Abstract
Unfavorable environmental conditions such as heat, cold, drought, metal/metalloid toxicity, and pathogens enhance production of intra-and inter-cellular levels of reactive oxygen species (ROS) in plants. ROS, acting as signaling molecules, activate signal transduction pathways in response to various stresses. Alternatively, ROS cause irreversible cellular damage due to lipid peroxidation, oxidation of protein, inactivation of enzymes, DNA damage, and interact with other vital constituents of plant cells through their strong oxidative properties, which drastically alter plant morphological structures, becoming disadvantageous for survival and productivity. Higher plants have complex defense systems to scavenge ROS. Being a central molecule of the defense system, gamma-aminobutyric acid (GABA) is ubiquitous from prokaryotes to eukaryotes cells. GABA helps mitigate ROS in plants and GABA shunt pathway plays a key role either as metabolites or endogenous signaling molecules in several regulatory mechanisms under stress conditions. The GABA transporters (GATs) being activated with the attachment of GABA under environmental stress stimuli facilitate high content of Ca2+ into the cytosol. Ca2+ combines with calmodulin (CaM) -binding domain that activates the glutamate decarboxylase (GAD) enzyme for the conversion of glutamate into GABA. This synchronized process regulates GABA shunt gene expressions under stress conditions and improves defense mechanisms in plants. This review highlights the regulatory aspects of GABA shunt pathway for ROS production as well as in the defense mechanism of plants.
Similar content being viewed by others
Abbreviations
- AATs:
-
Amino acid transporters
- ABA:
-
Abscisic acid
- ALDH:
-
Aldehyde dehydrogenase
- ALMT:
-
Aluminum-activated malate transporter
- Al:
-
Aluminium
- AtGABP:
-
Arabidopsis thaliana GABA permease
- ATP:
-
Adenosine triphosphate
- AtProT:
-
Arabidopsis thaliana proline transporter
- C:
-
Carbon
- Ca:
-
Calcium
- Ca(NO3)2 :
-
Calcium nitrate
- CaM:
-
Calmodulin or calcium-modulated
- Cd:
-
Cadmium
- Cr:
-
Cromium
- DAO:
-
Diamine oxidase
- ETC:
-
Electron transport chain
- GABA:
-
Gamma-aminobutyric acid
- GABA-T:
-
GABA transaminase
- GAD:
-
Glutamate decarboxylase
- GATs:
-
GABA transporters
- GHB:
-
γ-Hydroxybutyric acid
- H+ :
-
Proton
- HO2 • :
-
Hydroperoxyl radical
- H2O2 :
-
Hydrogen peroxide
- LeProT:
-
Solanum lycopersicum proline transporter
- MDA:
-
Malondialdehyde
- MDH:
-
Malate dehydrogenase
- N:
-
Nitrogen
- NAD+ :
-
Nicotinamide adenine dinucleotide
- NADH:
-
Nicotinamide adenine dinucleotide + hydrogen
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate + hydrogen
- O2 •− :
-
Superoxide radical
- 1O2 :
-
Singlet oxygen
- OH• :
-
Hydroxyl radical
- ONOO• :
-
Peroxynitrite
- PAs:
-
Polyamines
- PAO:
-
Polyamine oxidase
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- Pro:
-
Proline
- ProTs:
-
Proline transporters
- PYRR:
-
Pyrroline
- PYRRDH:
-
Pyrroline dehydrogenase
- ROS:
-
Reactive oxygen species
- RO• :
-
Alkoxy radical
- ROO• :
-
Peroxy radical
- SSA:
-
Succinic semialdehyde
- SSADH:
-
Semialdehyde dehydrogenase
- SSR:
-
Succinic semialdehyde reductase
- TRX:
-
Thioredoxin
- UV:
-
Ultra violet
References
Aghdam MS, Naderi R, Jannatizadeh A, Sarcheshmeh MAA, Babalar M (2016) Enhancement of postharvest chilling tolerance of Anthurium cut flowers by gamma-aminobutyric acid (GABA) treatments. Sci Hortic 198:52–60
Akçay N, Bor M, Karabudak T, Özdemir F, Türkan I (2012) Contribution of gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. J Plant Physiol 169:452–458
Alqarawi AA, Hashem A, Abd-Allah EF, Al-Huqal AA, Alshahrani TS, Alshalawi SR (2016) Protective role of γ- aminobutyric acid on Cassia italica Mill under salt stress. Legume Res 39:396–404
Al-Quraan NA (2015) GABA shunt deficiencies and accumulation of reactive oxygen species under UV treatments: insight from Arabidopsis thaliana calmodulin mutants. Acta Physiol Plant 37:86
Al-QuraanAL-AjlouniObedat NZD (2019) The GABA shunt pathway in germinating seeds of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) under salt stress. Seed Sci Res 29:250–260
