Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome

EMBO J. 2010 Oct 20;29(20):3496-506. doi: 10.1038/emboj.2010.227. Epub 2010 Sep 10.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Chromatin / metabolism
  • DNA Methylation
  • DNA Transposable Elements / genetics
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Plant*
  • Histone Demethylases / genetics*
  • Histone Demethylases / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Jumonji Domain-Containing Histone Demethylases
  • Mutation
  • Transcription, Genetic

Substances

  • Arabidopsis Proteins
  • Chromatin
  • DNA Transposable Elements
  • DNA-Binding Proteins
  • Histones
  • Histone Demethylases
  • IBM1 protein, Arabidopsis
  • Jumonji Domain-Containing Histone Demethylases