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Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

Author

Listed:
  • Sjon Hartman

    (Utrecht University)

  • Zeguang Liu

    (Utrecht University)

  • Hans Veen

    (Utrecht University)

  • Jorge Vicente

    (University of Nottingham)

  • Emilie Reinen

    (Utrecht University)

  • Shanice Martopawiro

    (Utrecht University)

  • Hongtao Zhang

    (Rothamsted Research)

  • Nienke Dongen

    (Utrecht University)

  • Femke Bosman

    (Utrecht University)

  • George W. Bassel

    (University of Birmingham)

  • Eric J. W. Visser

    (Radboud University Nijmegen)

  • Julia Bailey-Serres

    (Utrecht University
    University of California)

  • Frederica L. Theodoulou

    (Rothamsted Research)

  • Kim H. Hebelstrup

    (Aarhus University)

  • Daniel J. Gibbs

    (University of Birmingham)

  • Michael J. Holdsworth

    (University of Nottingham)

  • Rashmi Sasidharan

    (Utrecht University)

  • Laurentius A. C. J. Voesenek

    (Utrecht University)

Abstract

Timely perception of adverse environmental changes is critical for survival. Dynamic changes in gases are important cues for plants to sense environmental perturbations, such as submergence. In Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-degron pathway and mediates adaptation to flooding-induced hypoxia. However, how plants detect and transduce early submergence signals remains elusive. Here we show that plants can rapidly detect submergence through passive ethylene entrapment and use this signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent hypoxia. Our results reveal the biological link between three gaseous signals for the regulation of flooding survival and identifies key regulatory targets for early stress perception that could be pivotal for developing flood-tolerant crops.

Suggested Citation

  • Sjon Hartman & Zeguang Liu & Hans Veen & Jorge Vicente & Emilie Reinen & Shanice Martopawiro & Hongtao Zhang & Nienke Dongen & Femke Bosman & George W. Bassel & Eric J. W. Visser & Julia Bailey-Serres, 2019. "Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12045-4
    DOI: 10.1038/s41467-019-12045-4
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    Cited by:

    1. Jian Zeng & Xin’Ai Zhao & Zhe Liang & Inés Hidalgo & Michael Gebert & Pengfei Fan & Christian Wenzl & Sebastian G. Gornik & Jan U. Lohmann, 2023. "Nitric oxide controls shoot meristem activity via regulation of DNA methylation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Agata Zubrycka & Charlene Dambire & Laura Dalle Carbonare & Gunjan Sharma & Tinne Boeckx & Kamal Swarup & Craig J. Sturrock & Brian S. Atkinson & Ranjan Swarup & Françoise Corbineau & Neil J. Oldham &, 2023. "ERFVII action and modulation through oxygen-sensing in Arabidopsis thaliana," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Stefan C. Dekker & Aletta D. Kraneveld & Jerry van Dijk & Agni Kalfagianni & Andre C. Knulst & Herman Lelieveldt & Ellen H. M. Moors & Eggo Müller & Raymond H. H. Pieters & Corné M. J. Pieterse & Step, 2020. "Towards Healthy Planet Diets—A Transdisciplinary Approach to Food Sustainability Challenges," Challenges, MDPI, vol. 11(2), pages 1-19, September.

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