Al-Quraan NA, Al-Share AT (2016) Characterization of the γ-aminobutyric acid shunt pathway and oxidative damage in Arabidopsis thaliana pop 2 mutants under various abiotic stresses. Biol Plant 60:132–138
Al-Quraan NA, Locy RD, Singh NK (2011) Implications of paraquat and hydrogen peroxide-induced oxidative stress treatments on the GABA shunt pathway in Arabidopsis thaliana calmodulin mutants. Plant Biotechnol Rep 5:225–234
Al-Quraan NA, Sartawe FA, Qaryouti MM (2013) Characterization of γ-aminobutyric acid metabolism and oxidative damage in wheat (Triticum aestivum L.) seedlings under salt and osmotic stress. J Plant Physiol 170:1003–1009
Annicchiarico P, Piano E (2004) Indirect selection for root development of white clover and implications for drought tolerance. J Agron Crop Sci 190:28–34
Ansari MI, Chen SCG (2009) Biochemical characterization of gamma-aminobutyric acid (GABA): pyruvate transaminase during rice leaf senescence. Int J Integr Biol 16:27–32
Ansari MI, Lee RH, Chen SCG (2005) A novel senescence- associated gene encoding γ-aminobutyric acid (GABA): pyruvate transaminase is upregulated during rice leaf senescence. Physiol Plant 123:1–8
Ansari MI, Hasan S, Jalil SU (2014) Leaf senescence and GABA shunt. Bioinformation 10:730–732
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396
Ashraf MFMR, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Bai Q, Yang R, Zhang L, Gu Z (2013) Salt stress induces accumulation of γ-aminobutyric acid in germinated foxtail millet (Setaria italica L.). Cereal Chem 90:145–149
Bai X, Xu J, Shao X, Luo W, Niu Z, Gao C, Wan D (2019) A novel gene coding γ-aminobutyric acid transporter may improve the tolerance of Populus euphratica to adverse environments. Front Plant Sci 10:123–131
Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiol 141:311. https://doi.org/10.1104/pp.104.900191
Bao H, Li Y (2015) Virus-induced gene silencing reveals control of reactive oxygen species accumulation and salt tolerance in tomato by γ- aminobutyric acid metabolic pathway. Plant Cell Environ 38:600–613
Batushansky A, Kirma M, Grillich N, Pham PA, Rentsch D, Galili G, Fernie AR, Fait A (2015) The transporter GAT1 plays an important role in GABA-mediated carbon–nitrogen interactions in Arabidopsis. Front Plant Sci 6:785. https://doi.org/10.3389/fpls.2015.00785
Baum G, Chen Y, Arazi T, Takatsuji H, Fromm H (1993) A plant glutamate decarboxylase containing a calmodulin binding domain. J Biol Chem 268:19610–19617
Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H (1996) Calmudulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. Embo J 15:2988–2996
Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:1113–1121
Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115
Bouché N, Fait A, Bouché D, Møller SG, Fromm H (2003) Mitochondrial succinate-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt in required to restricts levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100:6843–6848
Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125
Bown AW, Shelp BJ (1997) The metabolism and function of gamma aminobutyric acid. Plant Physiol 115:1–5
Bown AW, Hall DE, MacGregor KB (2002) Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiol 129:1430–1440
Bown AW, MacGregor KB, Shelp BJ (2006) γ- aminobutyrate: defense against invertebrate pests? Trends Plant Sci 11:424–427
Breitbreuz KE, Shelp BJ (1995) Subcellular compartmentation of the 4-aminobutyrate shunt in protoplast from developing soybean cotelydons. Plant Physiol 108:99–103
Breitkreuz KE, Shelp BJ, Fischer WN, Rentsch D (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett 450:280–284
Breitkreuz KE, Allan WL, Van Cauwenberghe OR, Jakobs C, Talibi D, Andre B, Shelp BJ (2003) A novel gamma-hydroxybutyrate dehydrogenase: identification and expression of an Arabidopsis cDNA and potential role under oxygen deficiency. J Biol Chem 278:41552–41556
Cao J, Barbosa JM, Singh NK, Locy RD (2013) GABA shunt mediates thermotolerance in Saccharomyces cerevisiae by reducing the production of reactive oxygen species. Yeast 30:129–144
