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

Hartman, Sjon; Liu, Zeguang; Van Veen, Hans; Vicente, Jorge; Reinen, Emilie; Martopawiro, Shanice; Zhang, Hongtao; Van Dongen, Nienke; Bosman, Femke; Bassel, George W.; Visser, J. W.; Bailey-Serres, Julia; Theodoulou, Frederica L.; Hebelstrup, Kim H.; 10 Gibbs, Daniel J.; Holdsworth, Michael J.; Sasidharan, Rashmi; Voesenek, Laurentius A.C.J.

Authors

Sjon Hartman

Zeguang Liu

Hans Van Veen

Jorge Vicente

Emilie Reinen

Shanice Martopawiro

Hongtao Zhang

Nienke Van Dongen

Femke Bosman

George W. Bassel

J. W. Visser

Julia Bailey-Serres

Frederica L. Theodoulou

Kim H. Hebelstrup

Daniel J. 10 Gibbs

Rashmi Sasidharan

Laurentius A.C.J. Voesenek



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.

Citation

Hartman, S., Liu, Z., Van Veen, H., Vicente, J., Reinen, E., Martopawiro, S., …Voesenek, L. A. (2019). Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nature Communications, 10, https://doi.org/10.1038/s41467-019-12045-4

Journal Article Type Article
Acceptance Date Aug 16, 2019
Online Publication Date Sep 5, 2019
Publication Date Sep 5, 2019
Deposit Date Aug 23, 2019
Publicly Available Date Sep 9, 2019
Journal Nature Communications
Electronic ISSN 2041-1723
Publisher Nature Publishing Group
Peer Reviewed Peer Reviewed
Volume 10
Article Number 4020
DOI https://doi.org/10.1038/s41467-019-12045-4
Keywords General Biochemistry, Genetics and Molecular Biology; General Physics and Astronomy; General Chemistry
Public URL https://nottingham-repository.worktribe.com/output/2482891
Publisher URL https://www.nature.com/articles/s41467-019-12045-4
Additional Information Received: 25 April 2019; Accepted: 16 August 2019; First Online: 5 September 2019; : The authors declare no competing interests.

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