Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements

  1. David Secco
  2. Chuang Wang
  3. Huixia Shou
  4. Matthew D Schultz
  5. Serge Chiarenza
  6. Laurent Nussaume
  7. Joseph R Ecker
  8. James Whelan
  9. Ryan Lister  Is a corresponding author
  1. The University of Western Australia, Australia
  2. Zhejiang University, China
  3. Salk Institute for Biological Studies, United States
  4. Université d'Aix-Marseille, France
  5. La Trobe University, Australia

Abstract

Cytosine DNA methylation (mC) is a genome modification that can regulate the expression of coding and non-coding genetic elements. However, little is known about the involvement of mC in response to environmental cues. Using whole genome bisulfite sequencing to assess the spatio-temporal dynamics of mC in rice grown under phosphate starvation and recovery conditions, we identified widespread phosphate starvation-induced changes in mC, preferentially localized in transposable elements (TEs) close to highly induced genes. These changes in mC occurred after changes in nearby gene transcription, were mostly DCL3a-independent, could partially be propagated through mitosis, however no evidence of meiotic transmission was observed. Similar analyses performed in Arabidopsis revealed a very limited effect of phosphate starvation on mC, suggesting a species-specific mechanism. Overall, this suggests that TEs in proximity to environmentally induced genes are silenced via hypermethylation, and establishes the temporal hierarchy of transcriptional and epigenomic changes in response to stress.

Article and author information

Author details

  1. David Secco

    ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia
    Competing interests
    The authors declare that no competing interests exist.
  2. Chuang Wang

    State Key laboratory of Plant Physiology and Biochemistry, College of Life Science, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Huixia Shou

    State Key laboratory of Plant Physiology and Biochemistry, College of Life Science, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Matthew D Schultz

    Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Serge Chiarenza

    UMR 6191 CEA, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement des Plantes, Université d'Aix-Marseille, Saint-Paul-lez-Durance, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Laurent Nussaume

    UMR 6191 CEA, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement des Plantes, Université d'Aix-Marseille, Saint-Paul-lez-Durance, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Joseph R Ecker

    Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. James Whelan

    Department of Botany, School of Life Science, ARC Centre of Excellence in Plant Energy Biology, La Trobe University, Bundoora, Australia
    Competing interests
    The authors declare that no competing interests exist.
  9. Ryan Lister

    ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia
    For correspondence
    ryanlister@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: June 10, 2015
  2. Accepted: July 20, 2015
  3. Accepted Manuscript published: July 21, 2015 (version 1)
  4. Version of Record published: August 18, 2015 (version 2)

Copyright

© 2015, Secco 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

  • 7,494
    views
  • 1,882
    downloads
  • 255
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. David Secco
  2. Chuang Wang
  3. Huixia Shou
  4. Matthew D Schultz
  5. Serge Chiarenza
  6. Laurent Nussaume
  7. Joseph R Ecker
  8. James Whelan
  9. Ryan Lister
(2015)
Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements
eLife 4:e09343.
https://doi.org/10.7554/eLife.09343

Share this article

https://doi.org/10.7554/eLife.09343

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.

    1. Genetics and Genomics
    Can Hu, Xue-Ting Zhu ... Jin-Qiu Zhou
    Research Article

    Telomeres, which are chromosomal end structures, play a crucial role in maintaining genome stability and integrity in eukaryotes. In the baker’s yeast Saccharomyces cerevisiae, the X- and Y’-elements are subtelomeric repetitive sequences found in all 32 and 17 telomeres, respectively. While the Y’-elements serve as a backup for telomere functions in cells lacking telomerase, the function of the X-elements remains unclear. This study utilized the S. cerevisiae strain SY12, which has three chromosomes and six telomeres, to investigate the role of X-elements (as well as Y’-elements) in telomere maintenance. Deletion of Y’-elements (SY12), X-elements (SY12XYΔ+Y), or both X- and Y’-elements (SY12XYΔ) did not impact the length of the terminal TG1-3 tracks or telomere silencing. However, inactivation of telomerase in SY12, SY12XYΔ+Y, and SY12XYΔ cells resulted in cellular senescence and the generation of survivors. These survivors either maintained their telomeres through homologous recombination-dependent TG1-3 track elongation or underwent microhomology-mediated intra-chromosomal end-to-end joining. Our findings indicate the non-essential role of subtelomeric X- and Y’-elements in telomere regulation in both telomerase-proficient and telomerase-null cells and suggest that these elements may represent remnants of S. cerevisiae genome evolution. Furthermore, strains with fewer or no subtelomeric elements exhibit more concise telomere structures and offer potential models for future studies in telomere biology.