SpringerLink
Log in

An Appraisal of Ancient Molecule GABA in Abiotic Stress Tolerance in Plants, and Its Crosstalk with Other Signaling Molecules

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Gamma-aminobutyric acid (GABA), a non-proteinaceous amino acid, is reported in prokaryotes and eukaryotes, since ancient times. However, it has gained attention in the present time because of its rapid accumulation during stressed conditions in plants as well as in the cyanobacteria. In plants, it regulates the number of physiological processes such as pollen tube growth, root growth, TCA cycle, N2-metabolism, and osmoregulation. Several biotic and abiotic stresses prevail in the environment, which lead to enhanced accumulation of reactive oxygen species (ROS) thus causing oxidative damage. However, a rapid increase in the accumulation of GABA during stress in various plant forms like bacteria, cyanobacteria, fungi, and plants indicates its putative role in stress regulation and acclimation. This review summarizes the biosynthesis of GABA, its role in abiotic stress tolerance, and its crosstalk with ROS, nitric oxide, Ca+2 ions, phytohormones, and polyamines in stress acclimation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aghdam MS, Asghari M, Farmani B, Mohayeji M, Moradbeygi H (2012) Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. Sci Hortic 144:116–120

    CAS  Google Scholar 

  • Aghdam MS, Naderi R, Sarcheshmeh MAA, Babalar M (2015) Amelioration of postharvest chilling injury in anthurium cut flowers by γ-aminobutyric acid (GABA) treatments. Postharvest Biol Technol 110:70–76

    Google Scholar 

  • Akçay N, Bor M, Karabudak T, Ozdemir F, Türkan I (2012) Contribution of Gamma aminobutyric acid (GABA) to salt stress responses of Nicotianasylvestris CMSII mutant and wild type plants. J Plant Physiol 169:452–458

    PubMed  Google Scholar 

  • Alcazar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876. https://doi.org/10.1007/s10529-006-9179-3

    Article  CAS  PubMed  Google Scholar 

  • Al-Quraan NA, Al-Sharbati M, Dababneh Y, Al-Olabi M (2014) Effect of temperature, salt, and osmotic stresses on seed germination and chlorophyll contents in lentil (Lens culinaris Medik). Acta Hortic. https://doi.org/10.17660/ActaHortic.2014.1054.4

    Article  Google Scholar 

  • AL-Quraan NA, AL-Omari HA (2017) GABA accumulation and oxidative damage responses to salt, osmotic and H2O2 treatments in two lentil (Lens culinaris Medik) accessions. Plant Biosys 151:148–157

    Google Scholar 

  • 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. https://doi.org/10.1007/s11738-015-1836-5

    Article  Google Scholar 

  • Ashraf M (1993) Effect of sodium chloride on water relations and some organic osmotica in arid zone plant species Melilotus indica (L.) All Der. Tropen Land Wirt 94:95–102

    Google Scholar 

  • Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3421

    CAS  PubMed  Google Scholar 

  • Babateen OM (2016) GABA signaling regulation by GLP-1 receptor agonists and GABA—a receptors modulator. Dissertation. Acta Universitatis Upsaliensis, Uppsala. ISBN 978-91-554-9548-0

  • Begara-Morales JC, Chaki M, Valderrama R, Sánchez-Calvo B, Mata-Pérez C, Padilla MN, Huorpas FJ, Barroso JB (2018) Nitric oxide buffering and conditional nitric oxide release in stress response. J Exp Bot 69:3425–3438

    CAS  PubMed  Google Scholar 

  • Bhattacharjee S (2014) Membrane lipid peroxidation and its conflict of interest: the two faces of oxidative stress. Curr Sci 107:11

    Google Scholar 

  • Boonburapong B, Laloknam S, Incharoensakdi A (2015) Accumulation of gamma-aminobutyric acid in the halotolerant cyanobacterium Aphanothece halophytica under salt and acid stress. J Appl Phycol 28:1

