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GABA and Potassium Modulates Defence Systems, Assimilation of Nitrogen and Carbon, and Yield Traits Under Salt Stress in Wheat

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Abstract

Salt stress cause enormous loss in crop productivity and yield around the globe, which jeopardizes agro-ecosystem, and significantly affects food production. Wheat is consumed all over the world, but is highly susceptible under salt stress conditions. In the present study, we investigated the independent and co-application of γ-aminobutyric acid (GABA) and potassium (K) to counteract salt-induced tolerance mechanisms, growth attributes and yield traits. Both GABA and K play indispensable roles in counteracting the deleterious impacts of oxidative stress indicators with activated defense mechanisms (ascorbate–glutathione pathway and glyoxalase system), improved nitrogen and carbon assimilation, and photosynthesis-related traits in salt stressed wheat plants. Moreover, GABA and K application induced considerable changes in osmolyte concentration, stomatal dynamics, and improved yield traits under salt stress in wheat plants. Overall, current study showed the significant outcomes of co-application of GABA and K in alleviating salt stress-induced adversities in wheat, and could be manipulated for developing salt tolerant wheat plants.

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References

  • Alamri S, Kushwaha BK, Singh VP, Siddiqui MH, Al-Amri AA, Alsubaie QD, Ali HM (2021) Ascorbate and glutathione independently alleviate arsenate toxicity in brinjal but both require endogenous nitric oxide. Physiol Plant 173(1):276–286

    CAS  PubMed  Google Scholar 

  • Asthir B, Kaur G, Kaur B (2020) Convergence of pathways towards ascorbate–glutathione for stress mitigation. J Plant Biol 63(4):243–257

    CAS  Google Scholar 

  • Balasooriya BL, Samson R, Mbikwa F, Boeckx P, Van Meirvenne M (2009) Biomonitoring of urban habitat quality by anatomical and chemical leaf characteristics. Environ Exp Bot 65:386–394

    CAS  Google Scholar 

  • Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100

    CAS  Google Scholar 

  • Barrs HD, Weatherly PE (1962) A re-examination of relative turgidity for estimating water deficits in leaves. Austra J Biol Sci 15:413–428

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    CAS  Google Scholar 

  • Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water use efficiency in a changing world. Front Plant Sci 10:225

    PubMed  PubMed Central  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    CAS  PubMed  Google Scholar 

  • Bohra JS, Doerffling K (1993) Potassium nutrition of rice (Oryza sativa L.) varieties under NaCl salinity. Plant Soil 152(2):299–303

    Google Scholar 

  • Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9(3):110–115

    CAS  PubMed  Google Scholar 

  • Bown AW, Shelp BJ (1997) The metabolism and functions of γ-aminobutyric acid. Plant Physiol 115:1–5

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. Abiotic Stress Plants Mech Adapt 1:21–38

    Google Scholar 

  • Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672

    CAS  PubMed  Google Scholar 

  • Crawford LA, Bown AW, Breitkreuz KE, Guinel FC (1994) The synthesis of γ-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol 104:865–871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65(5):1259–1270

    CAS  PubMed  Google Scholar 

  • Dixon RO, Fowden L (1961) γ-Aminobutyric acid metabolism in plants: part 2 metabolism in higher plants. Ann Bot 25(4):513–530

    CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1951) Colourimetric determination of sugars and related substances. Anal Chem 26:351–356

    Google Scholar 

  • Elia AC, Galarini R, Taticchi MI, Dörr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurusmelas under mercury exposure. Ecotoxol Environ Saf 55(2):162–167

    CAS  Google Scholar 

  • Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiol 72:297–302

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Ann Rev Plant Biol 64:429–450

    CAS  Google Scholar 

  • Fiala R, FialováI VM, Luxová M (2021) Effect of silicon on the young maize plants exposed to nickel stress. Plant Physiol Biochem 166:645–656

    CAS  PubMed  Google Scholar 

  • Foyer CH, Galtier N (1996) Source-sink interaction and communication in leaves. Photoassimilate distribution in plants and crops. Source-sink Relationships. New York 331–340.

