UBP12 and UBP13 negatively regulate the activity of the ubiquitin-dependent peptidases DA1, DAR1 and DAR2

Abstract

Protein ubiquitination is a very diverse post-translational modification leading to protein degradation or delocalization, or altering protein activity. In Arabidopsis thaliana, two E3 ligases, BIG BROTHER (BB) and DA2, activate the latent peptidases DA1, DAR1 and DAR2 by mono-ubiquitination at multiple sites. Subsequently, these activated peptidases destabilize various positive regulators of growth. Here, we show that two ubiquitin-specific proteases, UBP12 and UBP13, deubiquitinate DA1, DAR1 and DAR2, hence reducing their peptidase activity. Overexpression of UBP12 or UBP13 strongly decreased leaf size and cell area, and resulted in lower ploidy levels. Mutants in which UBP12 and UBP13 were downregulated produced smaller leaves that contained fewer and smaller cells. Remarkably, neither UBP12 nor UBP13 were found to be cleavage substrates of the activated DA1. Our results therefore suggest that UBP12 and UBP13 work upstream of DA1, DAR1 and DAR2 to restrict their protease activity and hence fine-tune plant growth and development.

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Author details

  1. Hannes Vanhaeren

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    For correspondence
    hahae@psb.vib-ugent.be
    Competing interests
    The authors declare that no competing interests exist.
  2. Ying Chen

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Mattias Vermeersch

    Department of Plant Systems Biology, VIB/UGent, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  4. Liesbeth De Milde

    Department of Plant Systems Biology, VIB/UGent, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  5. Valerie De Vleeschhauwer

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  6. Annelore Natran

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  7. Geert Persiau

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  8. Dominique Eeckhout

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  9. Geert De Jaeger

    Center for Plant Systems Biology, VIB/UGent, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  10. Kris Gevaert

    VIB Center for Medical Biotechnology, Department of Biomolecular Medicine, VIB/UGent, Ghent, Belgium
    For correspondence
    kris.gevaert@vib-ugent.be
    Competing interests
    The authors declare that no competing interests exist.
  11. Dirk Inzé

    VIB Center for Plant Systems Biology, Department of Plant Biotechnology and Bioinformatics, VIB/UGent, Zwijnaarde, Belgium
    For correspondence
    dirk.inze@psb.vib-ugent.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3217-8407

Funding

Ghent University Bijzonder Onderzoeksfondsen (BOF08/01M00408)

  • Mattias Vermeersch

Ghent University Bijzonder Onderzoeksfondsen (01SC3117)

  • Ying Chen

Chinese Scholarship Council (201604910566)

  • Ying Chen

Research Foundation Flanders (12V0218N)

  • Hannes Vanhaeren

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

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Publication history

  1. Received: September 27, 2019
  2. Accepted: March 24, 2020
  3. Accepted Manuscript published: March 25, 2020 (version 1)
  4. Version of Record published: April 8, 2020 (version 2)

Copyright

© 2020, Vanhaeren 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. Hannes Vanhaeren
  2. Ying Chen
  3. Mattias Vermeersch
  4. Liesbeth De Milde
  5. Valerie De Vleeschhauwer
  6. Annelore Natran
  7. Geert Persiau
  8. Dominique Eeckhout
  9. Geert De Jaeger
  10. Kris Gevaert
  11. Dirk Inzé
(2020)
UBP12 and UBP13 negatively regulate the activity of the ubiquitin-dependent peptidases DA1, DAR1 and DAR2
eLife 9:e52276.
https://doi.org/10.7554/eLife.52276
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