    Google Scholar 

  • Bor M, Turkan I (2019) Is there a room for GABA in ROS and RNS signalling? Environ Exp Bot 161:67–73

    CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    CAS  PubMed  Google Scholar 

  • Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    CAS  PubMed  Google Scholar 

  • Bown AW, Shelp BJ (2016) Plant GABA: not just a metabolite. Trends in Plant Sci 21:811–813

    CAS  Google Scholar 

  • Carapito R, Hatsch D, Vorwerk S, Petkovski E, Jeltsch JM, Phalip V (2008) Gene expression in Fusarium graminearum grown on plant cell wall. Fungal Genet Biol 45:738–748

    CAS  PubMed  Google Scholar 

  • Carillo P (2018) GABA shunt in durum wheat. Front Plant Sci 9:100

    PubMed  PubMed Central  Google Scholar 

  • Carvajal F, Palma F, Jamilena M, Garrido D (2015) Preconditioning treatment induces chilling tolerance in zucchini fruit improving different physiological mechanisms against cold injury. Ann Appl Biol 166:340–354

    CAS  Google Scholar 

  • Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945

    PubMed  PubMed Central  Google Scholar 

  • Cheng B, Li Z, Liang L, Cao Y, Zeng W, Zhang X, Ma X, Huang L, Nie G, Liu W, Peng Y (2018) The γ-aminobutyric acid (GABA) alleviates salt stress damage during seeds germination of white clover associated with Na+/K+ transportation, dehydrins accumulation, and stress-related genes expression in white clover. Int J Mol Sci 19:9

    Google Scholar 

  • Che-Othman MH, Jacoby RP, Millar AH, Taylor NL (2019) Wheat mitochondrial respiration shifts from the TCA cycle to the GABA shunt under salt stress. New Phytol 225(3):1166–1180

    PubMed  Google Scholar 

  • Corpas FJ, Del Rio LA, Palma JM (2019) Plant peroxisomes at the crossroad of NO and H2O2 metabolism. J Integr Plant Biol 61(7):803–816

    CAS  PubMed  Google Scholar 

  • Cui H, Kong Y, Zhang H (2011) Oxidative stress, mitochondrial dysfunction, and aging. J Signal Transduct 2012:13

    Google Scholar 

  • Cui Y, Miao K, Niyaphorn S, Qu X (2020) Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. Int J Mol Sci 21:995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dagron A, Chapalain A, Mijouin L, Hillion M, Duclairoir-Poc C, Chevalier S, Taupin L, Orange N, Feuilloley MGJ (2013) Effect of gaba, a bacterial metabolite, on Pseudomonas fluorescens surface properties and cytotoxicity. Int J Mol Sci 14(6):12186–12204

    Google Scholar 

  • Daş ZA, Dimlioğlu G, Bor M, Özdemir F (2016) Zinc induced activation of GABA-shunt in tobacco (Nicotiana tobaccum L.). Environ Exp Bot 122:78–84

    Google Scholar 

  • De Angeli A, Zhang J, Meyer S, Martinoia E (2013) AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat Commun 4:1804

    PubMed  Google Scholar 

  • De Simone A, Hubbard R, De la TNV, Velappan Y, Wilson M, Considine MJ, Soppe WJJ, Foyer CH (2017) Redox changes during the cell cycle in the embryonic meristem of Arabidopsis thaliana. Antioxid Redox Signal 27:1505–1519

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz-Vivancos P, De SA, Kiddle G, Foyer CH (2015) Glutathione-linking cell proliferation to oxidative stress. Free Radic Biol Med 89:1154–1104

    CAS  PubMed  Google Scholar 

  • Dimlioğlu G, Daş ZA, Bor M, Özdemir F, Türkan İ (2015) The impact of GABA in harpin-elicited biotic stress responses in Nicotiana tabaccum. J Plant Physiol 188:51–57