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    CAS  PubMed  Google Scholar 

  • Giraldo P, Benavente E, Manzano-Agugliaro F, Gimenez E (2019) Worldwide research trends on wheat and barley: a bibliometric comparative analysis. Agronomy 9(7):352

    Google Scholar 

  • Goulding K, Murrell TS, Mikkelsen RL, Rosolem C, Johnston J, Wang H, Alfaro MA (2021) Outputs: potassium losses from agricultural systems. In: Murrell TS, Mikkelsen RL, Sulewski G, Norton R, Thompson ML (eds) Improving potassium recommendations for agricultural crops. Springer, Cham

    Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reducatse and 2-vinylpiridyne. Anal Biochem 106:207–212

    CAS  PubMed  Google Scholar 

  • Hageman RH, Reed AJ (1980) Nitrate reductase from higher plants. Meth Enzymol 69:270–280

    CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    CAS  PubMed  Google Scholar 

  • Hedge JE, Hofreiter BT (1962) In: Carbohydrate Chemistry, 17 (Eds) Whistler RL, Be Miller JN. Acad Press, New York

  • Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58(9):2369–2387

    CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Cir Calforn Agri Exp Stat 347:32

    Google Scholar 

  • Hossain MZ, Hossain MD, Fujita M (2006) Induction of pumpkin glutathione S-transferase by different stresses and its possible mechanisms. Biol Plant 50:210–218

    CAS  Google Scholar 

  • Hu W, Yang J, Meng Y, Wang Y, Chen B, Zhao W, Oosterhuis DM, Zhou Z (2015) Potassium application affects carbohydrate metabolism in the leaf subtending the cotton (Gossypium hirsutum L.) boll and its relationship with boll biomass. Field Crop Res 179:120–131

    Google Scholar 

  • Idrees S, Shabir S, Ilyas N, Batool N, Kanwal S (2015) Assessment of cadmium on wheat (Triticum aestivum L) in hydroponics medium. Agrociencia 49(8):917–929

    Google Scholar 

  • Isayenkov SV, Maathuis FJ (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80

    PubMed  PubMed Central  Google Scholar 

  • Jakli B, Tavakol E, Tränkner M, Senbayram M, Dittert K (2017) Quantitative limitations to photosynthesis in K deficient sunflower and their implications on water-use efficiency. J Plant Physiol 209:20–30

    CAS  PubMed  Google Scholar 

  • Jensen RG (2000) Activation of Rubisco regulates photosynthesis at high temperature and CO2. Proceed Nat Acad Sci 97(24):12937–12938

    CAS  Google Scholar 

  • Kaur C, Sharma S, Singla-Pareek SL, Sopory SK (2016) Methylglyoxal detoxification in plants: role of glyoxalase pathway. Ind J Plant Physiol 21(4):377–390

    Google Scholar 

  • Khan MIR, Khan NA (2017) Reactive oxygen species and antioxidant systems in plants: Role and regulation under abiotic stress. Springer Singapore, Singapore

    Google Scholar 

  • Khan MIR, Jahan B, AlAjmi MF, Rehman MT, Khan NA (2020) Ethephon mitigates nickel stress by modulating antioxidant system, glyoxalase system and proline metabolism in Indian mustard. PhysiolMolBiol Plants 26(6):1201–1213

    CAS  Google Scholar 

  • Khan MIR, Jalil SU, Chopra P, Chhillar H, Ferrante A, Khan NA, Ansari MI (2021) Role of GABA in plant growth, development and senescence. Plant Gene 26:100283

    CAS  Google Scholar 

  • Khanna RR, Jahan B, Iqbal N, Khan NA, AlAjmi MF, Rehman MT, Khan MI (2021) GABA reverses salt-inhibited photosynthetic and growth responses through its influence on NO-mediated nitrogen-sulfur assimilation and antioxidant system in wheat. J Biotech 10(325):73–82

    Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509

    CAS  Google Scholar 

  • Kraiser T, Gras DE, Gutiérrez AG, González B, Gutiérrez RA (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62(4):1455–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari S, Chhillar H, Chopra P, Khanna RR, Khan MI (2021) Potassium: a track to develop salinity tolerant plants. Plant Physiol Biochem 167:1011–1023

    CAS  PubMed  Google Scholar 

  • Kuo TM, Warner RL, Kleinhofs A (1982) In vitro stability of nitrate reductase from barley leaves. Phytochemistry 21(3):531–533

    CAS  Google Scholar 

  • Li ZG (2016) Methylglyoxal and glyoxalase system in plants: old players, new concepts. Bot Rev 82(2):183–203

    Google Scholar 

  • Lindner RC (1994) Rapid analytical methods for some of the more common inorganic constituents of plant tissues. Plant Physiol 19:1

