重要的扩增子序列变体 (ASV) 减少。在土壤和无菌生长培养基中生长的植物的转录组分析共同揭示了水杨酸 (SA) 介导的自身免疫和 ibm1 中防御代谢物 camalexin 的产生突变体。对全基因组组蛋白修饰和 DNA 甲基化的分析强调了表观遗传修饰允许在几个重要的防御调节因子处进行转录。一致地，ibm1突变体表现出对病原体丁香假单胞菌DC3000 的抗性增加，具有更强的免疫反应。此外，对有益细菌的反应， ibm1对植物生长的促进作用显着受损。通过将 SA 外源性应用到野生型植物，以及对细胞扩增很重要且在 ibm1 中被 DNA 高甲基化抑制的AGP19无效突变，部分模拟了这种损伤. IBM1 依赖性表观遗传调控对植物与微生物的相互作用产生了强烈而广泛的影响，从而塑造了根系微生物群的组装。