    PubMed  Google Scholar 

  • Dutta S, Mitra M, Agarwal P, Mahapatra K, De S, Sett U, Roy S (2018) Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal Behav 13:8

    Google Scholar 

  • El-kereamy A, Ranathunge Bi Y-M, K, Beatty PH, Good AG, Rothstein SJ, (2012) The Rice R2R3-MYB Transcription Factor OsMYB55 Is Involved in the Tolerance to High Temperature and Modulates Amino Acid Metabolism. PLoS ONE. 7(12):e52030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan LQ, Yang LW, Gao HB, Wu XL, **a Q, Gong BB (2012) Effects of exogenous gamma-aminobutyric acid on polyamine metabolism of melon seedlings under hypoxia stress. Ying Yong Sheng Tai XueBao 23(6):1599–1606

    CAS  Google Scholar 

  • Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis AKA, Tavladoraki P (2012) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62:1155–1168

    Google Scholar 

  • Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194(1):7–15

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilliham M, Tyerman SD (2016) Linking metabolism to membrane signaling: the GABA-malate connection. Trends Plant Sci 21(4):295–301

    CAS  PubMed  Google Scholar 

  • Guan YJ, Hu J, Wang XJ, Shao CX (2009) Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress. J Zhejiang Univ Sci B 10(6):427–433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851

    CAS  PubMed  Google Scholar 

  • Guo Z, Tan J, Zhuo C, Wang C, **ang B, Wang Z (2014) Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosyl methionine synthetase in Medicago sativa sub sp. falcata that confers cold tolerance through up-regulating polyamine oxidation. Plant Biotechnol J 12:601–612

    CAS  PubMed  Google Scholar 

  • Hu XH, Xu ZR, Xu WN, Li JM, 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

    CAS  PubMed  Google Scholar 

  • Jalil SU, Iqbal M, Khan R, Ansari MI (2019) Role of GABA transaminase in the regulation of development and senescence in Arabidopsis thaliana. Curr Plant Biol 19:100119

    Google Scholar 

  • Jantaro S, Kanwal S (2017) Low-Molecular-Weight Nitrogenous Compounds (GABA and Polyamines) in Blue-Green Algae. Algal Green Chemistry. https://doi.org/10.1016/B978-0-444-63784-0.00008-4

    Article  Google Scholar 

  • Ji J, Yue J, **e T, Chen W, Du C, Chang E, Shi S (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(3):675–690

    CAS  PubMed  Google Scholar 

  • Jiao C, Duan Y, Lin Q (2019) MAPK mediates NO/cGMP-induced GABA accumulation in soybean sprouts. Food Sci Technol 100:253–262

    Google Scholar 

  • Kanwal S, Incharoensakdi A (2019) The role of GAD pathway for regulation of GABA accumulation and C/N balance in Synechocystis sp. PCC6803. J Appl Phycol 31:3503–3514

    Google Scholar 

  • Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509

    CAS  Google Scholar 

  • Kobayashi Y, Ohyama Y, Kobayashi Y, Ito H, Iuchi S, Fujita M, Zhao CR, Tanveer T, Ganesan M, Kobayashi M, Koyama H (2014) STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol Plant 7(2):311–322

    CAS  PubMed  Google Scholar 

  • Koike S, Matsukura C, Takayama M, Asamizu M, Ezura H (2013) Suppression of γ -aminobutyric acid (GABA) transaminases induces prominent GABA accumulation, dwarfism and infertility in the tomato (Solanum lycopersicum L.). Plant Cell Physiol 54:793–807

    CAS  PubMed  Google Scholar 

  • Krishnamurthy A, Rathinasabapathi B (2013) Auxin and its transport play a role in plant tolerance to arsenite induced oxidative stress in Arabidopsis thaliana. Plant Cell Environ 36(10):1838–1849

    CAS  PubMed  Google Scholar 

  • Krishnan S, Laskowski 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(5):358–366