Cekic FÖ (2018) Exogenous GABA stimulates endogenous GABA and phenolic acid contents in tomato plants under salt stress. Celal Bayar Uni J Sci 14:61–64
Che-Othman MH, Jacoby RP, Millar AH, Taylor NL (2019) Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytol 225:1166–1180
Clark SM, Di Leo R, Dhanoa PK, Van Cauwenberghe OR, Mullen RT, Shelp BJ (2009) Biochemical characterization, mitochondrial localization, expression, and potential functions for an Arabidopsis γ-aminobutyrate transaminase that utilizes both pyruvate and glyoxylate. J Exp Bot 60:1743–1757
Coleman ST, Fang TK, Rovinsky SA, Turano FJ, Moye- Rowley WS (2001) Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem 276:244–250
Corpas FJ, Barroso JB, del Río LA (2002) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163. https://doi.org/10.1186/1471-2229-11-163
Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107
Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, Das Gupta J, Tyryshkin A (2001) The origin of atmospheric oxygen on earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98:2170–2175
Dover S, Halpern YS (1972) Utilization of γ-aminobutyric acid as the sole carbon and nitrogen source by Escherichia coli K-12 mutants. J Bacteriol 109(2):835–843
Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Ann Rev Plant Physiol Plant Mol Biol 48:223–250
Duan JJ, Li J, Guo SR, Kang YY (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620e1635. https://doi.org/10.1016/j.jplph.2007.11.006
Du H, Wang Z, Yu W, Huang B (2012) Metabolic responses of hybrid bermudagrass to short-term and long-term drought stress. J Am Soc Hortic Sci. https://doi.org/10.21273/JASHS.137.6.411
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147. https://doi.org/10.3389/fpls.2017.01147
Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415–420
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13:14–19
Fan L, Wu X, Tian Z, Jia K, Pan Y, Li J, Gao H (2015) Comparative proteomic analysis of gamma-aminobutyric acid responses in hypoxia-treated and untreated melon roots. Phytochem 116:28–37
Fu D, Sun Y, Yu C, Zheng X, Yu T, Lu H (2017) Comparison of the effects of three types of aminobutyric acids on the control of Penicillium expansum infection in pear fruit. J Sci Food Agric 97:1497–1501
Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia – is survival a balancing act? Trends Plant Sci 9:449–456
Gilliham M, Tyerman SD (2016) Linking metabolism to membrane signaling: the GABA-malate connection. Trends Plant Sci 21:295–301
Gregersen PL, Culetic A, Boschian L, Krupnska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622
Guo P, Baum M, Grando S, Ceccarelli S, Bai G, Li R, Korff MV, Varshney RK, Graner A, Valkoun J (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544
Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Front Plant Sci 7(9):1343. https://doi.org/10.3389/fpls.2016.01343
Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322
Hatmi S, Gruau C, Trotel-Aziz P, Villaume S, Rabenoelina F, Baillieul F, Aziz A (2015) Drought stress tolerance in grapevine involves activation of polyamine oxidation contributing to improved immune response and low susceptibility to Botrytis cinerea. J Exp Bot 66(3):775–787
Hoover GJ, Van Cauwenberghe OR, Breitkreuz KE, Clark SM, Merrill AR, Shelp BJ (2007) Characteristics of an Arabidopsis glyoxylate reductase: general biochemical properties and substrate specificity for the recombinant protein, and developmental expression and implications for glyoxylate and succinic semialdehyde metabolism in planta. Can J Bot 85:883–895
Hu WH, Song XS, Shi K, Xia XJ, Zhou YH, Yu JQ (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46:581–588
Hu X, Xu Z, Xu W, Li J, Zhao N, Zhou Y (2015) Application of γ-aminobutyric acid demonstrates a protective role of polyamine and GABA metabolism in muskmelon seedlings under Ca(NO3)2 stress. Plant Physiol Biochem 92:1–10
Jalil SU, Ansari MI (2008) Plant microbiome and its functional mechanism in response to environmental stress. Int J Green Pharm 12:S81. https://doi.org/10.22377/ijgp.v12i01.1603
Jalil SU, Ansari MI (2020a) Stress implication and crop productivity. In: Hasanuzzaman M (ed) Plant ecophysiology and adaptation under climate change: mechanism and perspectives. Springer, Singapore, pp 73–86
