Nitric Oxide Signal, Nitrogen Metabolism, and Water Balance Affected by γ-Aminobutyric Acid (GABA) in Relation to Enhanced Tolerance to Water Stress in Creeping Bentgrass

Abstract

γ-Aminobutyric acid (GABA) plays an important role in regulating stress tolerance in plants. Purposes of this study was to determine the effect of an exogenous supply of GABA on tolerance to water stress in creeping bentgrass (Agrostis stolonifera), and further reveal the GABA-induced key mechanisms related to water balance, nitrogen (N) metabolism and nitric oxide (NO) production in response to water stress. Plants were pretreated with or without 0.5 mM GABA solution in the roots for 3 days, and then subjected to water stress induced by −0.52 MPa polyethylene glycol 6000 for 12 days. The results showed that water stress caused leaf water deficit, chlorophyll (Chl) loss, oxidative damage (increases in superoxide anion, hydrogen peroxide, malondialdehyde, and protein carbonyl content), N insufficiency, and metabolic disturbance. However, the exogenous addition of GABA significantly increased endogenous GABA content, osmotic adjustment and antioxidant enzyme activities (superoxide dismutase, catalase, dehydroascorbate reductase, glutathione reductase and monodehydroascorbate reductase), followed by effectively alleviating water stress damage, including declines in oxidative damage, photoinhibition, and water and Chl loss. GABA supply not only provided more available N, but also affected N metabolism through activating nitrite reductase and glutamine synthetase activities under water stress. The supply of GABA did not increase glutamate content and glutamate decarboxylase activity, but enhanced glutamate dehydrogenase activity, which might indicate that GABA promoted the conversion and utilization of glutamate for maintaining Chl synthesis and tricarboxylic acid cycle when creeping bentgrass underwent water stress. In addition, GABA-induced NO production, depending on nitrate reductase and NO-associated protein pathways, could be associated with the enhancement of antioxidant defense. Current findings reveal the critical role of GABA in regulating signal transduction and metabolic homeostasis in plants under water-limited condition.

Adaptability to High Temperature and Stay-Green Genotypes Associated With Variations in Antioxidant, Chlorophyll Metabolism, and γ-Aminobutyric Acid Accumulation in Creeping Bentgrass Species

“…As a non-protein amino acid, GABA is involved in nitrogen balance, energy metabolism, and metabolic shift with other metabolites (Fait et al, 2008;Lee et al, 2021). Enhanced GABA accumulation or metabolism could contribute to better adaptation to abiotic stresses, such as heat stress, in different plant species Tang et al, 2020;Rossi et al, 2021). The catabolism of GABA produces glutamic acid, which is an important biosynthetical precursor of Chl (Bouché and Fromm, 2004).…”

γ-Aminobutyrate (GABA) Regulated Plant Defense: Mechanisms and Opportunities

“…Table 4 briefly summarizes many examples from the literature wherein tolerance to hypoxia, drought, salinity, chilling, heat, osmotic stress and proton stress, as well as heavy metals (i.e., aluminum, arsenic and chromium) is improved in vegetative organs by the application of exogenous GABA [ 39 , 150 , 151 , 152 , 153 , 154 , 155 , 156 , 157 , 158 , 159 , 160 , 161 , 162 , 163 , 164 , 165 , 166 , 167 , 168 , 169 , 170 , 171 , 172 , 173 , 174 , 175 , 176 , 177 , 178 , 179 , 180 , 181 , 182 , 183 , 184 ]. The application of exogenous GABA typically increases the level of endogenous GABA, and elicits a diverse range of biochemical, molecular and physiological responses.…”

“…There is also evidence for the GABA-induced production of nitric oxide (NO) ( Table 4 ), which could be associated with the enhancement of antioxidant defense, as well as regulation of epigenetic mechanisms and gene transcription [ 157 , 174 , 186 ]. The stress tolerance could also be related to GABA-induced changes in pathways associated with other phytohormones such as ABA (ABA receptors), ethylene (ACC oxidase, ACC synthase), PAs (arginine decarboxylase, free and conjugated forms, S-adenosylmethionine decarboxylase) and salicylate ( Table 4 ) [ 60 , 156 , 172 , 175 , 187 ], which can regulate metabolic homeostasis and influence the expression of stress factors (miRNAs, transcription factors, heat shock proteins) with known and yet-to-be-determined functions [ 156 , 183 , 188 ].…”

“…These result in lower levels of ROS, malondialdehyde (a product of ROS-mediated peroxidation of membrane polyunsaturated fatty acids and marker for the depletion of antioxidant systems), and protein carbonylation (product of protein peroxidation and a marker of oxidative damage), lower activities of NADPH oxidase, lipoxygenase and polyphenol oxidase, and restoration of ion homeostasis (electrolyte leakage), which is indicative of membrane stability. There is also evidence for the GABA-induced production of nitric oxide (NO) (Table 4), which could be associated with the enhancement of antioxidant defense, as well as regulation of epigenetic mechanisms and gene transcription [157,174,186]. The stress tolerance could also be related to GABA-induced changes in pathways associated with other phytohormones such as ABA (ABA receptors), ethylene (ACC oxidase, ACC synthase), PAs (arginine decarboxylase, free and conjugated forms, S-adenosylmethionine decarboxylase) and salicylate (Table 4) [60,156,172,175,187], which can regulate metabolic homeostasis and influence the expression of stress factors (miRNAs, transcription factors, heat shock proteins) with known and yet-to-be-determined functions [156,183,188].…”

γ-Aminobutyric Acid (GABA) Priming Improves Seed Germination and Seedling Stress Tolerance Associated With Enhanced Antioxidant Metabolism, DREB Expression, and Dehydrin Accumulation in White Clover Under Water Stress

“…In addition, the GABA application significantly increased the activity of POD and APX and the accumulation of osmolytes, thus effectively alleviating the oxidative damage and water imbalance in the leaves of perennial ryegrass ( Lolium perenne ) under water deficient condition ( Krishnan et al, 2013 ). The GABA enhanced antioxidant metabolism to mitigate oxidative damage, which is a key regulatory pathway for improving drought tolerance of creeping bentgrass ( Tang et al, 2020 ). Although the GABA is beneficial for plants adaption to abiotic stresses, the study about its function during seeds germination is still at initial stages.…”