    Google Scholar 

  • 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 7:8786

    PubMed  PubMed Central  Google Scholar 

  • Li Z, Yu J, Peng Y, Huang B (2016) Metabolic pathways regulated by γ-aminobutyric acid (GABA) contributing to heat tolerance in cree** bentgrass (Agrostis stolonifera). Sci Rep 6:30338

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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(2):436–449

    CAS  Google Scholar 

  • Li Z, Peng Y, Huang B (2018) Alteration of transcripts of stress-protective genes and transcriptional factors by γ-aminobutyric acid (GABA) associated with improved heat and drought tolerance in cree** bentgrass (Agrostis stolonifera). Int J Mol Sci 19:1623

    PubMed  PubMed Central  Google Scholar 

  • Li Z, Cheng B, Zeng W, Liu Z, Peng Y (2019) The transcriptional and post-transcriptional regulation in perennial cree** bentgrass in response to γ-aminobutyric acid (GABA) and heat stress. Environ Exper Bot 162:515–524

    CAS  Google Scholar 

  • Li L, Dou N, Zhang H, Wu C (2021) The versatile GABA in plants. Plant Signal Behav 16:1862565. https://doi.org/10.1080/15592324.2020.1862565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin JS, Kuo CC, Yang IC, Tsai WA, Shen YH, Lin CC, Liang YC, Li YC, Kuo YW, King YC, Lai HM, Jeng ST (2018) MicroRNA160 modulates plant development and heat shock protein gene expression to mediate heat tolerance in Arabidopsis. Front Plant Sci 9:68

    PubMed  PubMed Central  Google Scholar 

  • Liu T, Liu Z, Li Z, Peng Y, Zhang X, Ma X, Huang L, Liu W, Nie G, He L (2019) Regulation of heat shock factor pathways by γ-aminobutyric acid (GABA) associated with thermotolerance of cree** Bentgrass. Int J Mol Sci 20(19):4713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu X, Guan Q, Zhu J (2013) Down regulation of CSD2 by a heat-inducible miR398 is required for thermotolerance in Arabidopsis. Plant Signal Behav. 8:e24952

    PubMed  PubMed Central  Google Scholar 

  • Luo HY, Gao Yang LW, **ao-Lei HB, WU, Liu HH, (2011) Physiological mechanism of GABA soaking to tomato seed germination and seedling development under NaCl stress. Acta Bot Boreal Occid Sin 31:2235–2242

    CAS  Google Scholar 

  • Ma Y, Wang P, Chen Z, Gu Z, Yang R (2018) GABA enhances physio-biochemical metabolism and antioxidant capacity of germinated hulless barley under NaCl stress. J Plant Physiol 231:192–201

    CAS  PubMed  Google Scholar 

  • Majumdar R, Barchi B, Turlapati SA, Gagne M, Minocha R, Long S, Minocha SC (2016) Glutamate, ornithine, arginine, proline, and polyamine metabolic interactions: the pathway is regulated at the post-transcriptional level. Front Plant Sci 7:78

    PubMed  PubMed Central  Google Scholar 

  • Malekzadeh P, Khara J, Heidari R (2012) Effect of exogenous Gamma-aminobutyric acid on physiological tolerance of wheat seedlings exposed to chilling stress. Iran J Plant Physiol 3:1

    Google Scholar 

  • Malekzadeh P, Khara J, Heydari R (2014) Alleviating effects of exogenous Gamma-aminobutiric acid on tomato seedling under chilling stress. Physiol Mol Biol Plants 20(1):133–137

    CAS  PubMed  Google Scholar 

  • Malekzadeh P, Khosravi-Nejad F, Hatamnia AA, Mehr RS (2017) Impact of postharvest exogenous γ-aminobutyric acid treatment on cucumber fruit in response to chilling tolerance. Physiol Mol Biol Plants 23:827–836

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marček T, Hamow KÁ, Végh B, Janda T, Darko E (2019) Metabolic response to drought in six winter wheat genotypes. PLoS ONE 14:2