    Google Scholar 

  • Maccarrone M, Melino G, Finazzi-Agro A (2001) Lipoxygenases and their involvement in programmed cell death. Cell Death Differ 8(8):776–784

    CAS  PubMed  Google Scholar 

  • Mayer RR, Cherry JL, Rhodes D (1990) Effects of heat shock on amino acid metabolism of cowpea cells. Phytochemistry 94:796–810

    CAS  Google Scholar 

  • Mekonnen DW, Flugge 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 

  • Mohammadi M, Karr AL (2001) Superoxide anion generation in effective and ineffective soybean root nodules. J Plant Physiol 158:1023–1029

    CAS  Google Scholar 

  • Mostofa MG, Ghosh A, Li ZG, Siddiqui MN, Fujita M, Tran LSP (2018) Methylglyoxal–a signaling molecule in plant abiotic stress responses. Free Rad Biol Med 122:96–109

    CAS  PubMed  Google Scholar 

  • Mullan D, Pietragalla J (2012) Leaf relative water content. Physiological breeding II: A field guide to wheat phenotyping CIMMYT, Mexico, 25–27.

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    CAS  Google Scholar 

  • Munns R, Day DA, Fricke W, Watt M, Arsova B, Barkla BJ, Bose J, Byrt CS, Chen Z-H, Foster KJ, Gilliham M, Henderson SW, Jenkins CLD, Kronzucker HJ, Miklavcic SJ, Plett D, Roy SJ, Shabala S, Shelden MC, Soole KL, Taylor NL, Tester M, Wege S, Wegner LH, Tyerman SD (2020) Energy costs of salt tolerance in crop plants. New Phytol 225:1072–1090

    CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Okamura M (1980) An improved method for determination of L-ascorbic acid and L-dehydroascorbic acid in blood plasma. Clin Chim Acta 103:259–268

    CAS  PubMed  Google Scholar 

  • Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Phyiol 97:1265–1267

    CAS  Google Scholar 

  • Pottosin I, Velarde-Buendía AM, Dobrovinskaya O (2014) Potassium and sodium transport channels under NaCl stress. In: Ahmad P, Wani MR (eds) Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, NewYork, pp 325–359

    Google Scholar 

  • Prasad A, Kumar S, Khaliq A, Pandey A (2011) Heavy metals and arbuscular mycorrhizal (AM) fungi can alter the yield and chemical composition of volatile oil of sweet basil (Ocimum basilicum L). Biol Fert Soil 47(8):853–861

    CAS  Google Scholar 

  • Principato GB, Rosi G, Talesa V (1987) Purification and characterization of two forms of glyoxalase II from the liver and brain of Wistar rats. Biochim Biophys Acta 911(3):349–355

    CAS  PubMed  Google Scholar 

  • 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(1):1–14

    CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rewald B, Shelef O, Ephrath JE, Rachmilevitch S (2013) Adaptive plasticity of salt-stressed root systems. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, NewYork, pp 169–201

    Google Scholar 

  • Roberts E (1988) The establishment of GABA as a neurotransmitter. In: Squires RF (ed) GABA and Benzodiazepine Receptors. CRC Press, Boca Raton, FL, pp 1–21

    Google Scholar 

  • Sabagh AE, Islam MS, Skalicky M, Raza MA, Singh K, Hossain MA, Hossain A, Mahboob W, Iqbal MA, Ratnasekera D, Singhal RK (2021) Salinity stress in wheat (Triticum aestivum L) in the changing climate: adaptation and management strategies. Front Agron. https://doi.org/10.3389/fagro.2021.661932

    Article  Google Scholar 

  • Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency with spatial reference to woodland flora. Phil Tran Royal Soc 216:1–65

    Google Scholar 

  • Satya Narayan V, Nair PM (1990) Metabolism, enzymology and possible roles of 4-aminobutyrate in higher plants. Phytochemistry 29:367–375

    Google Scholar 

  • Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60:709–711

    CAS  PubMed  Google Scholar 

  • Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669

    CAS  PubMed  Google Scholar 

  • Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trend Plant Sci 4(11):446–452

    CAS  Google Scholar 

  • Shipley B, Vu TT (2002) Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytol 153(2):359–364

    Google Scholar 

  • Smith MR, Rao IM, Merchant A (2018) Source-sink relationships in crop plants and their influence on yield development and nutritional quality. Front Plant Sci 9:1889

