Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

  1. Jaemyung Choi
  2. David B Lyons
  3. Daniel Zilberman  Is a corresponding author
  1. John Innes Centre, United Kingdom
  2. John Innes Centre, Austria

Abstract

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically associated with small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

Data availability

Sequencing data have been deposited in GEO under accession code GSE179796.

The following data sets were generated

Article and author information

Author details

  1. Jaemyung Choi

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  2. David B Lyons

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  3. Daniel Zilberman

    Department of Cell and Developmental Biology, John Innes Centre, Klosterneuburg, Austria
    For correspondence
    daniel.zilberman@ist.ac.at
    Competing interests
    Daniel Zilberman, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0123-8649

Funding

H2020 European Research Council (725746)

  • Jaemyung Choi
  • David B Lyons
  • Daniel Zilberman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Richard Amasino, University of Wisconsin Madison, United States

Version history

  1. Preprint posted: July 31, 2021 (view preprint)
  2. Received: August 1, 2021
  3. Accepted: November 30, 2021
  4. Accepted Manuscript published: December 1, 2021 (version 1)
  5. Version of Record published: February 9, 2022 (version 2)

Copyright

© 2021, Choi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jaemyung Choi
  2. David B Lyons
  3. Daniel Zilberman
(2021)
Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin
eLife 10:e72676.
https://doi.org/10.7554/eLife.72676

Share this article

https://doi.org/10.7554/eLife.72676

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