The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana

Heike Wollmann, Hume Stroud, Ramesh Yelagandula, Yoshiaki Tarutani, Danhua Jiang, Li Jing, Bhagyshree Jamge, Hidenori Takeuchi, Sarah Holec, Xin Nie, Tetsuji Kakutani, Steven E. Jacobsen, Frédéric Berger

Research output: Contribution to journalArticlepeer-review

Abstract

Background: Gene bodies of vertebrates and flowering plants are occupied by the histone variant H3.3 and DNA methylation. The origin and significance of these profiles remain largely unknown. DNA methylation and H3.3 enrichment profiles over gene bodies are correlated and both have a similar dependence on gene transcription levels. This suggests a mechanistic link between H3.3 and gene body methylation. Results: We engineered an H3.3 knockdown in Arabidopsis thaliana and observed transcription reduction that predominantly affects genes responsive to environmental cues. When H3.3 levels are reduced, gene bodies show a loss of DNA methylation correlated with transcription levels. To study the origin of changes in DNA methylation profiles when H3.3 levels are reduced, we examined genome-wide distributions of several histone H3 marks, H2A.Z, and linker histone H1. We report that in the absence of H3.3, H1 distribution increases in gene bodies in a transcription-dependent manner. Conclusions: We propose that H3.3 prevents recruitment of H1, inhibiting H1's promotion of chromatin folding that restricts access to DNA methyltransferases responsible for gene body methylation. Thus, gene body methylation is likely shaped by H3.3 dynamics in conjunction with transcriptional activity.

Original languageEnglish (US)
Article number94
JournalGenome biology
Volume18
Issue number1
DOIs
StatePublished - May 18 2017
Externally publishedYes

Keywords

  • Chromatin
  • DNA methylation
  • H2A.Z
  • H3.3
  • Histone variants
  • Linker histone H1

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

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