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The GABA shunt pathway in germinating seeds of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) under salt stress

Published online by Cambridge University Press:  06 December 2019

Nisreen A. AL-Quraan Open the ORCID record for Nisreen A. AL-Quraan [Opens in a new window] ,
Zakaria I. AL-Ajlouni  and
Dana I. Obedat
Nisreen A. AL-Quraan*
Affiliation:
Department of Biotechnology and Genetic Engineering, Faculty of Science and Arts, Jordan University of Science and Technology, Irbid22110, Jordan
Zakaria I. AL-Ajlouni
Affiliation:
Department of Plant Production, Faculty of Agriculture, Jordan University of Science and Technology, Irbid22110, Jordan
Dana I. Obedat
Affiliation:
Department of Biotechnology and Genetic Engineering, Faculty of Science and Arts, Jordan University of Science and Technology, Irbid22110, Jordan
*
Author for correspondence: Nisreen A. AL-Quraan, Email: naquraan@just.edu.jo
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Abstract

Soil salinity is one of the major abiotic stresses affecting seed germination, crop growth and productivity. In this study, seeds of three wheat (Triticum aestiveum L.) and three barley (Hordeum vulgare L.) cultivars were treated with different concentrations of NaCl to investigate the effect of salt on seed germination physiology and metabolism through the characterization of seed germination pattern, gamma-aminobutyric acid (GABA) shunt metabolite accumulation [GABA, glutamate (Glu) and alanine (Ala)] and glutamate decarboxylase (GAD) expression using RT-PCR. A trend of decreasing germination percentage with increasing NaCl concentrations was observed. Under all salt stress treatments, data showed significant increase with positive correlation (r = 0.50–0.99) between abundance of GABA shunt metabolites and salt concentration in all wheat and barley cultivars for 5 days. Increased GABA content was associated with a small but significant increase in Ala and Glu content in all cultivars. In all NaCl treatments, the transcription of GAD in terms of RNA abundance showed a significant increase in all cultivars with positive correlation (r = 0.50–0.98). Data showed significant association between GAD RNA transcription and the response of germinating seeds to salt stress in terms of GABA shunt metabolite accumulation. The elevated expression of GAD under salinity suggests the need for elevated activity of the GAD-mediated conversion of Glu to GABA during seed germination, which provides alternative metabolic routes to the respiratory machinery, balancing carbon and nitrogen metabolism and osmolyte synthesis in germinating seeds of wheat and barley under salt stress.

Keywords

barleyGABAgamma aminobutyric acidGADglutamateglutamate decarboxylasesalt stressseed germinationwheat
Type
Research Paper
Information
Seed Science Research , Volume 29 , Issue 4 , December 2019 , pp. 250 - 260
Copyright
Copyright © Cambridge University Press 2019

