Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effect of drought stress on wheat (Triticum durum) growth and metabolism: insight from GABA shunt, reactive oxygen species and dehydrin genes expression

Nisreen A. AL-Quraan https://orcid.org/0000-0001-7328-054X A * , Nezar H. Samarah https://orcid.org/0000-0002-2820-3382 B and Ayah A. Tanash A
+ Author Affiliations
- Author Affiliations

A Department of Biotechnology and Genetic Engineering, Faculty of Science and Arts, Jordan University of Science and Technology, Irbid 22110, Jordan.

B Department of Plant Production, Faculty of Agriculture, Jordan University of Science and Technology, Irbid 22110, Jordan.

* Correspondence to: naquraan@just.edu.jo

Handling Editor: Muhammad Waseem

Functional Plant Biology 51, FP22177 https://doi.org/10.1071/FP22177
Submitted: 10 August 2022  Accepted: 18 October 2022  Published: 8 November 2022

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Activation of γ-aminobutyric acid (GABA) shunt pathway and upregulation of dehydrins are involved in metabolic homeostasis and protective mechanisms against drought stress. Seed germination percentage, seedling growth, levels of GABA, alanine, glutamate, malondialdehyde (MDA), and the expression of glutamate decarboxylase (GAD) and dehydrin (dhn and wcor) genes were examined in post-germination and seedlings of four durum wheat (Triticum durum L.) cultivars in response to water holding capacity levels (80%, 50%, and 20%). Data showed a significant decrease in seed germination percentage, seedling length, fresh and dry weight, and water content as water holding capacity level was decreased. Levels of GABA, alanine, glutamate, and MDA were significantly increased with a negative correlation in post-germination and seedling stages as water holding capacity level was decreased. Prolonged exposure to drought stress increased the GAD expression that activated GABA shunt pathway especially at seedlings growth stage to maintain carbon/nitrogen balance, amino acids and carbohydrates metabolism, and plant growth regulation under drought stress. The mRNA transcripts of dhn and wcor significantly increased as water availability decreased in all wheat cultivars during the post-germination stage presumably to enhance plant tolerance to drought stress by cell membrane protection, cryoprotection of enzymes, and prevention of reactive oxygen species (ROS) accumulation. This study showed that the four durum wheat cultivars responded differently to drought stress especially during the seedling growth stage which might be connected with ROS scavenging systems and the activation of antioxidant enzymes that were associated with activation of GABA shunt pathway and the production of GABA in durum seedlings.

Keywords: dhn, drought, durum wheat, GABA, GAD, metabolism, seed germination, seedlings growth, wcor.

References

Abid M, Ali S, Qi LK, Zahoor R, Tian Z, Jiang D, Snider JL, Dai T (2018) Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Scientific Reports 8, 4615.
| Crossref | Google Scholar |

Abu-Zaitoun SY, Chandrasekhar K, Assili S, Shtaya MJ, Jamous RM, Mallah OB, Nashef K, Sela H, Distelfeld A, Alhajaj N, Ali-Shtayeh MS, Peleg Z, Ben-David R (2018) Unlocking the genetic diversity within a Middle-East panel of durum wheat landraces for adaptation to semi-arid climate. Agronomy 8(10), 233.
| Crossref | Google Scholar |

Aghdam MS, Razavi F, Karamneghad F (2016) Maintaining the postharvest nutritional quality of peach fruits by γ-Aminobutyric acid. Iranian Journal of Plant Physiology 5, 1457-1463.
| Google Scholar |

Ahmad Z, Waraich EA, Akhtar S, Anjum S, Ahmad T, Mahboob W, Hafeez OBA, Tapera T, Labuschagne M, Rizwan M (2018) Physiological responses of wheat to drought stress and its mitigation approaches. Acta Physiologiae Plantarum 40, 80.
| Crossref | Google Scholar |

Al-Ghzawi ALA, Khalaf YB, Al-Ajlouni ZI, AL-Quraan NA, Musallam I, Hani NB (2018) The effect of supplemental irrigation on canopy temperature depression, chlorophyll content, and water use efficiency in three wheat (Triticum aestivum L. and T. durum Desf.) varieties grown in dry regions of Jordan. Agriculture 8(5), 67.
| Crossref | Google Scholar |

Allagulova CR, Gimalov FR, Shakirova FM, Vakhitov VA (2003) The plant dehydrins: structure and putative functions. Biochemistry (Moscow) 68, 945-951.
| Crossref | Google Scholar |

Almaghrabi OA (2012) Impact of drought stress on germination and seedling growth parameters of some wheat cultivars. Life Science Journal 9, 590-598.
| Google Scholar |

Alqarawi AA, Hashem A, Abd_Allah EF, Al-Huqail AA, Alshahrani TS, Alshalawi SR, Egamberdieva D (2016) Protective role of gamma amminobutyric acid on Cassia italica Mill under salt stress. Legume Research-An International Journal 39, 396-404 10.18805/lr.v0iOF.9561.
| 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 Biosystems-An International Journal Dealing with all Aspects of Plant Biology 151, 148-157.
| Crossref | Google Scholar |

AL-Quraan NA, Locy RD, Singh NK (2010) Expression of calmodulin genes in wild type and calmodulin mutants of Arabidopsis thaliana under heat stress. Plant Physiology and Biochemistry 48, 697-702.
| Crossref | Google Scholar |

