Natural depletion of H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation
- John Innes Centre, United Kingdom
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.
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Active DNA demethylation in plant companion cells reinforces transposon methylation in gametesNCBI Gene Expression Omnibus, GSE38935.
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Non-CG methylation patterns shape the epigenetic landscape in ArabidopsisNCBI Gene Expression Omnibus, GSE51304.
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EMF1 and PRC2 Cooperate to Repress Key Regulators of Arabidopsis DevelopmentNCBI Gene Expression Omnibus, GSE34689.
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Establishing a reference epigenome in arabidopsis seedlingsNCBI Gene Expression Omnibus, GSE24710.
Article and author information
Author details
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.
Reviewing Editor
- Richard Amasino, University of Wisconsin Madison, United States
Version history
- Received: October 8, 2018
- Accepted: May 26, 2019
- Accepted Manuscript published: May 28, 2019 (version 1)
- Version of Record published: June 26, 2019 (version 2)
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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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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