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Hypoxia-induced increase in GABA content is essential for restoration of membrane potential and preventing ROS-induced disturbance to ion homeostasis

Citation

Wu, Qi and Su, N and Huang, Xin and Cui, J and Shabala, L and Zhou, M and Yu, M and Shabala, S, Hypoxia-induced increase in GABA content is essential for restoration of membrane potential and preventing ROS-induced disturbance to ion homeostasis, Plant Communications, 2, (3) Article 100188. ISSN 2590-3462 (2021) [Refereed Article]


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Copyright Statement

Copyright 2021 The Author(s). This is an open access article under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

DOI: doi:10.1016/j.xplc.2021.100188

Abstract

When plants are exposed to hypoxic conditions, the level of γ-aminobutyric acid (GABA) in plant tissues increases by several orders of magnitude. The physiological rationale behind this elevation remains largely unanswered. By combining genetic and electrophysiological approach, in this work we show that hypoxia-induced increase in GABA content is essential for restoration of membrane potential and preventing ROS-induced disturbance to cytosolic K+ homeostasis and Ca2+ signaling. We show that reduced O2 availability affects H+-ATPase pumping activity, leading to membrane depolarization and K+ loss via outward-rectifying GORK channels. Hypoxia stress also results in H2O2 accumulation in the cell that activates ROS-inducible Ca2+ uptake channels and triggers self-amplifying "ROS-Ca hub," further exacerbating K+ loss via non-selective cation channels that results in the loss of the cell's viability. Hypoxia-induced elevation in the GABA level may restore membrane potential by pH-dependent regulation of H+-ATPase and/or by generating more energy through the activation of the GABA shunt pathway and TCA cycle. Elevated GABA can also provide better control of the ROS-Ca2+ hub by transcriptional control of RBOH genes thus preventing over-excessive H2O2 accumulation. Finally, GABA can operate as a ligand directly controlling the open probability and conductance of K+ efflux GORK channels, thus enabling plants adaptation to hypoxic conditions.

Item Details

Item Type:Refereed Article
Keywords:hypoxia, GABA, membrane potential, ROS, ion homeostasis, potassium homeostasis, calcium signaling, NADPH oxidase, GORK, H+-ATPase, reactive oxygen species
Research Division:Biological Sciences
Research Group:Plant biology
Research Field:Plant physiology
Objective Division:Plant Production and Plant Primary Products
Objective Group:Other plant production and plant primary products
Objective Field:Other plant production and plant primary products not elsewhere classified
UTAS Author:Wu, Qi (Mr Qi Wu)
UTAS Author:Su, N (Mrs Nana Su)
UTAS Author:Huang, Xin (Mr Xin Huang)
UTAS Author:Shabala, L (Associate Professor Lana Shabala)
UTAS Author:Zhou, M (Professor Meixue Zhou)
UTAS Author:Shabala, S (Professor Sergey Shabala)
ID Code:147643
Year Published:2021
Web of Science® Times Cited:15
Deposited By:TIA - Research Institute
Deposited On:2021-11-10
Last Modified:2022-04-08
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