Jalil SU, Ansari MI (2020b) Physiological role of gamma aminobutyric acid in salt stress tolerance. In: Hasanuzzaman M, Tanveer M (eds) Salt and drought stress tolerance in plants, signaling and communication in plants. Springer, Switzerland, pp 337–350
Jalil SU, Ahmad I, Ansari MI (2016) Phenotypic characterization of GABA-transaminase mutants of Arabidopsis thaliana. Adv Life Sci 5:10005–10008
Jalil SU, Ahmad I, Ansari MI (2017) Functional loss of GABA transaminase (GABA-T) expressed early leaf senescence under various stress conditions in Arabidopsis thaliana. Curr Plant Biol 9–10:11–22
Jalil SU, Khan MAA, Ansari MI (2019a) Tremendous role of GABA shunt metabolic pathway in plant system. J Biol Chem Res 36:188–196
Jalil SU, Khan MQR, Ansari MI (2019b) Role of GABA transaminase in the regulation of development and senescence in Arabidopsis thaliana. Curr Plant Biol 19:100119. https://doi.org/10.1016/j.cpb.2019.100119
Ji J, Yue J, XieChenDuChangChenJiangShi TWCELZS (2018) Roles of γ-aminobutyric acid on salinity-responsive genes at transcriptomic level in poplar: involving in abscisic acid and ethylene-signalling pathways. Planta 248:675–690
Jia Y, Zou D, Wang J, Sha H, Liu H, Inayat MA, Sun J, Zheng H, Xia N, Zhao H (2017) Effects of γ- aminobutyric acid, glutamic acid, and calcium chloride on rice (Oryza sativa L.) under cold stress during the early vegetative stage. J Plant Growth Regul 36:240–253
Jin X, Liu T, Xu J, Gao Z, Hu X (2019) Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biol 19:48. https://doi.org/10.1186/s12870-019-1660-y
Kalhor MS, Aliniaeifard S, Seif M, Asayesh EJ, Bernard F, Hassani B, Li T (2018) Enhanced salt tolerance and photosynthetic performance: implication of γ-aminobutyric acid application in salt-exposed lettuce (Lactuca sativa L.) plants. Plant Physiol Biochem 130:157–172
Kalhor MS, Aliniaeifard S, Bernard F, Seif M, Latifi M, Hassani B, Didaran F, Bossachi M, Rezadoost H, Li T (2020) γ-aminobutyric acid confers cadmium tolerance in maize plants by concerted regulation of polyamine metabolism and antioxidant defense systems. Sci Rep 10:3356. https://doi.org/10.1038/s41598-020-59592-1
Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32
Karuppanapandian T, Moon JC, Kim C, Manoharan K, Kim W (2011) Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci 5:709–725
Kaur R, Zhawar VK (2021) Regulation of secondary antioxidants and carbohydrates by gamma-aminobutyric acid under salinity–alkalinity stress in rice (Oryza sativa L.). Biol Fut. https://doi.org/10.1007/s42977-020-00055-z
Kenersley AM, Turano FJ (2000) Gamma-aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509
Krishnan S, Laskowski K, Shukla V, Merewitz EB (2013) Mitigation of drought stress damage by exogenous application of a non-protein amino acid γ-aminobutyric acid on perennial ryegrass. J Am Soc Hortic Sci 138:358–366
Kumar N, Dubey AK, Upadhyay AK, Gautam A, Ranjan R, Srikishna S, Sahu N, Behera SK, Mallick S (2017) GABA accretion reduces Lsi-1 and Lsi-2 gene expressions and modulates physiological responses in Oryza sativa to provide tolerance towards arsenic. Sci Rep 7:1. https://doi.org/10.1038/s41598-017-09428-2
Kwak J, Nguyen V, Schroeder J (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329
Lane TR, Stiller M (1970) Glutamic acid decarboxylation in Chlorella. Plant Physiol 45:558–562
Lee JH, Kim YJ, Jeong DY, Sathiyaraj G, Pulla RK, Shim JS, In JG, Yang DC (2010) Isolation and characterization of a glutamate decarboxylase (GAD) gene and their differential expression in response to abiotic stresses from Panax ginseng C. A. Meyer. Mol Biol Rep 37:3455–3463
Lee J, Kim S, Kim S, Shim IS (2020) Production of γ-aminobutyric acid and its supplementary role in the TCA cycle in rice (Oryza sativa L.) seedlings. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10066-8
Li MF, Guo SJ, Yang XH, Meng QW, Wei XJ (2016a) Exogenous gamma-aminobutyric acid increases salt tolerance of wheat by improving photosynthesis and enhancing activities of antioxidant enzymes. Biol Plant 60:123–131
