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

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

doi:10.1038/s41467-019-12045-4

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

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

Sub Plant Ecophysiology

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Article number	4020
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12045-4
Publication status	Published - 5 Sept 2019

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Hartman, S., Liu, Z., van Veen, H., Vicente, J., Reinen, E., Martopawiro, S., Zhang, H., van Dongen, N., Bosman, F., Bassel, G. W., Visser, E. J. W., Bailey-Serres, J., Theodoulou, F. L., Hebelstrup, K. H., Gibbs, D. J., Holdsworth, M. J., Sasidharan, R., & Voesenek, L. A. C. J. (2019). Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nature Communications, 10(1), Article 4020. https://doi.org/10.1038/s41467-019-12045-4

@article{28d2015fd432429bbb3ea3d3b00d94aa,

title = "Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress",

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.",

author = "Sjon Hartman and Zeguang Liu and \{van Veen\}, Hans and Jorge Vicente and Emilie Reinen and Shanice Martopawiro and Hongtao Zhang and \{van Dongen\}, Nienke and Femke Bosman and Bassel, \{George W\} and Visser, \{Eric J W\} and Julia Bailey-Serres and Theodoulou, \{Frederica L\} and Hebelstrup, \{Kim H\} and Gibbs, \{Daniel J\} and Holdsworth, \{Michael J\} and Rashmi Sasidharan and Voesenek, \{Laurentius A C J\}",

year = "2019",

month = sep,

day = "5",

doi = "10.1038/s41467-019-12045-4",

language = "English",

volume = "10",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

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Hartman, S, Liu, Z, van Veen, H, Vicente, J, Reinen, E, Martopawiro, S, Zhang, H, van Dongen, N, Bosman, F, Bassel, GW, Visser, EJW, Bailey-Serres, J, Theodoulou, FL, Hebelstrup, KH, Gibbs, DJ, Holdsworth, MJ, Sasidharan, R & Voesenek, LACJ 2019, 'Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress', Nature Communications, vol. 10, no. 1, 4020. https://doi.org/10.1038/s41467-019-12045-4

TY - JOUR

T1 - Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

AU - Hartman, Sjon

AU - Liu, Zeguang

AU - van Veen, Hans

AU - Vicente, Jorge

AU - Reinen, Emilie

AU - Martopawiro, Shanice

AU - Zhang, Hongtao

AU - van Dongen, Nienke

AU - Bosman, Femke

AU - Bassel, George W

AU - Visser, Eric J W

AU - Bailey-Serres, Julia

AU - Theodoulou, Frederica L

AU - Hebelstrup, Kim H

AU - Gibbs, Daniel J

AU - Holdsworth, Michael J

AU - Sasidharan, Rashmi

AU - Voesenek, Laurentius A C J

PY - 2019/9/5

Y1 - 2019/9/5

N2 - 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.

AB - 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.

U2 - 10.1038/s41467-019-12045-4

DO - 10.1038/s41467-019-12045-4

M3 - Article

C2 - 31488841

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4020

ER -

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

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