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

Abstract
Data availability
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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

1. He S
2. Vickers M
3. Zhang J
4. Feng X
(2018) Developmental depletion of histone H1 in Arabidopsis sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation
NCBI Gene Expression Omnibus, GSE120519.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE120519

The following previously published data sets were used

1. Nishimura T
2. Zilberman D
(2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes
NCBI Gene Expression Omnibus, GSE38935.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE38935
1. Wilczynski B
2. Rutowicz K
(2015) Analysis of genomic distribution of three linker histone variants in Arabidopsis under normal and low light conditions, by ChIP-chip
ArrayExpress, E-MTAB-2804.

https://www.ebi.ac.uk/arrayexpress/experiments/E-MTAB-2804/
1. Stroud H
(2013) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis
NCBI Gene Expression Omnibus, GSE51304.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE51304
1. Zilberman D
2. Nishimura T
(2012) EMF1 and PRC2 Cooperate to Repress Key Regulators of Arabidopsis Development
NCBI Gene Expression Omnibus, GSE34689.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE34689
(2011) Establishing a reference epigenome in arabidopsis seedlings
NCBI Gene Expression Omnibus, GSE24710.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE24710

Article and author information

Author details

Shengbo He

Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3773-9995
Martin Vickers

Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Jingyi Zhang

Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

Competing interests
The authors declare that no competing interests exist.
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.

"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

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.