    Google Scholar 

  • 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(14):3755–3766

    CAS  PubMed  Google Scholar 

  • Mekonnen DW, Flügge UI, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci 245:25–34

    CAS  PubMed  Google Scholar 

  • Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KAS, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63:1054–1062

    CAS  PubMed  Google Scholar 

  • Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: Are GABA metabolism and signaling entwined? Front Plant Sci 6:419

    PubMed  PubMed Central  Google Scholar 

  • Mirabella R, Rauwerda H, Allmann S, Scala A, Spyropoulou EA, De VM, Boersma MR, Breit TM, Haring MA, Schuurink RC (2015) WRKY40 and WRKY6 act downstream of the green leaf volatile E-2-hexenal in Arabidopsis. Plant J 83:6

    Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125

    CAS  PubMed  Google Scholar 

  • Mohapatra S, MinochaLong RS, Minocha SC (2010) Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids 38:4

    Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    CAS  PubMed  Google Scholar 

  • Nayyar H, Kaur R, Kaur S, Singh R (2014) γ-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

    CAS  Google Scholar 

  • Nonaka S, Arai C, Takayama M, Matsukura C, Ezura H (2017) Efficient increase of ɣ-aminobutyric acid (GABA) content in tomato fruits by targeted mutagenesis. Sci Rep 7(1):7057

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palma F, Carvajal F, Ramos JM, Jamilena M, Garrido D (2015) Effect of putrescine application on maintenance of zucchini fruit quality during cold storage: contribution of GABA shunt and other related nitrogen metabolites. Postharvest Biol Technol 99:131–140

    CAS  Google Scholar 

  • Palmer AJ, Baker A, Muench SP (2016) The varied functions of aluminium-activated malate transporters–much more than aluminium resistance. BiochemSoc Trans 44:856–862

    CAS  Google Scholar 

  • Planamente S, Vigouroux A, Mondy S, Nicaise M, Faure D, Morera S (2010) A conserved mechanism of GABA binding and antagonism is revealed by structure-function analysis of the periplasmic binding protein Atu2422 in Agrobacterium tumefaciens. J Biol Chem. 285(39):30294–30303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109

    PubMed  PubMed Central  Google Scholar 

  • Podlesakova K, Ugena L, Spichal L, Dolezal K, De DN (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 48:53–65

    CAS  Google Scholar 

  • Priya M, Sharma L, Kaur R, Bindumadhava H, Nair RM, Siddique KHM, Nair 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    CAS  PubMed  Google Scholar 

  • Ramesh S, Tyerman S, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijó JA, Ryan PR, Gilliham M (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 6:7879

    CAS  PubMed  Google Scholar 

  • Ramesh SA, Tyerman SD, Gilliham M, Xu B (2016) γ-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74:1577–1603

    PubMed  Google Scholar 

  • Ramesh SA, Tyerman SD, Gilliham M, Xu B (2017) g-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74:1577–1603

    CAS  PubMed  Google Scholar 

  • Ramesh SA, Kamran M, Sullivan W, Chirkova L, Okamoto M, Degryse F, McLaughlin M, Gilliham M, Tyerman SD (2018) Aluminum-activated malate transporters can facilitate GABA transport. Plant Cell 30:1147–1164

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos-Ruiz R, Martinez F, Knauf-Beiter G (2019) The effects of GABA in plants. Cogent Food Agric 5(1):1670553

    Google Scholar 

  • Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saeidia M, Moradib F, Abdolic M (2017) Impact of drought stress on yield, photosynthesis rate, and sugar alcohols contents in wheat after anthesis in semiarid region of Iran. Arid Land Res Manag 31(2):204–218

    Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, Del RLA (2013) Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. Sub cell Biochem. https://doi.org/10.1007/978-94-007-6889-5_13

    Article  Google Scholar 

  • Scholz SS, Malabarba J, Reichelt M, Heyer M, Ludewig F, Mithofer A (2017) Evidence for GABA-induced systemic GABA accumulation in Arabidopsis upon wounding. Front Plant Sci 8:388

