Epigenetic silencing of a multifunctional plant stress regulator

  1. Mark Zander
  2. Björn C Willige
  3. Yupeng He
  4. Thu A Nguyen
  5. Amber E Langford
  6. Ramlah Nehring
  7. Elizabeth Howell
  8. Robert McGrath
  9. Anna Bartlett
  10. Rosa Castanon
  11. Joseph R Nery
  12. Huaming Chen
  13. Zhuzhu Zhang
  14. Florian Jupe
  15. Anna Stepanova
  16. Robert J Schmitz
  17. Mathew Lewsey
  18. Joanne Chory
  19. Joseph R Ecker  Is a corresponding author
  1. Salk Institute for Biological Studies, United States
  2. Howard Hughes Medical Institute, Salk Institute for Biological Studies, United States

Abstract

The central regulator of the ethylene (ET) signaling pathway, which controls a plethora of developmental programs and responses to environmental cues in plants, is ETHYLENE-INSENSITIVE2 (EIN2). Here we identify a chromatin-dependent regulatory mechanism at EIN2 requiring two genes: ETHYLENE-INSENSITIVE6 (EIN6), which is a H3K27me3 demethylase also known as RELATIVE OF EARLY FLOWERING6 (REF6), and EIN6 ENHANCER (EEN), the Arabidopsis homolog of the yeast INO80 chromatin remodeling complex subunit IES6 (INO EIGHTY SUBUNIT). Strikingly, EIN6 (REF6) and the INO80 complex redundantly control the level and the localization of the repressive histone modification H3K27me3 and the histone variant H2A.Z at the 5' untranslated region (5'UTR) intron of EIN2. Concomitant loss of EIN6 (REF6) and the INO80 complex shifts the chromatin landscape at EIN2 to a repressive state causing a dramatic reduction of EIN2 expression. These results uncover a unique type of chromatin regulation which safeguards the expression of an essential multifunctional plant stress regulator.

Data availability

Sequence data have been deposited in GEO under accession GSE122314.An overview of all sequenced data is given in Supplementary File 2.Visualized sequencing data can be found under http://neomorph.salk.edu/ein6een.php

The following data sets were generated

Article and author information

Author details

  1. Mark Zander

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Björn C Willige

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yupeng He

    Genomic Analysis Laboratory, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Thu A Nguyen

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Amber E Langford

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Ramlah Nehring

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Elizabeth Howell

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Robert McGrath

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Anna Bartlett

    Genomic Analysis Laboratory, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Rosa Castanon

    Genomic Analysis Laboratory, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Joseph R Nery

    Genomic Analysis Laboratory, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Huaming Chen

    Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Zhuzhu Zhang

    Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Florian Jupe

    Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Anna Stepanova

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Robert J Schmitz

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7538-6663
  17. Mathew Lewsey

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2631-4337
  18. Joanne Chory

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  19. Joseph R Ecker

    Plant Biology Laboratory, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States
    For correspondence
    ecker@salk.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5799-5895

Funding

National Science Foundation (MCB-1024999)

  • Joseph R Ecker

National Institutes of Health (5R35 GM122604)

  • Joanne Chory

Department of Energy, Office of Basic Energy Sciences (DE-FG02-04ER15517)

  • Joseph R Ecker

Gordon and Betty Moore Foundation (GBMF3034)

  • Joseph R Ecker

Howard Hughes Medical Institute

  • Joseph R Ecker

Deutsche Forschungsgemeinschaft (Za-730/1-1)

  • Mark Zander

Salk Pioneer Postdoctoral Endowment Fund

  • Mark Zander

Human Frontier Science Program (LT000222/2013-L)

  • Björn C Willige

EU Marie Curie FP7 International Outgoing Fellowship (252475)

  • Mathew Lewsey

Howard Hughes Medical Institute

  • Joanne Chory

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

Publication history

  1. Received: April 20, 2019
  2. Accepted: August 15, 2019
  3. Accepted Manuscript published: August 16, 2019 (version 1)
  4. Version of Record published: September 10, 2019 (version 2)

Copyright

© 2019, Zander 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. Mark Zander
  2. Björn C Willige
  3. Yupeng He
  4. Thu A Nguyen
  5. Amber E Langford
  6. Ramlah Nehring
  7. Elizabeth Howell
  8. Robert McGrath
  9. Anna Bartlett
  10. Rosa Castanon
  11. Joseph R Nery
  12. Huaming Chen
  13. Zhuzhu Zhang
  14. Florian Jupe
  15. Anna Stepanova
  16. Robert J Schmitz
  17. Mathew Lewsey
  18. Joanne Chory
  19. Joseph R Ecker
(2019)
Epigenetic silencing of a multifunctional plant stress regulator
eLife 8:e47835.
https://doi.org/10.7554/eLife.47835

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