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Gene‐body chromatin modification dynamics mediate epigenome differentiation in Arabidopsis
Author(s) -
Inagaki Soichi,
Takahashi Mayumi,
Hosaka Aoi,
Ito Tasuku,
Toyoda Atsushi,
Fujiyama Asao,
Tarutani Yoshiaki,
Kakutani Tetsuji
Publication year - 2017
Publication title -
the embo journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 7.484
H-Index - 392
eISSN - 1460-2075
pISSN - 0261-4189
DOI - 10.15252/embj.201694983
Subject(s) - biology , demethylase , chromatin , genetics , gene silencing , regulation of gene expression , histone , microbiology and biotechnology , gene
Abstract Heterochromatin is marked by methylation of lysine 9 on histone H3 (H3K9me). A puzzling feature of H3K9me is that this modification localizes not only in promoters but also in internal regions (bodies) of silent transcription units. Despite its prevalence, the biological significance of gene‐body H3K9me remains enigmatic. Here we show that H3K9me‐associated removal of H3K4 monomethylation (H3K4me1) in gene bodies mediates transcriptional silencing. Mutations in an Arabidopsis H3K9 demethylase gene IBM 1 induce ectopic H3K9me2 accumulation in gene bodies, with accompanying severe developmental defects. Through suppressor screening of the ibm1 ‐induced developmental defects, we identified the LDL 2 gene, which encodes a homolog of conserved H3K4 demethylases. The ldl2 mutation suppressed the developmental defects, without suppressing the ibm1 ‐induced ectopic H3K9me2. The ectopic H3K9me2 mark directed removal of gene‐body H3K4me1 and caused transcriptional repression in an LDL 2‐dependent manner. Furthermore, mutations of H3K9 methylases increased the level of H3K4me1 in the gene bodies of various transposable elements, and this H3K4me1 increase is a prerequisite for their transcriptional derepression. Our results uncover an unexpected role of gene‐body H3K9me2/H3K4me1 dynamics as a mediator of heterochromatin silencing and epigenome differentiation.