    PubMed  PubMed Central  Google Scholar 

  • Seifikalhor M, Aliniaeifard S, Hassani B, Niknam V, Lastochkina O (2019) Diverse role of γ-aminobutyric acid in dynamic plant cell responses. Plant Cell Rep. https://doi.org/10.1007/s00299-019-02396-z

    Article  PubMed  Google Scholar 

  • Shang H, Cao S, Yang Z, Cai Y, Zheng Y (2011) Effect of exogenous gamma-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. J Agric Food Chem 59(4):1264–1268

    CAS  PubMed  Google Scholar 

  • Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ (2012a) Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci 193(194):130–135

    PubMed  Google Scholar 

  • Shelp BJ, Bozzo GG, Simpson ZA, JP, Trobache CP, Allan WL, (2012b) Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. II. Integr Anal Bot 90(9):781–793

    CAS  Google Scholar 

  • Shelp BJ, Bozzo GG, Zarei A, Simpson JP, Trobacher CP, Allan WL (2012c) Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. Integr anal Bot 90(9):781–793

    CAS  Google Scholar 

  • Shelp BJ, Zarei A (2017) Subcellular compartmentation of 4-aminobutyrate (GABA) metabolism in Arabidopsis: an update. Plant Signal Behav 12:e1322244

    PubMed  PubMed Central  Google Scholar 

  • Sheng L, Shen D, Luo Y, Sun X, Wang J, Luo T, Zeng Y, Xu J, Deng X, Cheng Y (2017) Exogenous γ-aminobutyric acid treatment affects citrate and amino acid accumulation to improve fruit quality and storage performance of postharvest citrus fruit. Food Chem 216:138–145

    CAS  PubMed  Google Scholar 

  • Sheteiwy MS, Shao H, Qi W, Hamoud YA, Shaghaleh H, Khan NU, Yang R, Tang B (2019) GABA-alleviated oxidative injury induced by salinity, osmotic stress and their combination by regulating cellular and molecular signals in rice. Int J Mol Sci 20(22):5709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi SQ, Zheng S, Jiang ZP, Qi LW, Sun XM, Li CX, Liu JF, **ao 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

    CAS  PubMed  Google Scholar 

  • Signorelli S, Dans PD, Coitino EL, Borsani O, Monza J (2015) Connecting proline and γ-aminobutyric acid in stressed plants through non-enzymatic reactions. PLoS ONE 10(3):e0115349

    PubMed  PubMed Central  Google Scholar 

  • Singh R, Parihar P, Singh S, Mishra RK, Singh VP, Prasad SM (2017) Reactive oxygen species signaling and stomatal movement: current updates and future perspectives. Redox Biol 11:213–218

    PubMed  Google Scholar 

  • Steward F, Thompson J, Dent C (1949) γ-Aminobutyric acid, a constituent of the potato tuber. Sci 110:439–440

    Google Scholar 

  • Su N, Wu Q, Chen J, Shabala L, Mithöfer A, Wang H, Qu M, Yu M, Shabala CJ, S, (2019) GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion. J Exp Bot 70:6349–6361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suhel M, Husain T, Prasad SM, & Singh VP (2022) GABA Requires Nitric Oxide for Alleviating Arsenate Stress in Tomato and Brinjal Seedlings. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10576-7

    Article  Google Scholar 

  • Takayama M, Koike S, Kusano M, Matsukura C, Saito K, Ariizumi T, Ezura H (2015) Tomato glutamate decarboxylase genes SlGAD2 and SlGAD3 play key roles in regulating γ-aminobutyric acid levels in tomato (Solanum lycopersicum). Plant Cell Physiol 56:1533–1545

