γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis

Aluminum (Al) toxicity is a major limiting factor for plant growth and crop production in acidic soils. This study aims to investigate the effects of γ-aminobutyric acid (GABA) priming on mitigating acid-Al toxicity to creeping bentgrass (<i>Agrostis stolonifera</i>) associated with chan...

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Main Authors: Min Zhou, Yan Yuan, Junnan Lin, Long Lin, Jianzhen Zhou, Zhou Li
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/18/14309
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author Min Zhou
Yan Yuan
Junnan Lin
Long Lin
Jianzhen Zhou
Zhou Li
author_facet Min Zhou
Yan Yuan
Junnan Lin
Long Lin
Jianzhen Zhou
Zhou Li
author_sort Min Zhou
collection DOAJ
description Aluminum (Al) toxicity is a major limiting factor for plant growth and crop production in acidic soils. This study aims to investigate the effects of γ-aminobutyric acid (GABA) priming on mitigating acid-Al toxicity to creeping bentgrass (<i>Agrostis stolonifera</i>) associated with changes in plant growth, photosynthetic parameters, antioxidant defense, key metabolites, and genes related to organic acids metabolism. Thirty-seven-old plants were primed with or without 0.5 mM GABA for three days and then subjected to acid-Al stress (5 mmol/L AlCl<sub>3</sub>·6H<sub>2</sub>O, pH 4.35) for fifteen days. The results showed that acid-Al stress significantly increased the accumulation of Al and also restricted aboveground and underground growths, photosynthesis, photochemical efficiency, and osmotic balance, which could be effectively alleviated by GABA priming. The application of GABA significantly activated antioxidant enzymes, including superoxide dismutase, peroxidase, catalase, and ascorbate peroxidase, to reduce oxidative damage to cells under acid-Al stress. Metabolomics analysis demonstrated that the GABA pretreatment significantly induced the accumulation of many metabolites such as quinic acid, pyruvic acid, shikimic acid, glycine, threonine, erythrose, glucose-6-phosphate, galactose, kestose, threitol, ribitol, glycerol, putrescine, galactinol, and myo-inositol associated with osmotic, antioxidant, and metabolic homeostases under acid-Al stress. In addition, the GABA priming significantly up-regulated genes related to the transportation of malic acid and citric acid in leaves in response to acid-Al stress. Current findings indicated GABA-induced tolerance to acid-Al stress in relation to scavenging of reactive oxygen species, osmotic adjustment, and accumulation and transport of organic metabolites in leaves. Exogenous GABA priming could improve the phytoremediation potential of perennial creeping bentgrass for the restoration of Al-contaminated soils.
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spelling doaj.art-2f1ec5e5ceb14ea68c2330eecd73bcd32023-11-19T11:10:53ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-09-0124181430910.3390/ijms241814309γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic HomeostasisMin Zhou0Yan Yuan1Junnan Lin2Long Lin3Jianzhen Zhou4Zhou Li5College of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaAluminum (Al) toxicity is a major limiting factor for plant growth and crop production in acidic soils. This study aims to investigate the effects of γ-aminobutyric acid (GABA) priming on mitigating acid-Al toxicity to creeping bentgrass (<i>Agrostis stolonifera</i>) associated with changes in plant growth, photosynthetic parameters, antioxidant defense, key metabolites, and genes related to organic acids metabolism. Thirty-seven-old plants were primed with or without 0.5 mM GABA for three days and then subjected to acid-Al stress (5 mmol/L AlCl<sub>3</sub>·6H<sub>2</sub>O, pH 4.35) for fifteen days. The results showed that acid-Al stress significantly increased the accumulation of Al and also restricted aboveground and underground growths, photosynthesis, photochemical efficiency, and osmotic balance, which could be effectively alleviated by GABA priming. The application of GABA significantly activated antioxidant enzymes, including superoxide dismutase, peroxidase, catalase, and ascorbate peroxidase, to reduce oxidative damage to cells under acid-Al stress. Metabolomics analysis demonstrated that the GABA pretreatment significantly induced the accumulation of many metabolites such as quinic acid, pyruvic acid, shikimic acid, glycine, threonine, erythrose, glucose-6-phosphate, galactose, kestose, threitol, ribitol, glycerol, putrescine, galactinol, and myo-inositol associated with osmotic, antioxidant, and metabolic homeostases under acid-Al stress. In addition, the GABA priming significantly up-regulated genes related to the transportation of malic acid and citric acid in leaves in response to acid-Al stress. Current findings indicated GABA-induced tolerance to acid-Al stress in relation to scavenging of reactive oxygen species, osmotic adjustment, and accumulation and transport of organic metabolites in leaves. Exogenous GABA priming could improve the phytoremediation potential of perennial creeping bentgrass for the restoration of Al-contaminated soils.https://www.mdpi.com/1422-0067/24/18/14309aluminum toxicityphotochemical efficiencyorganic acidosmotic adjustmentoxidative damagegene expression
spellingShingle Min Zhou
Yan Yuan
Junnan Lin
Long Lin
Jianzhen Zhou
Zhou Li
γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis
International Journal of Molecular Sciences
aluminum toxicity
photochemical efficiency
organic acid
osmotic adjustment
oxidative damage
gene expression
title γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis
title_full γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis
title_fullStr γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis
title_full_unstemmed γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis
title_short γ-Aminobutyric Acid Priming Alleviates Acid-Aluminum Toxicity to Creeping Bentgrass by Regulating Metabolic Homeostasis
title_sort γ aminobutyric acid priming alleviates acid aluminum toxicity to creeping bentgrass by regulating metabolic homeostasis
topic aluminum toxicity
photochemical efficiency
organic acid
osmotic adjustment
oxidative damage
gene expression
url https://www.mdpi.com/1422-0067/24/18/14309
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