Li Z, Yu J, Peng Y, Huang B (2016b) Metabolic pathways regulated by γ-aminobutyric acid (GABA) contributing to heat tolerance in creeping bentgrass (Agrostissto lonifera). Sci Rep 6:30338. https://doi.org/10.1038/srep30338
Li Y, Fan Y, Ma Y, Zhang Z, Yue H, Wang L, Li J, Jiao Y (2017) Effects of exogenous γ-aminobutyric acid (GABA) on photosynthesis and antioxidant system in pepper (Capsicum annuum L.) seedlings under low light stress. J Plant Growth Regul 36:436–449
Li E, Luo X, Liao S, Shen W, Li Q, Liu F, Zou Y (2018) Accumulation of γ-aminobutyric acid during cold storage in mulberry leaves. Int J Food Sci Technol 53:2664–2672
Liu X, Huang B (2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bent grass. Crop Sci 40:503–510
Liu C, Zhao L, Yu G (2011) The dominant glutamic acid metabolic flux to produce γ-aminobutyric acid over proline in Nicotiana tabacum leaves under water stress relates to its significant role in antioxidant activity. J Integr Plant Biol 53:608–618
Locy RD, Wu SJ, Bisnette J, Barger TW, McNabb D, Zik M, Fromm H, Singh NK, Cherry JH (2000) The regulation of GABA accumulation by heat stress in Arabidopsis. In: Cherry JH, Locy RD, Rychter (eds) Plant tolerance to abiotic stresses in agriculture: Role of genetic engineering. NATO Science Series (Series 3: High Technology) Springer: Dordrecht. pp. 39-52
Lou YR, Bor M, Yan J, Preuss AS, Jander G (2016) Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation. Plant Physiol 171(2):1443–1455
Ma Y, Wang P, Wang M, Sun M, Gu Z, Yang R (2018) GABA mediates phenolic compounds accumulation and the antioxidant system enhancement in germinated hulless barley under NaCl stress. Food Chem 270:593–601
MacGregor KB, Shelp BJ, Peiris SE, Bown AW (2003) Overexpression of glutamate decarboxylase in transgenic tobacco deters feeding by phytophagous insect larvae. J Chem Ecol 29:2177–2182
Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49
Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017) γ-aminobutyric acid (GABA) confers chromium stress tolerance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology 26:675–690
Malekzadeh P, Khara J, Heydari R (2014) Alleviating effects of exogenous gamma-aminobutyric acid on tomato seedling under chilling stress. Physiol Mol Biol Plants 20:133–137
Matysik J, Alia A, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532
Mazzucotelli E, Tartari A, Cattivelli L, Forlani G (2006) Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57:3755–3766
McLean MD, Yevtushenko DP, Deschene D, Van Cauwenberghe OR, Makhmoudova A, Potter JW, Bown AW, Shelp BJ (2003) Overexpression of glutamate decarboxylase in transgenic tobacco plants confers resistance to the northern root-knot nematode. Mol Breed 11:277–285
Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PBK (2004) Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68
Meyer A, Eskandari S, Grallath S, Rentsch D (2006) AtGAT1, a high affinity transporter for γ-aminobutyric acid in Arabidopsis thaliana. J Biol Chem 281:7197–7204
Mhamdi A, Van Breusegem F (2018) Reactive oxygen species in plant development. Development 145:dev164376. https://doi.org/10.1242/dev.164376
Michaeli S, Fait A, Lagor K, Nunes-Nesi A, Grillich A, Yellin A, Bar D, Khan M, Fernie AR, Turano FJ, Fromm H (2011) A mitochondrial GABA permease connects the GABA shunt and the TCA cycle and is essential for normal carbon metabolism. Plant J Cell Mol Biol 67:485–498
Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5(5):175. https://doi.org/10.3389/fpls.2014.00175
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19
Miyashita Y, Good A (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol 49:92–102
Mo H, Wang X, Zhang Y, Zhang G, Zhang J, Ma Z (2015) Cotton polyamine oxidase is required for spermine and camalexin signalling in the defence response to Verticillium dahliae. Plant J 83:962–975
Morse DE, Hooker N, Duncan H, Jensen L (1979) Gamma aminobutyric acid, a neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science 204:407–410
Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13
Navrot N, Roubier N, Gelbaye E, Jacquot JP (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185–195
Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190:355–365
Nayyar H, Kaur R, Kaur S, Singh R (2014) Υ- aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul 33:408–419
Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134
Palma F, Carvajal F, Jiménez-Muñoz R, Pulido A, Jamilena M, Garrido D (2019) Exogenous γ-aminobutyric acid treatment improves cold tolerance of zucchini fruit during postharvest storage. Plant Physiol Biochem 136:188–195
Park DH, Mirabella R, Bronstein PA, Preston GM, Haring MA, Lim CK, Collmer A, Schuurink RC (2010) Mutations in γ-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J 64:318–330
Podlešáková K, Ugena L, Spíchal L, Dole K, De Diego N (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 48(1):53–65
Prasad PVV, Bheemanahalli R, Jagadish SVK (2017) Field crops and the fear of heat stress-opportunities, challenges and future directions. Field Crops Res 200:114–121
Priya M, Sharma L, Kaur R, Bindumadhava H, Nair RM, Siddique KHM, Nayyar H (2019) GABA (γ-aminobutyric acid), as a thermo-protectant, to improve the reproductive function of heat-stressed mungbean plants. Sci Rep 9:7788. https://doi.org/10.1038/s41598-019-44163-w
Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 29:7879. https://doi.org/10.1038/ncomms8879
Ramputh AI, Bown AW (1996) Rapid γ- aminobutyric acid synthesis and the inhibition of the growth and development of oblique-banded leaf roller larvae. Plant Physiol 111:1349–1352
Reimer RJ, Fremeau RT, Bellocchio EE, Edwards RH (2001) The essence of excitation. Curr Opin Cell Biol 13:417–420
Renault H, Roussel V, El-Amrani A, Arzel M, Renault D, Bouchéreau A, Deleu C (2010) The Arabidopsis pop 2–1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 10:20. https://doi.org/10.1186/1471-2229-10-20
Renault H, El-Amrani A, Berger A, Mouille G, Taconnat LS, Bouchereau A, Deleu C (2013) γ-aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ 36:1009–1018
Rezaei-Chiyaneh E, Seyyedi SM, Ebrahimian E, Moghaddam SS, Damalas CA (2018) Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind Crops Prod 112:741–748
Rico A, Preston GM (2008) Pseudomonas syringae pv. Tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant-Microbe Interact 21:269–282
Sachdev S, Ansari SA, Ansari MI, Fujita M, Hasanuzzaman M (2021) Abiotic stress and reactive oxygen species: generation, signaling, and defense mechanisms. Antioxidants 10(2):277. https://doi.org/10.3390/antiox10020277
Salah A, Zhan M, Cao C, Han Y, Ling L, Liu Z, Li P, Ye M, Jiang Y (2019) γ-aminobutyric acid promotes chloroplast ultrastructure, antioxidant capacity, and growth of waterlogged maize seedlings. Sci Rep 9:484. https://doi.org/10.1038/s41598-018-36334-y
Satyanarayan V, Nair PM (1990) Metabolism, enzymology and possible roles of 4-aminobutyrate in higher plants. Phytochem 29:367–375
Scholz SS, Reichelt M, Mekonnen DW, Ludewig F, Mithöfer A (2015) Insect herbivory-elicited GABA accumulation in plants in wound-induced, direct, systemic and jasmonate-dependent defense response. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01128
Schwacke R, Gralath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-aminobutyric acid in tomato pollen. Plant Cell 11:377–392
Seifi HS, Shelp BJ (2019) Spermine differentially refines plant defense responses against biotic and abiotic stresses. Front Plant Sci 10(2):117. https://doi.org/10.3389/fpls.2019.00117
Seifi HS, Curvers K, De Vleesschauwer D, Deleare I, Aziz A, Hofte M (2013) Concurrent overactivation of the cytosolic glutamine synthetase and the GABA shunt in the ABA-deficient sitiens mutant tomato leads to resistance against Botrytis cinerea. New Phytol 199:490–550
Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144
Shang H, Shifeng C, Zhenfeng Y, Yuting C, Yonghua Z (2011) Effect of exogenous γ-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. J Agric Food Chem 59:1264–1268
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. https://doi.org/10.1155/2012/217037
Shelp BJ, Bown AW, Mclean MD (1999) Metabolism and function of gamma aminobutyric acid. Trends Plant Sci 4:446–452