    CAS  PubMed  Google Scholar 

  • Takayama M, Matsukura C, Ariizumi T, Ezuram H (2017) Activating glutamate decarboxylase activity by removing the autoinhibitory domain leads to hyper γ-aminobutyric acid (GABA) accumulation in tomato fruit. Plant Cell Re 36:103–116

    CAS  Google Scholar 

  • Talbi SMC, Romero-Puertas A, Hernandez L, Terron A, Ferchichi LMS (2015) Drought tolerance in a Saharian plant Oudneya africana: Role of antioxidant defences. Environ Exp Bot 111:114–126

    Google Scholar 

  • Tang X, Yu R, Zhou Q, Jiang S, Le G (2018) Protective effects of γ-aminobutyric acid against H2O2-induced oxidative stress in RIN-m5F pancreatic cells. Nutr Metab (lond) 15:60

    PubMed  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrian M, Alcazar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18

    CAS  PubMed  Google Scholar 

  • Turkan I (2018) ROS and RNS: key signalling molecules in plants. J Exp Bot 69(14):3313–3315

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signal Behav 3:525–536

    PubMed  PubMed Central  Google Scholar 

  • Vijayakumari K, Puthur J (2016) γ-Aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Regul 78(1):57–67

    CAS  Google Scholar 

  • Virdi AS, Singh S, Singh P (2015) Abiotic stress responses in plants: roles of calmodulin regulated proteins. Front Plant Sci 6:809

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Luo Z, Huang X, Yang K, Gao S, Du R (2014) Effect of exogenous c-aminobutyric acid (GABA) treatment on chilling injury and antioxidant capacity in banana peel. Sci Hortic-Amst 168:132–137

    CAS  Google Scholar 

  • Wang X, Huang W, Yang Z, Liu J, Huang B (2016) Transcriptional regulation of heat shock proteins and ascorbate peroxidase by CtHsfA2b from African bermudagrass conferring heat tolerance in Arabidopsis. Sci Rep 6:28021

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Gu W, Meng Y, **e T, Li L, Li J, Wei S (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

    PubMed  PubMed Central  Google Scholar 

  • Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D’Amelia L, Dell’Aversana E, Piccolella S, Fuggi A, Carillo P (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiol Plant 159:290–312

    CAS  PubMed  Google Scholar 

  • **ng SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of gamma-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem. 45(8):560–6

    CAS  PubMed  Google Scholar 

  • Xu Y, Zhan C, Huang B (2011) Heat shock proteins in association with heat tolerance in grasses. Int J Proteomics. https://doi.org/10.1155/2011/529648

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu M, Gruber BD, Delhaize E, White RG, James RA, You J, Yang Z, Ryan PR (2015) The barley anion channel, HvALMT1, has multiple roles in guard cell physiology and grain metabolism. Physiol Plant 153:183–193

    CAS  PubMed  Google Scholar 

  • Xu B, Long Y, Feng X, Zhu X, Sai N, Chirkova L, Betts A, Herrmann J, Edwards EJ, Okamoto M (2021) GABA signalling modulates stomatal opening to enhance plant water use efficiency and drought resilience. Nat Commun 12:1952

    PubMed  PubMed Central  Google Scholar 

  • Yang A, Cao S, Yang Z, Cai Y, Zheng Y (2011) γ-Aminobutyric acid treatment reduces chilling injury and activates the defence response of peach fruit. Food Chem 129:1619–1622

    CAS  Google Scholar 

  • Yang R, Guo Q, Gu Z (2013) GABA shunt and polyamine degradation pathway on γ-aminobutyric acid accumulation in germinating fava bean (Vicia faba L.) under hypoxia. Food Chem 136:152–159

    CAS  PubMed  Google Scholar 

  • Yin Y, Yang R, Gu Z (2014) Calcium regulating growth and GABA metabolism pathways in germinating soybean (Glycine max L.) under NaCl stress. Eur Food Res Technol 239(1):149–156

    CAS  Google Scholar 

  • Yong B, **e H, Li Z, Li Y-P, Zhang Y, Nie G, Zhang XQ, Ma X, Huang LK, Yan YH, Peng Y (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

