The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons

Abstract

MADS-box transcription factors (TFs) are ubiquitous in eukaryotic organisms and play major roles during plant development. Nevertheless, their function in seed development remains largely unknown. Here we show that the imprinted Arabidopsis thaliana MADS-box TF PHERES1 (PHE1) is a master regulator of paternally expressed imprinted genes, as well as of non-imprinted key regulators of endosperm development. PHE1 binding sites show distinct epigenetic modifications on maternal and paternal alleles, correlating with parental-specific transcriptional activity. Importantly, we show that the CArG-box-like DNA-binding motifs bound by PHE1 have been distributed by RC/Helitron transposable elements. Our data provide an example of molecular domestication of these elements, which by distributing PHE1 binding sites throughout the genome, have facilitated the recruitment of crucial endosperm regulators into a single transcriptional network.

Data availability

ChIP-seq data generated in this study is available at NCBI's Gene Expression Omnibus database (https://www.ncbi.nlm.nih.gov/geo/), under the accession number GSE129744.

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

Article and author information

Author details

  1. Rita A Batista

    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:" 0000-0002-2083-4622
  2. Jordi Moreno-Romero

    Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  3. Yichun Qiu

    Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  4. Joram van Boven

    Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. 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.
  6. Duarte D Figueiredo

    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:" 0000-0001-7990-3592
  7. 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

  • Claudia Köhler

Knut och Alice Wallenbergs Stiftelse

  • Claudia Köhler

Goran Gustafsson Foundation for Research in Natural Sciences and Medicine

  • Claudia Köhler

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, John Innes Centre, United Kingdom

Version history

  1. Received: July 26, 2019
  2. Accepted: November 30, 2019
  3. Accepted Manuscript published: December 2, 2019 (version 1)
  4. Version of Record published: December 16, 2019 (version 2)

Copyright

© 2019, Batista 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. Rita A Batista
  2. Jordi Moreno-Romero
  3. Yichun Qiu
  4. Joram van Boven
  5. Juan Santos-González
  6. Duarte D Figueiredo
  7. Claudia Köhler
(2019)
The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons
eLife 8:e50541.
https://doi.org/10.7554/eLife.50541

Share this article

https://doi.org/10.7554/eLife.50541

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