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References

Abdul Jaleel, C., Gopi, R., Sankar, B., Manivannan, P., Kishorekumar, A., Sridharan, R. and Panneerselvam, R. (2007) Studies on germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress. South African Journal of Botany 73, 190–195.CrossRefGoogle Scholar
Abebe, T., Guenzi, A.C., Martin, B. and Cushman, J.C. (2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiology 131, 1748–1755.CrossRefGoogle ScholarPubMed
Akçay, N., Bor, M., Karabudak, T., Özdemir, F. and Türkan, I. (2012) Contribution of gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. Journal of Plant Physiology 169, 452–458.CrossRefGoogle ScholarPubMed
Allan, W., Simpson, J., Clark, S. and Shelp, B. (2008) γ-Hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms. Journal of Experimental Botany 59, 2555–2564.CrossRefGoogle ScholarPubMed
Almansouri, M., Kinet, J.M. and Lutts, S. (2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant and Soil 231, 243–254.CrossRefGoogle Scholar
AL-Quraan, N.A. and Al-Omari, H.A. (2017) GABA accumulation and oxidative damage responses to salt, osmotic and H2O2 treatments in two lentil (Lens culinaris Medik) accessions. Plant Biosystems 151, 148–157.Google Scholar
AL-Quraan, N.A. and Al-Sharbati, M., Dababneh, Y. and Al-Olabi, M. (2014) Effect of temperature, salt and osmotic stresses on seed germination and chlorophyll contents in lentil (Lens culinaris Medik). Acta Horticulturae 1054, 47–54.CrossRefGoogle Scholar
AL-Quraan, N.A. and AL-Share, A.T. (2016). Characterization of GABA shunt pathway and oxidative damage in Arabidopsis thaliana mutants of gamma-aminobutyric acid transaminase (POP2) under various abiotic stresses. Biologia Plantarum 60, 132–138.CrossRefGoogle Scholar
AL-Quraan, N.A., Locy, R.D. and Singh, N.K. (2010) Expression of calmodulin genes in wild type and calmodulin mutants of Arabidopsis thaliana under heat stress. Plant Physiology and Biochemistry 48, 697–702.CrossRefGoogle ScholarPubMed
AL-Quraan, N.A., Sartawe, F.A.B. and Qaryouti, M.M. (2013) Characterization of γ-aminobutyric acid metabolism and oxidative damage in wheat (Triticum aestivum L.) seedlings under salt and osmotic stress. Journal of Plant Physiology 170, 1003–1009.CrossRefGoogle ScholarPubMed
AL-Quraan, N., Ghunaim, A. and Alkhatib, R. (2015) The influence of chlorsulfuron herbicide on GABA metabolism and oxidative damage in lentil (Lens culinaris Medik) and wheat (Triticum aestivum L.) seedlings. Acta Physiologia Plantarum 37, 227.CrossRefGoogle Scholar
Asada, K. (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.CrossRefGoogle Scholar
Astegno, A., Capitani, G. and Dominici, P. (2015) Functional roles of the hexamer organization of plant glutamate decarboxylase. Biochimica et Biophysica Acta 1854, 1229–1237.CrossRefGoogle ScholarPubMed
Bergmeyer, H.U. (1983) Methods of Enzymatic Analysis (2nd edn), volume I, 427. New York and London: Academic Press.Google Scholar
Bor, M., Seckin, B., Ozgur, R., Yılmaz, O., Ozdemir, F. and Turkan, I. (2009) Comparative effects of drought, salt, heavy metal and heat stresses on gamma aminobutryric acid abundances of sesame (Sesamum indicum L.). Acta Physiologia Plantarum 31, 655–659.CrossRefGoogle Scholar
Bown, A.W. and Shelp, B.J. (2016) Plant GABA: not just a metabolite. Trends in Plant Science 21, 811–813.CrossRefGoogle ScholarPubMed
Bown, A.W., MacGregor, K.B. and Shelp, B.J. (2006) Gamma-aminobutyrate: defense against invertebrate pests? Trends in Plant Science 11, 424–427.CrossRefGoogle ScholarPubMed
Carillo, P. (2018) GABA shunt in durum wheat. Frontiers in Plant Science 9, 100.CrossRefGoogle ScholarPubMed
Chandra, R., Bhargava, R.N., Yadav, S. and Mohan, D. (2009) Accumulation and distribution of toxic metals in Wheat (Triticum aestivum L.) and Indian mustard (Brassica compestries L.) irrigated with distillery and tannery effluent. Journal of Hazardous Materials 162, 1514–1521.CrossRefGoogle Scholar
Cheeseman, J.M. (2015) The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. New Phytologist 206, 557–570.CrossRefGoogle ScholarPubMed
Che-Othman, M.H., Jacoby, R.P., Millar, A.H. and Taylor, N.L. (2019) Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytologist. doi: 10.1111/nph.15713Google ScholarPubMed
Cramer, G., Ergül, A., Grimplet, J., Tillett, R., Tattersall, E., Bohlman, M., Vincent, D., Sonderegger, J., Evans, J., Osborne, C., Quilici, D., Schlauch, K., Schooley, D. and Cushman, J. (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Functional & Integrative Genomics 7, 111–134.CrossRefGoogle ScholarPubMed
