Histone H3 lysine 4 methylation recruits DNA demethylases to enforce gene expression in Arabidopsis

  • Ming Wang
  • , Yan He
  • , Zhenhui Zhong
  • , Ashot Papikian
  • , Shuya Wang
  • , Jason Gardiner
  • , Basudev Ghoshal
  • , Suhua Feng
  • , Yasaman Jami-Alahmadi
  • , James A. Wohlschlegel
  • , Steven E. Jacobsen*
  • *Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Patterning of DNA methylation in eukaryotic genomes is controlled by de novo methylation, maintenance mechanisms and demethylation pathways. In Arabidopsis thaliana, DNA demethylation enzymes are clearly important for shaping methylation patterns, but how they are regulated is poorly understood. Here we show that the targeting of histone H3 lysine four trimethylation (H3K4me3) with the catalytic domain of the SDG2 histone methyltransferase potently erased DNA methylation and gene silencing at FWA and also erased CG DNA methylation in many other regions of the Arabidopsis genome. This methylation erasure was completely blocked in the ros1 dml2 dml3 triple mutant lacking DNA demethylation enzymes, showing that H3K4me3 promotes the active removal of DNA methylation. Conversely, we found that the targeted removal of H3K4me3 increased the efficiency of targeted DNA methylation. These results highlight H3K4me3 as a potent anti-DNA methylation mark and also pave the way for development of more powerful epigenome engineering tools.

Original languageEnglish
Pages (from-to)206-217
Number of pages12
JournalNature Plants
Volume11
Issue number2
DOIs
Publication statusPublished - Feb 2025
Externally publishedYes

Bibliographical note

Publisher Copyright:
© The Author(s) 2025.

Funding

We thank M. Akhavan and the Broad Stem Cell Research Center Biosequencing core for DNA sequencing; B. Strahl for designing the SDG2 catalytic mutation; M. Gehring for rdd mutant seeds; F. Berger for Arabidopsis H2A.Z antibody; and M. Liu, J. Zhou and C. Ng for technical support. This work was supported by a Bill and Melinda Gates Foundation grant (OPP1125410) to S.E.J. and George G. & Betsy H. Laties Graduate Fellowship in Molecular Plant Biology to S.W. S.E.J. is a Howard Hughes Medical Institute Investigator.

FundersFunder number
Bill and Melinda Gates FoundationOPP1125410

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