Shelp BJ, Van Cauwenberghe OR, Bown AW (2003) Gamma aminobutyrate: from intellectual curiosity to practical pest control. Can J Bot 81:1045–1048
Shelp BJ, Bown AW, Faure D (2006) Extracellular γ-aminobutyrate mediates communication between plants and other organisms. Plant Physiol 142:1350–1352
Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ (2012) Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci 193–194:130–135
Shi SQ, Shi Z, Jiang ZP, Qi LW, Sun XM, Li CX, Liu JF, Xiao WF, Zhang SG (2010) Effects of exogenous GABA on gene expression of Caragana intermedia roots under NaCl stress: regulatory roles for H2O2 and ethylene production. Plant Cell Environ 33:149–162
Signorelli S, Dans PD, Coitiño EL, Borsani O, Monza J (2015) Connecting proline and γ-aminobutyric acid in stressed plants through non-enzymatic reactions. PLoS ONE 10:e0115349. https://doi.org/10.1371/journal.pone.0115349
Simpson JP, Di Leo R, Dhanoa PK, Allan WL, Makhmoudova A, Clark SM, Hoover GJ, Mollen RT, Shelp BJ (2008) Identification and characterization of a plastid localized Arabidopsis glyoxylate reductase isoform: comparison with a cytosolic isoform and implications for cellular redox homeostasis and aldehyde detoxification. J Exp Bot 59:2545–2554
Snowden CJ, Thomas B, Baxter CJ, Smith JAC, Sweetlove LJ (2015) A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition. Plant J 81:651–660
Solomon PS, Oliver RP (2002) Evidence that γ-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato. Planta 214:414–420
Song H, Wang XX, Wang H, Taoa YH (2010) Exogenous γ-aminobutyric acid alleviates oxidative damage caused by aluminium and proton stresses on barley seedlings. J Sci Food Agri 90:1410–1416
Song S, Li J, Gao H, Li QY, Yang LW, Gong RJ (2012) Effect of exogenous γ-aminobutyric acid on inorganic nitrogen metabolism and mineral elements contents of melon seedling under hypoxia stress. Acta Hort Sin 39:695–704
Steward FC, Thompson JF, Dent CE (1949) γ-aminobutyric acid a constituent of potato tubers? Sci 110:439–440
Sung MS, Chow TJ, Lee TM (2011) Polyamine acclimation alleviates hyper salinity-induced oxidative stress in a marine green microalga, Ulva fasciata, by modulation of antioxidative enzyme gene expression. J Phycol 47(3):538–547
Swanson S, Gilroy S (2010) ROS in plant development. Physiol Plant 138:384–392
Tanou G, Molassiotis A, Diamantidis G (2009) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot 65:270–281
Tarkowski ŁP, Signorelli S, Höfte M (2020) γ-Aminobutyric acid and related amino acids in plant immune responses: emerging mechanisms of action. Plant Cell Environ 43:1103–1116
Tegeder MWJM (2012) Molecular evolution of plant AAP and LHT amino acid transporters. Front Plant Physiol 3:1–11. https://doi.org/10.3389/fpls.2012.00021
Tian XL, Wu XL, Li Y, Zhang SQ (2005) The effect of gamma-aminobutyric acid in superoxide dismutase, peroxidase and catalase activity response to salt stress in maize seedling. Shi Yan Sheng Wu Xue Bao 38:75–79
Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452. https://doi.org/10.3389/fpls.2018.00452
Tretter YP, Hertel M, Munz B, Bruggencate G, Werner S, Alzheimer C (2000) Induction of activin A is essential for the neuroprotective action of basic fibroblast growth factor in vivo. Nat Med 6:812–815
Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390
Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol 154:444–448
Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655
Vijayakumari K, Puthur JT (2015) γ-aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Regul 78:57–67
Wallace W, Secor J, Schrader LE (1984) Rapid accumulation of gamma-aminobutyric acid and alanine in soybean leaves in response to an abrupt transfer to lower temperature, darkness, or mechanical manipulation. Plant Physiol 75:170–175
Wang CY, Li JR, Xia QP, Wu XL, Gao HB (2014a) Influence of exogenous γ-aminobutyric acid (GABA) on GABA metabolism and amino acid contents in roots of melon seedling under hypoxia stress. J Appl Ecol 25:2011–2018
Wang Y, Luo Z, Huang X, Yang K, Gao S, Du R (2014b) Effect of exogenous γ-aminobutyric acid (GABA) treatment on chilling injury and antioxidant capacity in banana peel. Sci Hortic 168:132–137
