Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy

  1. Hikaru Sato
  2. Juan Santos-González
  3. Claudia Köhler  Is a corresponding author
  1. Swedish University of Agricultural Sciences, Sweden

Abstract

Polycomb Repressive Complex 2 (PRC2)-mediated trimethylation of histone H3 on lysine 27 (H3K27me3) and methylation of histone 3 on lysine 9 (H3K9me) are two repressive epigenetic modifications that are typically localized in distinct regions of the genome. For reasons unknown, however, they co-occur in some organisms and special tissue types. In this study, we show that maternal alleles marked by H3K27me3 in the Arabidopsis endosperm were targeted by the H3K27me3 demethylase REF6 and became activated during germination. In contrast, maternal alleles marked by H3K27me3, H3K9me2, and CHG methylation (CHGm) are likely to be protected from REF6 targeting and remained silenced. Our study unveils that combinations of different repressive epigenetic modifications time a key adaptive trait by modulating access of REF6.

Data availability

All data generated in this study were deposited to the Gene Expression Omnibus and are available under the accession number GSE158907.

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

Article and author information

Author details

  1. Hikaru Sato

    Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7628-0414
  2. Juan Santos-González

    Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8712-9776
  3. Claudia Köhler

    Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
    For correspondence
    claudia.kohler@slu.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2619-4857

Funding

Vetenskapsrådet (2017-04119)

  • Claudia Köhler

Knut och Alice Wallenbergs Stiftelse (2018-0206)

  • Claudia Köhler

Goran Gustafsson Foundation for Research in Natural Sciences and Medicine

  • Claudia Köhler

The Human Frontier Science Program (LT000162/2018-L)

  • Hikaru Sato

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

Reviewing Editor

  1. Daniel Zilberman, Institute of Science and Technology Austria, Austria

Version history

  1. Received: November 4, 2020
  2. Preprint posted: November 12, 2020 (view preprint)
  3. Accepted: August 23, 2021
  4. Accepted Manuscript published: August 24, 2021 (version 1)
  5. Version of Record published: August 31, 2021 (version 2)

Copyright

© 2021, Sato 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.

Metrics

  • 1,441
    Page views
  • 299
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Hikaru Sato
  2. Juan Santos-González
  3. Claudia Köhler
(2021)
Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy
eLife 10:e64593.
https://doi.org/10.7554/eLife.64593

Share this article

https://doi.org/10.7554/eLife.64593

Further reading

    1. Chromosomes and Gene Expression
    Rachel A Johnston, Katherine A Aracena ... Jenny Tung
    Research Advance

    Previously, we showed that a massively parallel reporter assay, mSTARR-seq, could be used to simultaneously test for both enhancer-like activity and DNA methylation-dependent enhancer activity for millions of loci in a single experiment (Lea et al., 2018). Here, we apply mSTARR-seq to query nearly the entire human genome, including almost all CpG sites profiled either on the commonly used Illumina Infinium MethylationEPIC array or via reduced representation bisulfite sequencing. We show that fragments containing these sites are enriched for regulatory capacity, and that methylation-dependent regulatory activity is in turn sensitive to the cellular environment. In particular, regulatory responses to interferon alpha (IFNA) stimulation are strongly attenuated by methyl marks, indicating widespread DNA methylation-environment interactions. In agreement, methylation-dependent responses to IFNA identified via mSTARR-seq predict methylation-dependent transcriptional responses to challenge with influenza virus in human macrophages. Our observations support the idea that pre-existing DNA methylation patterns can influence the response to subsequent environmental exposures—one of the tenets of biological embedding. However, we also find that, on average, sites previously associated with early life adversity are not more likely to functionally influence gene regulation than expected by chance.

    1. Chromosomes and Gene Expression
    Masaaki Sokabe, Christopher S Fraser
    Insight

    A new in vitro system called Rec-Seq sheds light on how mRNA molecules compete for the machinery that translates their genetic sequence into proteins.