Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome

• Published in: The EMBO journal Vol. 29; no. 20; pp. 3496 - 3506
• Main Authors: Inagaki, Soichi, Miura-Kamio, Asuka, Nakamura, Yasukazu, Lu, Falong, Cui, Xia, Cao, Xiaofeng, Kimura, Hiroshi, Saze, Hidetoshi, Kakutani, Tetsuji
• Format: Journal Article
• Language: English
• Published: Chichester, UK John Wiley & Sons, Ltd 20.10.2010; Nature Publishing Group UK; Springer Nature B.V; Nature Publishing Group
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Botany; chromatin; Chromatin - metabolism; Deoxyribonucleic acid; DNA; DNA Methylation; DNA Transposable Elements - genetics; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; EMBO09; EMBO30; Epigenesis, Genetic; Epigenetics; Gene Expression Regulation, Plant; Genomics; histone demethylase; Histone Demethylases - genetics; Histone Demethylases - metabolism; Histones - genetics; Histones - metabolism; IBM1; Jumonji Domain-Containing Histone Demethylases; Methylation; Molecular biology; Mutation; Transcription, Genetic; transposon; transposon; DNA methylation; chromatin; histone demethylase; IBM1
• ISSN: 0261-4189; 1460-2075; 1460-2075
• DOI: 10.1038/emboj.2010.227

In diverse eukaryotes, constitutively silent sequences, such as transposons and repeats, are marked by methylation at histone H3 lysine 9 (H3K9me). Although selective H3K9me is critical for maintaining genome integrity, mechanisms to exclude H3K9me from active genes remain largely unexplored. Here, we show in Arabidopsis that the exclusion depends on a histone demethylase gene, IBM1 (increase in BONSAI methylation). Loss‐of‐function ibm1 mutation results in ectopic H3K9me and non‐CG methylation in thousands of genes. The ibm1 ‐induced genic H3K9me depends on both histone methylase KYP/SUVH4 and DNA methylase CMT3, suggesting interdependence of two epigenetic marks—H3K9me and non‐CG methylation. Notably, IBM1 enhances loss of H3K9me in transcriptionally de‐repressed sequences. Furthermore, disruption of transcription in genes induces ectopic non‐CG methylation, which mimics the loss of IBM1 function. We propose that active chromatin is stabilized by an autocatalytic loop of transcription and H3K9 demethylation. This process counteracts a similarly autocatalytic accumulation of silent epigenetic marks, H3K9me and non‐CG methylation. The mechanisms by which heterochromatic modifications are excluded from active genes are not well understood. This study demonstrates that H3K9 demethylation by IBM1 depends on the transcription of target genes, preventing them from accumulating silent epigenetic marks.