    PubMed  PubMed Central  Google Scholar 

  • Yu D, Eldred WD (2005) Glycine and GABA interact to regulate the nitric oxide/cGMP signaling pathway in the turtle retina. Visual Neuro Sci 22(6):825

    Google Scholar 

  • Yu C, Zeng L, Sheng K, Chen F, Zhou T, Zheng X, Yu T (2014) γ-Aminobutyric acid induces resistance against Penicillium expansum by priming of defence responses in pear fruit. Food Chem 159:29–37

    CAS  PubMed  Google Scholar 

  • Zarei A, Trobacher CP, Shelp BJ (2015a) NAD+-aminoaldehyde dehydrogenase candidates for 4-aminobutyrate (GABA) and β-alanine production during terminal oxidation of polyamines in apple fruit. FEBS Lett 589:2695–2700

    CAS  PubMed  Google Scholar 

  • Zarei A, Trobacher CP, Cooke AR, Meyers AJ, Hall JC, Shelp BJ (2015b) Apple fruit copper amine oxidase isoforms: peroxisomal MdAO1 prefers diamines as substrates, whereas extracellular MdAO2 exclusively utilizes monoamines. Plant Cell Physiol 56:137–147

    CAS  PubMed  Google Scholar 

  • Zarei A, Trobacher CP, Shelp BJ (2016) Arabidopsis aldehyde dehydrogenase 10 family members confer salt tolerance through putrescine-derived 4-aminobutyrate (GABA) production. Sci Rep 6:35115

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zarei A, Chiu GZ, Yu G, Trobacher CP, Shelp BJ (2017) Salinity-regulated expression of genes involved in GABA metabolism and signalling. Botany 95:6

    Google Scholar 

  • Zhong H, Tong L, Gu N, Gao F, Lu Y, **e RG, Zhang X (2017) Endocannabinoid signaling in hypothalamic circuits regulates arousal from general anesthesia in mice. J Clin Investig 127(6):2295–2309

    PubMed  PubMed Central  Google Scholar 

  • Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9

    CAS  PubMed  Google Scholar 

  • Zhu X, Liao J, **a X, **ong 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

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Mohammad Suhel is grateful to the University Grants Commission, New Delhi, for granting fellowship. Tajammul Husain thankful to the CSIR for providing fellowship. Dr. Samiksha Singh is grateful to the University Grants Commission for providing Dr. D.S. Kothari Post-Doctoral Fellowship (No. F.4-2/2006(BSR)/OT/19-20/0006) to carry out this work. Aparna Pandey is thankful as SRF (CSIR UGC-NET Dec. 2018, Ref. No. 627).

Author information

Authors and Affiliations

  1. Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, 211002, India

    Mohammad Suhel, Tajammul Husain, Aparna Pandey & Sheo Mohan Prasad

  2. Centre of Advanced Studies in Botany, Institute of Science, Banaras Hindu University, Varanasi, 221005, India

    Samiksha Singh & Nawal Kishore Dubey

  3. Plant Physiology Laboratory, Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, 211002, India

    Vijay Pratap Singh

Authors
  1. Mohammad Suhel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tajammul Husain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aparna Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Samiksha Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nawal Kishore Dubey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sheo Mohan Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vijay Pratap Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

VPS and SMP conceptualized the idea. MS, TH, AP, and SS wrote the review. NKD, SMP, and VPS corrected review.

Corresponding authors

Correspondence to Sheo Mohan Prasad or Vijay Pratap Singh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Naeem Khan.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suhel, M., Husain, T., Pandey, A. et al. An Appraisal of Ancient Molecule GABA in Abiotic Stress Tolerance in Plants, and Its Crosstalk with Other Signaling Molecules. J Plant Growth Regul 42, 614–629 (2023). https://doi.org/10.1007/s00344-022-10610-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10610-8

Keywords

Search

Navigation