Dodd, G.L. and Donovan, L.A. (1999) Water potential and ionic effects on germination and seedling growth of two cold desert shrubs. American Journal of Botany 86, 1146–1153.CrossRefGoogle ScholarPubMed
Fait, A., Fromm, H., Walter, D., Galili, G. and Fernie, A.R. (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13, 14–19.CrossRefGoogle ScholarPubMed
Fait, A., Nesi, A., Angelovici, R., Lehmann, M., Pham, P., Song, L., Haslam, R.P., Napier, J.A., Galili, G. and Fernie, A.R. (2011) Targeted enhancement of glutamate-to-γ-aminobutyrate conversion in Arabidopsis seeds affects carbon-nitrogen balance and storage reserves in a development-dependent manner. Plant Physiology 157, 1026–1042.CrossRefGoogle Scholar
Grieve, C.M. and Suarez, D.L. (1997) Purslane (Portulaca oleracea L.): a halophytic crop for drainage water reuse systems. Plant and Soil 192, 277–283.CrossRefGoogle Scholar
Hadi, S.M.S., Ahmed, M.Z., Hameed, A., Khan, M.A. and Gul, B. (2018) Seed germination and seedling growth responses of toothbrush tree (Salvadora persica L.) to different interacting abiotic stresses. Flora 243, 45–52.CrossRefGoogle Scholar
Hampson, C.R. and Simpson, G.M. (1990) Effects of temperature, salt, and osmotic potential on early growth of wheat (Triticum aestivum L.). I. Germination. Canadian Journal of Botany 68, 524–528.CrossRefGoogle Scholar
Hasegawa, P.M., Bressan, R.A., Zhu, J.K. and Bohnert, H.J. (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.CrossRefGoogle ScholarPubMed
Ibrahim, E.A. (2016) Seed priming to alleviate salinity stress in germinating seeds. Journal of Plant Physiology 192, 38–46.CrossRefGoogle ScholarPubMed
Jain, M., Tiwary, S. and Gadre, R. (2010) Sorbitol-induced changes in various growth and biochemical parameters in maize. Plant, Soil and Environment 56, 263–267.CrossRefGoogle Scholar
Kinnersley, A.M. and Turano, F.J. (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Reviews in Plant Sciences 19, 479–509.CrossRefGoogle Scholar
Krasensky, J. and Jonak, C. (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany 63, 1593–1608.CrossRefGoogle ScholarPubMed
Marín-Vinader, L., Van Genesen, S.T. and Lubsen, N.H. (2006) mRNA made during heat shock enters the first round of translation. Biochimica et Biophysica Acta 1759, 535–542.CrossRefGoogle Scholar
Mayer, R., Cherry, J. and Rhodes, D. (1990). Effects of heat shock on amino acid metabolism of cowpea cells. Plant Physiology 94, 796–810.CrossRefGoogle ScholarPubMed
Mazzucotelli, E., Tartari, A., Cattivelli, L. and Forlani, G. (2006) Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. Journal of Experimental Botany 57, 3755–3766.CrossRefGoogle ScholarPubMed
Miransari, M. and Smith, D. L. (2014) Plant hormones and seed germination. Environmental and Experimental Botany 99, 110–121.CrossRefGoogle Scholar
Moghadam, A.A., Ebrahimie, E., Taghavi, S.M., Niazi, A. and Djavaheri, M. (2012) Isolation and in silico functional analysis of MtATP6, a 6-kDa subunit of mitochondrial F1F0-ATP synthase, in response to abiotic stress. Genetics and Molecular Research 11, 3547–3567.CrossRefGoogle ScholarPubMed
Molina-Rueda, J. J., Garrido-Aranda, A. and Gallardo, F. (2015) Glutamate decarboxylase, in D'Mello, J.P.F. (ed), Amino Acids in Higher Plants. Wallingford: CABI.Google Scholar
Molina-Rueda, J., Pascual, M., Cánovas, F. and Gallardo, F. (2010) Characterization and developmental expression of a glutamate decarboxylase from maritime pine. Planta 232, 1471–1483.CrossRefGoogle ScholarPubMed
Munns, R. (2002) Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239–250.CrossRefGoogle ScholarPubMed
Nagajyoti, P.C., Lee, K.D. and Sreekanth, T.V.M. (2010) Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters 8, 199–216.CrossRefGoogle Scholar
Noiraud, N., Maurousset, L. and Lemonie, R. (2001) Transport of polyols in higher plants. Plant Physiology and Biochemistry 39, 717–728.CrossRefGoogle Scholar
Parvaiz, A. and Satyavati, S. (2008) Salt stress and phyto-biochemical responses of plants-a review. Plant, Soil and Environment 54, 89–99.CrossRefGoogle Scholar
Pascual, M., Molina-Rueda, J., Cánovas, F. and Gallardo, F. (2008) Spatial distribution of cytosolic NADP+-isocitrate dehydrogenase in pine embryo and seedlings. Tree Physiology 28, 1773–1782.CrossRefGoogle ScholarPubMed
Ramagopal, S. (1990) Inhibition of seed germination by salt and its subsequent effect on embryonic protein synthesis in barley. Journal of Plant Physiology 136, 621–625.CrossRefGoogle Scholar
