A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis

  1. Shanna Romand
  2. Hela Abdelkefi
  3. Cécile Lecampion
  4. Mohamed Belaroussi
  5. Melanie Dussenne
  6. Brigitte Ksas
  7. Sylvie Citerne
  8. Jose Caius
  9. Stefano D'Alessandro
  10. Hatem Fakhfakh
  11. Stefano Caffarri
  12. Michel Havaux
  13. Benjamin Field  Is a corresponding author
  1. Aix-Marseille University, CEA, CNRS, BIAM, France
  2. University of Carthage, Tunisia
  3. Université Paris-Saclay, UMR1318, INRAE, France
  4. Université Paris-Saclay, CNRS, INRAE, France
  5. University of Tunis El Manar, Tunisia

Abstract

Guanosine pentaphosphate and tetraphosphate (together referred to as ppGpp) are hyperphosphorylated nucleotides found in bacteria and the chloroplasts of plants and algae. In plants and algae artificial ppGpp accumulation can inhibit chloroplast gene expression, and influence photosynthesis, nutrient remobilisation, growth, and immunity. However, it is so far unknown whether ppGpp is required for abiotic stress acclimation in plants. Here, we demonstrate that ppGpp biosynthesis is necessary for acclimation to nitrogen starvation in Arabidopsis. We show that ppGpp is required for remodeling the photosynthetic electron transport chain to downregulate photosynthetic activity and for protection against oxidative stress. Furthermore, we demonstrate that ppGpp is required for coupling chloroplastic and nuclear gene expression during nitrogen starvation. Altogether, our work indicates that ppGpp is a pivotal regulator of chloroplast activity for stress acclimation in plants.

Data availability

All data presented in this study are included in the manuscript and supporting files Source Data files have been provided for Figures 1-5 (+ supplements).Sequencing data have been deposited at the European Nucleotide Archive under accession number PRJEB46181.

The following data sets were generated

Article and author information

Author details

  1. Shanna Romand

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Hela Abdelkefi

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Cécile Lecampion

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7862-517X
  4. Mohamed Belaroussi

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Melanie Dussenne

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Brigitte Ksas

    Faculty of Sciences, University of Carthage, Bizerte, Tunisia
    Competing interests
    The authors declare that no competing interests exist.
  7. Sylvie Citerne

    Institut JeanPierre Bourgin, Université Paris-Saclay, UMR1318, INRAE, Versailles, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Jose Caius

    Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Orsay, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Stefano D'Alessandro

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Hatem Fakhfakh

    Laboratory of Molecular Genetics, Immunology and Biotechnology, University of Tunis El Manar, Tunis, Tunisia
    Competing interests
    The authors declare that no competing interests exist.
  11. Stefano Caffarri

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Michel Havaux

    SAVE Team, Aix-Marseille University, CEA, CNRS, BIAM, Saint-Paul-lez-Durance,, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Benjamin Field

    LGBP Team, Aix-Marseille University, CEA, CNRS, BIAM, Marseille, France
    For correspondence
    ben.field@univ-amu.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2142-4606

Funding

Agence Nationale de la Recherche (ANR-17-CE13-0005)

  • Benjamin Field

Agence Nationale de la Recherche (ANR-17-EUR-0007)

  • Sylvie Citerne
  • Jose Caius

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

Reviewing Editor

  1. Shinji Masuda, Tokyo Institute of Technology, Japan

Version history

  1. Preprint posted: September 20, 2021 (view preprint)
  2. Received: October 28, 2021
  3. Accepted: February 14, 2022
  4. Accepted Manuscript published: February 14, 2022 (version 1)
  5. Version of Record published: March 1, 2022 (version 2)

Copyright

© 2022, Romand 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. Shanna Romand
  2. Hela Abdelkefi
  3. Cécile Lecampion
  4. Mohamed Belaroussi
  5. Melanie Dussenne
  6. Brigitte Ksas
  7. Sylvie Citerne
  8. Jose Caius
  9. Stefano D'Alessandro
  10. Hatem Fakhfakh
  11. Stefano Caffarri
  12. Michel Havaux
  13. Benjamin Field
(2022)
A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis
eLife 11:e75041.
https://doi.org/10.7554/eLife.75041

Share this article

https://doi.org/10.7554/eLife.75041

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