1. Plant Biology
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Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1

  1. Michael J Skelly
  2. James J Furniss
  3. Heather L Grey
  4. Ka-Wing Wong
  5. Steven H Spoel  Is a corresponding author
  1. University of Edinburgh, United Kingdom
Research Article
  • Cited 14
  • Views 3,498
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Cite this article as: eLife 2019;8:e47005 doi: 10.7554/eLife.47005

Abstract

Activation of systemic acquired resistance in plants is associated with transcriptome reprogramming induced by the unstable coactivator NPR1. Immune-induced ubiquitination and proteasomal degradation of NPR1 are thought to facilitate continuous delivery of active NPR1 to target promoters, thereby maximising gene expression. Because of this potentially costly sacrificial process, we investigated if ubiquitination of NPR1 plays transcriptional roles prior to its proteasomal turnover. Here we show ubiquitination of NPR1 is a progressive event in which initial modification by a Cullin-RING E3 ligase promotes its chromatin association and expression of target genes. Only when polyubiquitination of NPR1 is enhanced by the E4 ligase, UBE4, it is targeted for proteasomal degradation. Conversely, ubiquitin ligase activities are opposed by UBP6/7, two proteasome-associated deubiquitinases that enhance NPR1 longevity. Thus, immune-induced transcriptome reprogramming requires sequential actions of E3 and E4 ligases balanced by opposing deubiquitinases that fine-tune activity of NPR1 without strict requirement for its sacrificial turnover.

Data availability

RNA Seq data have been deposited in Array Express at EMBL-EBIunder accession code E-MTAB-7369.

The following data sets were generated

Article and author information

Author details

  1. Michael J Skelly

    Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9024-0037
  2. James J Furniss

    Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Heather L Grey

    Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Ka-Wing Wong

    Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Steven H Spoel

    Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    steven.spoel@ed.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4340-7591

Funding

Royal Society (UF090321)

  • Steven H Spoel

Biotechnology and Biological Sciences Research Council (BB/L006219/1)

  • Steven H Spoel

H2020 European Research Council (678511)

  • Steven H Spoel

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

Reviewing Editor

  1. Jian-Min Zhou, Chinese Academy of Sciences, China

Publication history

  1. Received: March 19, 2019
  2. Accepted: October 5, 2019
  3. Accepted Manuscript published: October 7, 2019 (version 1)
  4. Version of Record published: November 12, 2019 (version 2)

Copyright

© 2019, Skelly 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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Further reading

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