1. Chromosomes and Gene Expression
  2. Plant Biology

Natural depletion of H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation

  1. Shengbo He
  2. Martin Vickers
  3. Jingyi Zhang
  4. Xiaoqi Feng  Is a corresponding author
  1. John Innes Centre, United Kingdom
https://doi.org/10.7554/eLife.42530
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  1. Shengbo He
  2. Martin Vickers
  3. Jingyi Zhang
  4. Xiaoqi Feng
(2019)
Natural depletion of H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation
eLife 8:e42530.
https://doi.org/10.7554/eLife.42530
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Abstract

Transposable elements (TEs), the movement of which can damage the genome, are epigenetically silenced in eukaryotes. Intriguingly, TEs are activated in the sperm companion cell – vegetative cell (VC) – of the flowering plant Arabidopsis thaliana. However, the extent and mechanism of this activation are unknown. Here we show that about 100 heterochromatic TEs are activated in VCs, mostly by DEMETER-catalyzed DNA demethylation. We further demonstrate that DEMETER access to some of these TEs is permitted by the natural depletion of linker histone H1 in VCs. Ectopically expressed H1 suppresses TEs in VCs by reducing DNA demethylation and via a methylation-independent mechanism. We demonstrate that H1 is required for heterochromatin condensation in plant cells and show that H1 overexpression creates heterochromatic foci in the VC progenitor cell. Taken together, our results demonstrate that the natural depletion of H1 during male gametogenesis facilitates DEMETER-directed DNA demethylation, heterochromatin relaxation, and TE activation.

Data availability

We have deposited our sequencing data in GEO (GSE120519). The reviewer token to access the data is: elarkuwehngpdad. Source data files have been provided for Figures 1 to 3.

The following data sets were generated
The following previously published data sets were used

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Author details

  1. Shengbo He

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3773-9995

  2. Martin Vickers

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  3. Jingyi Zhang

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  4. Xiaoqi Feng

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    For correspondence
    xiaoqi.feng@jic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4008-1234

Funding

Biotechnology and Biological Sciences Research Council (BBL0250431)

  • Jingyi Zhang
  • Xiaoqi Feng

Gatsby Charitable Foundation

  • Shengbo He
  • Xiaoqi Feng

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

Copyright

© 2019, He 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. Shengbo He
  2. Martin Vickers
  3. Jingyi Zhang
  4. Xiaoqi Feng
(2019)
Natural depletion of H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation
eLife 8:e42530.
https://doi.org/10.7554/eLife.42530

Share this article

https://doi.org/10.7554/eLife.42530

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