Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress

M Hafiz Che-Othman, Richard P Jacoby, A Harvey Millar, Nicolas L Taylor

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Mitochondrial respiration and tricarboxylic acid (TCA) cycle activity are required during salt stress in plants to provide ATP and reductants for adaptive processes such as ion exclusion, compatible solute synthesis and reactive oxygen species (ROS) detoxification. However, there is a poor mechanistic understanding of how salinity affects mitochondrial metabolism, particularly respiratory substrate source. To determine the mechanism of respiratory changes under salt stress in wheat leaves, we conducted an integrated analysis of metabolite content, respiratory rate and targeted protein abundance measurements. Also, we investigated the direct effect of salt on mitochondrial enzyme activities. Salt-treated wheat leaves exhibit higher respiration rate and extensive metabolite changes. The activity of the TCA cycle enzymes pyruvate dehydrogenase complex and the 2-oxoglutarate dehydrogenase complex were shown to be directly salt-sensitive. Multiple lines of evidence showed that the gamma-aminobutyric acid (GABA) shunt was activated under salt treatment. During salt exposure, key metabolic enzymes required for the cyclic operation of the TCA cycle are physiochemically inhibited by salt. This inhibition is overcome by increased GABA shunt activity, which provides an alternative carbon source for mitochondria that bypasses salt-sensitive enzymes, to facilitate the increased respiration of wheat leaves.

Original languageEnglish
Pages (from-to)1166-1180
Number of pages15
JournalThe New Phytologist
Volume225
Issue number3
DOIs
Publication statusPublished - Feb 2020

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Citric Acid Cycle
tricarboxylic acid cycle
gamma-aminobutyric acid
gamma-Aminobutyric Acid
Triticum
salt stress
Respiration
Salts
salts
wheat
pyruvate dehydrogenase (lipoamide)
Enzymes
Respiratory Rate
enzymes
metabolites
leaves
reducing agents
Ketoglutarate Dehydrogenase Complex
Pyruvate Dehydrogenase Complex
solutes

Cite this

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title = "Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress",
abstract = "Mitochondrial respiration and tricarboxylic acid (TCA) cycle activity are required during salt stress in plants to provide ATP and reductants for adaptive processes such as ion exclusion, compatible solute synthesis and reactive oxygen species (ROS) detoxification. However, there is a poor mechanistic understanding of how salinity affects mitochondrial metabolism, particularly respiratory substrate source. To determine the mechanism of respiratory changes under salt stress in wheat leaves, we conducted an integrated analysis of metabolite content, respiratory rate and targeted protein abundance measurements. Also, we investigated the direct effect of salt on mitochondrial enzyme activities. Salt-treated wheat leaves exhibit higher respiration rate and extensive metabolite changes. The activity of the TCA cycle enzymes pyruvate dehydrogenase complex and the 2-oxoglutarate dehydrogenase complex were shown to be directly salt-sensitive. Multiple lines of evidence showed that the gamma-aminobutyric acid (GABA) shunt was activated under salt treatment. During salt exposure, key metabolic enzymes required for the cyclic operation of the TCA cycle are physiochemically inhibited by salt. This inhibition is overcome by increased GABA shunt activity, which provides an alternative carbon source for mitochondria that bypasses salt-sensitive enzymes, to facilitate the increased respiration of wheat leaves.",
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Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. / Che-Othman, M Hafiz; Jacoby, Richard P; Millar, A Harvey; Taylor, Nicolas L.

In: The New Phytologist, Vol. 225, No. 3, 02.2020, p. 1166-1180.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress

AU - Che-Othman, M Hafiz

AU - Jacoby, Richard P

AU - Millar, A Harvey

AU - Taylor, Nicolas L

PY - 2020/2

Y1 - 2020/2

N2 - Mitochondrial respiration and tricarboxylic acid (TCA) cycle activity are required during salt stress in plants to provide ATP and reductants for adaptive processes such as ion exclusion, compatible solute synthesis and reactive oxygen species (ROS) detoxification. However, there is a poor mechanistic understanding of how salinity affects mitochondrial metabolism, particularly respiratory substrate source. To determine the mechanism of respiratory changes under salt stress in wheat leaves, we conducted an integrated analysis of metabolite content, respiratory rate and targeted protein abundance measurements. Also, we investigated the direct effect of salt on mitochondrial enzyme activities. Salt-treated wheat leaves exhibit higher respiration rate and extensive metabolite changes. The activity of the TCA cycle enzymes pyruvate dehydrogenase complex and the 2-oxoglutarate dehydrogenase complex were shown to be directly salt-sensitive. Multiple lines of evidence showed that the gamma-aminobutyric acid (GABA) shunt was activated under salt treatment. During salt exposure, key metabolic enzymes required for the cyclic operation of the TCA cycle are physiochemically inhibited by salt. This inhibition is overcome by increased GABA shunt activity, which provides an alternative carbon source for mitochondria that bypasses salt-sensitive enzymes, to facilitate the increased respiration of wheat leaves.

AB - Mitochondrial respiration and tricarboxylic acid (TCA) cycle activity are required during salt stress in plants to provide ATP and reductants for adaptive processes such as ion exclusion, compatible solute synthesis and reactive oxygen species (ROS) detoxification. However, there is a poor mechanistic understanding of how salinity affects mitochondrial metabolism, particularly respiratory substrate source. To determine the mechanism of respiratory changes under salt stress in wheat leaves, we conducted an integrated analysis of metabolite content, respiratory rate and targeted protein abundance measurements. Also, we investigated the direct effect of salt on mitochondrial enzyme activities. Salt-treated wheat leaves exhibit higher respiration rate and extensive metabolite changes. The activity of the TCA cycle enzymes pyruvate dehydrogenase complex and the 2-oxoglutarate dehydrogenase complex were shown to be directly salt-sensitive. Multiple lines of evidence showed that the gamma-aminobutyric acid (GABA) shunt was activated under salt treatment. During salt exposure, key metabolic enzymes required for the cyclic operation of the TCA cycle are physiochemically inhibited by salt. This inhibition is overcome by increased GABA shunt activity, which provides an alternative carbon source for mitochondria that bypasses salt-sensitive enzymes, to facilitate the increased respiration of wheat leaves.

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KW - pyruvate dehydrogenase

KW - salinity

KW - sodium chloride

KW - SRM mass spectrometry

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KW - gamma-aminobutyric acid (GABA) shunt

KW - PYRUVATE-DEHYDROGENASE COMPLEX

KW - GAMMA-AMINOBUTYRIC-ACID

KW - ALPHA-KETOGLUTARATE DEHYDROGENASE

KW - DIHYDROLIPOAMIDE DEHYDROGENASE

KW - GLUTAMATE-DECARBOXYLASE

KW - ARABIDOPSIS-THALIANA

KW - MULTIENZYME COMPLEX

KW - SALINITY TOLERANCE

KW - BINDING DOMAIN

KW - BIOCHEMICAL-CHARACTERIZATION

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DO - 10.1111/nph.15713

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SP - 1166

EP - 1180

JO - The New Phytologist

JF - The New Phytologist

SN - 0028-646X

IS - 3

ER -