    PubMed  PubMed Central  Google Scholar 

  • Steward FC, Thompson JF, Dent CE (1949) γ-aminobutyric acid: a constituent of the potato tuber? Science 110:439–440

    Google Scholar 

  • Sustr M, Soukup A, Tylova E (2019) Potassium in root growth and development. Plants 8:435

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JF, Stewart CR, Morris CJ (1966) Changes in amino acid content of excised leaves during incubation. I. The effect of water content of leaves and atmospheric oxygen level. Plant Physiol 41:1578–1582

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during barley powdery mildew interaction. Plant J 11:1187–1194

    CAS  Google Scholar 

  • Tsushida T, Murai T (1987) Conversion of glutamic acid to γ-aminobutyric acid in tea leaves under anaerobic conditions. Agric Biol Chem 51:2865–2871

    CAS  Google Scholar 

  • Usuda H (1985) The activation state of ribulose 1,5-bisphosphate carboxylase in maize leaves in dark and light. Plant Cell Physiol 91:455–463

    Google Scholar 

  • Venora G, Calcagno F (1991) Study of stomatal parameters for selection of drought resistant varieties in Triticum durum DESF. Euphytica 57:275–283

    Google Scholar 

  • Vialet-Chabrand SR, Matthews JS, McAusland L, Blatt MR, Griffiths H, Lawson T (2017) Temporal dynamics of stomatal behavior: modeling and implications for photosynthesis and water use. Plant Physiol 174(2):603–613

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wahid I, Kumari S, Ahmad R, Hussain SJ, Alamri S, Siddiqui MH, Khan MI (2020) Silver nanoparticle regulates salt tolerance in wheat through changes in ABA concentration, ion homeostasis, and defense systems. Biomolecules 10(11):1506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace W, Secor J, Schrader LE (1984) Rapid accumulation of γ-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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: The N-acetyl-L-cysteine assay. Anal Bioanal Chem 403(9):2577–2581

    CAS  PubMed  Google Scholar 

  • Wu Q, Su N, Huang X, Cui J, Shabala L, Zhou M, Yu M, Shabala S (2021) Hypoxia-induced increase in GABA content is essential for restoration of membrane potential and preventing ROS-induced disturbance to ion homeostasis. Plant Comm 2(3):100188

    CAS  Google Scholar 

  • Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59(12):3317–3325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu SM, Lo SF, Ho THD (2015) Source–sink communication: Regulated by hormone, nutrient, and stress cross-signaling. Trend Plant Sci 20(12):844–857

    CAS  Google Scholar 

  • Zahoor R, Dong H, Abid M, Zhao W, Wang Y, Zhou Z (2017) Potassium fertilizer improves drought stress alleviation potential in cotton by enhancing photosynthesis and carbohydrate metabolism. Environ Exp Bot 137:73–83

    CAS  Google Scholar 

  • Zhang F, Niu J, Zhang W, Chen X, Li C, Yuan L, Xie J (2010) Potassium nutrition of crops under varied regimes of nitrogen supply. Plant Soil 335(1):21–34

    CAS  Google Scholar 

  • Zorb C, Senbayram M, Peiter E (2014) Potassium in agriculture – status and perspectives. J Plant Physiol 171(9):656–669

    PubMed  Google Scholar 

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Acknowledgements

MIRK is gratefully acknowledging the SERB-DST Grant (SRG/2020/001004).

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  1. Department of Botany, Jamia Hamdard, New Delhi, India

    Sarika Kumari, Faroza Nazir, Kajal Jain & M. Iqbal R. Khan

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  1. Sarika Kumari
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  2. Faroza Nazir
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  4. M. Iqbal R. Khan
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Contributions

Conceptualization, MIRK; experimentation, data analysis and software, SK, FN and KJ; Writing—Original draft preparation, SK and MIRK; Writing – Review and editing, MIRK, SK and FN. All authors have read and agreed to the published version of the manuscript.

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Correspondence to M. Iqbal R. Khan.

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Kumari, S., Nazir, F., Jain, K. et al. GABA and Potassium Modulates Defence Systems, Assimilation of Nitrogen and Carbon, and Yield Traits Under Salt Stress in Wheat. J Plant Growth Regul 42, 6721–6740 (2023). https://doi.org/10.1007/s00344-023-10992-3

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