Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis

  1. Leonardo Furci
  2. Ritushree Jain
  3. Joost Stassen
  4. Oliver Berkowitz
  5. James Whelan
  6. David Roquis
  7. Victoire Baillet
  8. Vincent Colot
  9. Frank Johannes
  10. Jurriaan Ton  Is a corresponding author
  1. University of Sheffield, United Kingdom
  2. La Trobe University, Australia
  3. Technical University of Munich, Germany
  4. Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale), PSL Université Paris, France

Abstract

Variation in DNA methylation enables plants to inherit traits independently of changes to DNA sequence. Here, we have screened an Arabidopsis population of epigenetic recombinant inbred lines (epiRILs) for resistance against Hyaloperonospora arabidopsidis (Hpa). These lines share the same genetic background, but show variation in heritable patterns of DNA methylation. We identified 4 epigenetic quantitative trait loci (epiQTLs) that provide quantitative resistance without reducing plant growth or resistance to other (a)biotic stresses. Phenotypic characterisation and RNA-sequencing analysis revealed that Hpa-resistant epiRILs are primed to activate defence responses at the relatively early stages of infection. Collectively, our results show that hypomethylation at selected pericentromeric regions is sufficient to provide quantitative disease resistance, which is associated with genome-wide priming of defence-related genes. Based on comparisons of global gene expression and DNA methylation between the wild-type and resistant epiRILs, we discuss mechanisms by which the pericentromeric epiQTLs could regulate the defence-related transcriptome.

Data availability

Transcriptome sequencing and bisulfite sequencing reads are available from the European Nucleotide Archive (ENA) under accession code PRJEB26953

The following data sets were generated
    1. Furci et al
    (2018) RNA-seq and WBGS
    European Nucleotide Archive, PRJEB26953.
The following previously published data sets were used

Article and author information

Author details

  1. Leonardo Furci

    Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Ritushree Jain

    Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Joost Stassen

    Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5483-325X
  4. Oliver Berkowitz

    Department of Animal, Plant and Soil Science, ARC Centre of Excellence in Plant Energy Biology, La Trobe University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7671-6983
  5. James Whelan

    Department of Animal, Plant and Soil Science, ARC Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. David Roquis

    Department of Plant Sciences, Technical University of Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Victoire Baillet

    Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale), PSL Université Paris, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Vincent Colot

    Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale), PSL Université Paris, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6382-1610
  9. Frank Johannes

    Department of Plant Sciences, Technical University of Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Jurriaan Ton

    Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom
    For correspondence
    j.ton@sheffield.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8512-2802

Funding

Leverhulme Trust (RL-2012-042)

  • Jurriaan Ton

H2020 European Research Council (RL-2012-042)

  • Jurriaan Ton

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 J Kliebenstein, University of California, Davis, United States

Version history

  1. Received: July 31, 2018
  2. Accepted: January 3, 2019
  3. Accepted Manuscript published: January 4, 2019 (version 1)
  4. Version of Record published: January 22, 2019 (version 2)

Copyright

© 2019, Furci 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. Leonardo Furci
  2. Ritushree Jain
  3. Joost Stassen
  4. Oliver Berkowitz
  5. James Whelan
  6. David Roquis
  7. Victoire Baillet
  8. Vincent Colot
  9. Frank Johannes
  10. Jurriaan Ton
(2019)
Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis
eLife 8:e40655.
https://doi.org/10.7554/eLife.40655

Share this article

https://doi.org/10.7554/eLife.40655

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