Ramden, H.A., Niemi, S.A. and Hadathi, Y.K.A. (1986) Salinity and seed germination of corn and soyabean. Iraqi Journal of Agricultural Science 4, 97–102.Google Scholar
Renault, H., El Amrani, A., Berger, A., Mouille, G., Soubigou-Taconnat, L., Bouchereau, A. and 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 and Environment 36, 1009–1018.CrossRefGoogle ScholarPubMed
Renault, H., Roussel, V., El Amrani, A., Arzel, M., Renault, D., Bouchereau, A. and Deleu, C. (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biology 10, 20.CrossRefGoogle ScholarPubMed
Romo, J.T. and Haferkamp, M.R. (1987) Effects of osmotic potential, potassium chloride, and sodium chloride on germination of greasewood (Sarcobatus vermiculatus). The Great Basin Naturalist 47, 110–116.Google Scholar
Scholz, S., Malabarba, J., Reichelt, M., Heyer, M., Ludewig, F. and Mithöfer, A. (2017) Evidence for GABA-induced systemic GABA accumulation in Arabidopsis upon wounding. Frontiers in Plant Science 8, 388.CrossRefGoogle ScholarPubMed
Seppanen, M.M., Cardi, T., Hyokki, M.B. and Pehu, E. (2000) Characterization and expression of cold-induced gluathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. Plant Science 153, 125–133.CrossRefGoogle Scholar
Shelp, B.J., Bozzo, G.G., Trobacher, C.P., Zarei, A., Deyman, K.L. and Brikis, C.J. (2012) Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Science 193–194, 130–135.CrossRefGoogle ScholarPubMed
Shelp, B.J., Walton, C.S., Snedden, W.A., Tuin, L.G., Oresnik, I.J. and Layzell, D.B. (1995) GABA shunt in developing soybean seed is associated with hypoxia. Physiologia Plantarum 94, 219–228.CrossRefGoogle Scholar
Shelp, B., Bown, A. and McLean, M. (1999) Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Sciences 4, 446–452.CrossRefGoogle ScholarPubMed
Uquillas, C., Letelier, I., Blanco, F., Jordana, X. and Holuigue, L. (2004) NPR1-independent activation of immediate early salicylic acid responsive genes in Arabidopsis. Molecular Plant-Microbe Interaction 17, 34–42.CrossRefGoogle ScholarPubMed
Veer, P. and Sharma, Y.K. (2010) Impact of osmotic stress on seed germination and seedling growth in black gram (Phaseolus mungo). Journal of Environmental Biology 31, 721–726.Google Scholar
Vicuña, S., Garreaud, R. and McPhee, J. (2011) Climate change impacts on the hydrology of a snowmelt driven basin in semiarid Chile. Climate Change 105, 469–488.CrossRefGoogle Scholar
Wang, W., Vinocur, B. and Altman, A. (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14.CrossRefGoogle ScholarPubMed
Wang, Y., Gu, W., Meng, Y., Xie, T., Li, L., Li, J. and Wei, S. (2017) γ-Aminobutyric acid imparts partial protection from salt stress injury to maize seedlings by improving photosynthesis and upregulating osmo-protectants and antioxidants. Scientific Reports 7, 43609.CrossRefGoogle Scholar
Woodrow, P., Ciarmiello, L., Annunziata, M., Pacifico, S., Iannuzzi, F., Mirto, A., D'Amelia, L., Dell'Aversana, E., Piccolella, S., Fuggi, A. and Carillo, P. (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiologia Plantarum 159, 290–312.CrossRefGoogle ScholarPubMed
Xing, S., Jun, Y., Hau, Z. and Liang, L. (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiology and Biochemistry 45, 560–566.CrossRefGoogle ScholarPubMed
Xu, H., Liao, P., Xiao, J., Zhang, Q., Dong, Y. and Kai, G. (2010) Molecular cloning and characterization of glutamate decarboxylase cDNA from the giant-embryo Oryza sativa. Archives of Biological Sciences 62, 873–879.CrossRefGoogle Scholar
Zammani, B.M., Niazi, A., Moghadam, A.A., Deihimi, T. and Ebrahimie, E. (2013) Genome wide analysis of key salinity-tolerance transporter (HKT1;5) in wheat and wild wheat relatives (A and D genomes). In Vitro Cellular & Developmental Biology – Plant 49, 97–106.CrossRefGoogle Scholar
Zhang, G. and Bown, A.W. (1997). The rapid determination of gamma-aminobutyric acid. Phytochemistry 44, 1007–1009.CrossRefGoogle Scholar
Zhang, H., Irving, L.J., McGill, C., Matthew, C., Zhou, D. and Kemp, P. (2010). The effects of salinity and osmotic stress on barley germination rate: sodium as an osmotic regulator. Annals of Botany 106, 1027–1035.CrossRefGoogle ScholarPubMed
Zhao, T.J., Sun, S., Liu, Y., Liu, J.M., Liu, Q., Yan, Y.B. and Zhou, H.M. (2006). Regulating the drought-responsive element (DRE)-mediated signaling pathway by synergic functions of trans-active and trans-inactive DRE binding factors in Brassica napus. Journal of Biological Chemistry 281, 10752–10759.CrossRefGoogle ScholarPubMed