Wang Y, Gu W, Meng Y, Xie T, Li L, Li J (2017) γ-aminobutyric acid imparts partial protection from salt stress injury to maize seedlings by improving photosynthesis and upregulating osmoprotectants and antioxidants. Sci Rep 7:43609. https://doi.org/10.1038/srep43609
Waqas MA, Kaya C, Riaz A, Farooq M, Nawaz I, Wilkes A, Li Y (2019) Potential mechanisms of abiotic stress tolerance in crop plants induced by thiourea. Front Plant Sci 10:1336. https://doi.org/10.3389/fpls.2019.01336
Xia QP, Goa HB, Li JR (2011) Effects of γ– aminobutyric acid on the photosynthesis and chlorophyll fluorescence parameters of muskmelon seedlings under hypoxia stress. Chin J Appl Ecol 22:999–1006
Yadav SK (2010) Cold stress tolerance mechanisms in plants. A review. Agron Sustain Dev 30:515–527
Yamauchi T, Fukazawa A, Nakazono M (2017) METALLOTHIONEIN genes encoding ROS scavenging enzymes are down-regulated in the root cortex during inducible aerenchyma formation in rice. Plant Signal Behav 12(11):e1388976. https://doi.org/10.1080/15592324.2017.1388976
Yang A, Cao S, Yang Z (2011) γ-aminobutyric acid treatment reduces chilling injury and activates the defence response of peach fruit. Food Chem 129:1619–1622
Yang R, Guo Q, Gu Z (2013) GABA shunt and polyamine degradation pathway on g-aminobutyric acid accumulation in germinating fava bean (Vicia faba L.) under hypoxia. Food Chem 136:152159. https://doi.org/10.1016/j.foodchem.2012.08.008
Yang J, Sun C, Zhang Y, Fu D, Zheng X, Yu T (2017) Induced resistance in tomato fruit by γ- aminobutyric acid for the control of Alternaria rot caused by Alternaria alternata. Food Chem 22:1014–1020
Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation. Plant Physiol 132(4):1973–1981
Yong B, Xie H, Li Z, Li YP, Zhang Y, Nie G, Zhang XQ, Ma X, Huang LK, Yan YH (2017) Exogenous application of GABA improves PEG-induced drought tolerance positively associated with GABA-shunt, polyamines, and proline metabolism in white clover. Front Physiol 8:1107. https://doi.org/10.3389/fphys.2017.01107
Yu C, Zeng L, Sheng K, Chen F, Yu T (2014) Υ- aminobutyric acid induces resistance against Penicillium expansum by priming of defense responses in pear fruit. Food Chem 159:29–37
Zarei A, Christophe P, Trobacher Shelp J (2016) Arabidopsis aldehyde dehydrogenase 10 family members confer salt tolerance through putrescine-derived 4-aminobutyrate (GABA) production. Sci Rep 6:35115. https://doi.org/10.1038/srep35115
Zeng J, Dong Z, Wu H, Tian Z, Zhao Z (2017) Redox regulation of plant stem cell fate. EMBO J 36:2844–2855
Zhao Y, Song X, Zhong DB, Yu L, Yu X (2020) γ-aminobutyric acid (GABA) regulates lipid production and cadmium uptake by Monoraphidium sp. QLY-1 under cadmium stress. Biores Technol 297:122500. https://doi.org/10.1016/j.biortech.2019.122500
Zhu X, Liao J, Xia X, Xiong F, Li Y, Shen J, Wen B, Ma Y, Wang Y, Fang W (2019) Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature. BMC Plant Biol 19:43. https://doi.org/10.1186/s12870-019-1646-9
Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant development. Cell Mol Biol Lett 10:515–534
Acknowledgements
We acknowledge very gratefully the past and present candidates of my laboratory as well as my scientific collaborator. Thanks are also due to Department of Science and Technology (Science and Engineering Research Board), Government of India, for their financial support to Mohammad Israil Ansari (Grant No. CRG/2018/000267). We acknowledge Md. Mahabub Alam, Department of Agronomy, Sher-e-Bangla Agricultural University, for his critical readings of the manuscript draft.
Author information
Authors and Affiliations
Contributions
Conceptualization, M.I.A. and M.H.; writing—original draft preparation, M.I.A., S.U.J; writing—review and editing, M.H., SAA, MIA; visualization, S.U.J., M.H.; supervision, M.I.A. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ansari, M.I., Jalil, S.U., Ansari, S.A. et al. GABA shunt: a key-player in mitigation of ROS during stress. Plant Growth Regul 94, 131–149 (2021). https://doi.org/10.1007/s10725-021-00710-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-021-00710-y