Soil-borne fungi alter the apoplastic purinergic signaling in plants by deregulating the homeostasis of extracellular ATP and its metabolite adenosine

Abstract

Purinergic signaling activated by extracellular nucleotides and their derivative nucleosides trigger sophisticated signaling networks. The outcome of these pathways determine the capacity of the organism to survive under challenging conditions. Both extracellular ATP (eATP) and Adenosine (eAdo) act as primary messengers in mammals, essential for immunosuppressive responses. Despite the clear role of eATP as a plant damage-associated molecular pattern, the function of its nucleoside, eAdo, and of the eAdo/eATP balance in plant stress response remain to be fully elucidated. This is particularly relevant in the context of plant-microbe interaction, where the intruder manipulates the extracellular matrix. Here, we identify Ado as a main molecule secreted by the vascular fungus Fusarium oxysporum. We show that eAdo modulates the plant's susceptibility to fungal colonization by altering the eATP-mediated apoplastic pH homeostasis, an essential physiological player during the infection of this pathogen. Our work indicates that plant pathogens actively imbalance the apoplastic eAdo/eATP levels as a virulence mechanism.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file.

Article and author information

Author details

  1. Christopher Kesten

    Department of Biology, ETH Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Valentin Leitner

    Department of Biology, ETH Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4984-5875
  3. Susanne Dora

    Department of Biology, ETH Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5411-9072
  4. James W Sims

    Department of Environmental Systems Science, ETH Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Julian Dindas

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Cyril Zipfel

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4935-8583
  7. Consuelo M De Moraes

    Department of Environmental Systems Science, ETH Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6737-9842
  8. Clara Sanchez-Rodriguez

    Department of Biology, ETH Zurich, Zürich, Switzerland
    For correspondence
    clara.sanchez@csic.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0987-9317

Funding

Peter und Traudl Engelhorn Stiftung

  • Christopher Kesten

ETH Zürich Foundation (SEED-05 19-2)

  • Christopher Kesten

Novo Nordisk Foundation (NNF20OC0060564)

  • Christopher Kesten

Lundbeck Foundation (R346-2020-1546)

  • Christopher Kesten

Swiss National Science Foundation (31003A_182625)

  • Cyril Zipfel

European Molecular Biology Organization (683-2018)

  • Julian Dindas

Swiss National Science Foundation (310030_184769)

  • Clara Sanchez-Rodriguez

ETH Zürich

  • Consuelo M De Moraes

ETH Zürich

  • Clara Sanchez-Rodriguez

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

Copyright

© 2023, Kesten 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. Christopher Kesten
  2. Valentin Leitner
  3. Susanne Dora
  4. James W Sims
  5. Julian Dindas
  6. Cyril Zipfel
  7. Consuelo M De Moraes
  8. Clara Sanchez-Rodriguez
(2023)
Soil-borne fungi alter the apoplastic purinergic signaling in plants by deregulating the homeostasis of extracellular ATP and its metabolite adenosine
eLife 12:e92913.
https://doi.org/10.7554/eLife.92913

Share this article

https://doi.org/10.7554/eLife.92913

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