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

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 transcriptio...

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Autores principales: Hartman, Sjon, Liu, Zeguang, van Veen, Hans, Vicente, Jorge, Reinen, Emilie, Martopawiro, Shanice, Zhang, Hongtao, van Dongen, Nienke, Bosman, Femke, Bassel, George W., Visser, Eric J. W., Bailey-Serres, Julia, Theodoulou, Frederica L., Hebelstrup, Kim H., Gibbs, Daniel J., Holdsworth, Michael J., Sasidharan, Rashmi, Voesenek, Laurentius A. C. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6728379/
https://www.ncbi.nlm.nih.gov/pubmed/31488841
http://dx.doi.org/10.1038/s41467-019-12045-4
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author Hartman, Sjon
Liu, Zeguang
van Veen, Hans
Vicente, Jorge
Reinen, Emilie
Martopawiro, Shanice
Zhang, Hongtao
van Dongen, Nienke
Bosman, Femke
Bassel, George W.
Visser, Eric J. W.
Bailey-Serres, Julia
Theodoulou, Frederica L.
Hebelstrup, Kim H.
Gibbs, Daniel J.
Holdsworth, Michael J.
Sasidharan, Rashmi
Voesenek, Laurentius A. C. J.
author_facet Hartman, Sjon
Liu, Zeguang
van Veen, Hans
Vicente, Jorge
Reinen, Emilie
Martopawiro, Shanice
Zhang, Hongtao
van Dongen, Nienke
Bosman, Femke
Bassel, George W.
Visser, Eric J. W.
Bailey-Serres, Julia
Theodoulou, Frederica L.
Hebelstrup, Kim H.
Gibbs, Daniel J.
Holdsworth, Michael J.
Sasidharan, Rashmi
Voesenek, Laurentius A. C. J.
author_sort Hartman, Sjon
collection PubMed
description 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.
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spelling pubmed-67283792019-09-09 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, Eric J. W. Bailey-Serres, Julia Theodoulou, Frederica L. Hebelstrup, Kim H. Gibbs, Daniel J. Holdsworth, Michael J. Sasidharan, Rashmi Voesenek, Laurentius A. C. J. Nat Commun Article 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. Nature Publishing Group UK 2019-09-05 /pmc/articles/PMC6728379/ /pubmed/31488841 http://dx.doi.org/10.1038/s41467-019-12045-4 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Hartman, Sjon
Liu, Zeguang
van Veen, Hans
Vicente, Jorge
Reinen, Emilie
Martopawiro, Shanice
Zhang, Hongtao
van Dongen, Nienke
Bosman, Femke
Bassel, George W.
Visser, Eric J. W.
Bailey-Serres, Julia
Theodoulou, Frederica L.
Hebelstrup, Kim H.
Gibbs, Daniel J.
Holdsworth, Michael J.
Sasidharan, Rashmi
Voesenek, Laurentius A. C. J.
Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
title Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
title_full Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
title_fullStr Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
title_full_unstemmed Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
title_short Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
title_sort ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6728379/
https://www.ncbi.nlm.nih.gov/pubmed/31488841
http://dx.doi.org/10.1038/s41467-019-12045-4
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