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 Biotechnology Reports 5, 225-234.
| Crossref | Google Scholar |

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. Journal of Plant Physiology 170, 1003-1009.
| Crossref | 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 Horticulturae 1054, 47-54.
| Crossref | Google Scholar |

AL-Quraan NA, AL-Ajlouni ZI, Obedat DI (2019) The GABA shunt pathway in germinating seeds of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) under salt stress. Seed Science Research 29, 250-260.
| Crossref | Google Scholar |

Amar SB, Safi H, Ayadi M, Azaza J, Khoudi H, Masmoudi K, Brini F (2013) Analysis of the promoter activity of a wheat dehydrin gene (DHN-5) under various stress conditions. Australian Journal of Crop Science 7, 1875-1883.
| Google Scholar |

Barbosa JM, Singh NK, Cherry JH, Locy RD (2010) Nitrate uptake and utilization is modulated by exogenous γ-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiology and Biochemistry 48, 443-450.
| Crossref | Google Scholar |

Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell & Environment 31, 11-38.
| Crossref | Google Scholar |

Bartoli CG, Gómez F, Martínez DE, Guiamet JJ (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). Journal of Experimental Botany 55, 1663-1669.
| Crossref | Google Scholar |

Bartyzel I, Pelczar K, Paszkowski A (2003) Functioning of the γ-aminobutyrate pathway in wheat seedlings affected by osmotic stress. Biologia Plantarum 46, 221-225.
| Crossref | Google Scholar |

Bashir R, Riaz HN, Shafiq M, Parveen N, Alenazi MM, Anwar S, Alebidi AI (2019) Foliar application of Y-aminobutyric acid (GABA) improves vegetative growth, and the physiological and antioxidative potential of Daucus Carota L. under water deficit conditions. Preprints 2019, 2019030227.
| Crossref | Google Scholar |

Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. The EMBO Journal 15, 2988-2996.
| Crossref | Google Scholar |

Bergmeyer HU, Bergmeyer J, Grassl M (1983) ‘Methods of enzymatic analysis. Vol. 2, Samples, reagents, assessment of results.’ 3rd edn. (Verlag Chemie: Weinheim)

Bismillah Khan M, Hussain M, Raza A, Farooq S, Jabran K (2015) Seed priming with CaCl2 and ridge planting for improved drought resistance in maize. Turkish Journal of Agriculture and Forestry 39, 193-203.
| Crossref | Google Scholar |

Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends in Plant Science 9, 110-115.
| Crossref | Google Scholar |

Bouché N, Fait A, Zik M, Fromm H (2004) The root-specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis. Plant Molecular Biology 55, 315-325.
| Crossref | Google Scholar |

Brini F, Saibi W, Amara I, Gargouri A, Masmoudi K, Hanin M (2010) Wheat dehydrin DHN-5 exerts a heat-protective effect on β-glucosidase and glucose oxidase activities. Bioscience, Biotechnology, and Biochemistry 74, 1050-1054.
| Crossref | Google Scholar |

Carillo P (2018) GABA shunt in durum wheat. Frontiers in Plant Science 9, 100.
| Crossref | Google Scholar |

Carrasco-Ríos L, Pinto M (2014) Effect of salt stress on antioxidant enzymes and lipid peroxidation in leaves in two contrasting corn, ‘Lluteno’ and ‘Jubilee’. Chilean Journal of Agricultural Research 74, 89-95.
| Crossref | Google Scholar |

Carvalho P, Azam-Ali S, Foulkes MJ (2014) Quantifying relationships between rooting traits and water uptake under drought in Mediterranean barley and durum wheat. Journal of Integrative Plant Biology 56(5), 455-469.
| Crossref | Google Scholar |

Chang H, Chen D, Kam J, Richardson T, Drenth J, Guo X, McIntyre CL, Chai S, Rae AL, Xue G-P (2016) Abiotic stress upregulated TaZFP34 represses the expression of type-B response regulator and SHY2 genes and enhances root to shoot ratio in wheat. Plant Science 252, 88-102.
| Crossref | Google Scholar |

Chen X, Min D, Yasir TA, Hu Y-G (2012) Evaluation of 14 morphological, yield-related and physiological traits as indicators of drought tolerance in Chinese winter bread wheat revealed by analysis of the membership function value of drought tolerance (MFVD). Field Crops Research 137, 195-201.
| Crossref | 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. International Journal of Molecular Sciences 19, 2520.
| Crossref | Google Scholar |

Che-Othman MH, Jacoby RP, Millar AH, Taylor NL (2020) Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytologist 225, 1166-1180.
| Crossref | Google Scholar |

Chugh V, Kaur N, Gupta AK (2011) Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Indian Journal of Biochemistry & Biophysics 48, 47-53.
| Google Scholar |

Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture – not by affecting ATP synthesis. Trends in Plant Science 5, 187-188.
| Crossref | Google Scholar |

Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. The Plant Cell 10, 623-638.
| Crossref | Google Scholar |

Deng X-F, Fu F-L, Ni N, Li W-C (2009) Differential gene expression in response to drought stress in maize seedling. Agricultural Sciences in China 8, 767-776.
| Crossref | Google Scholar |

Dhanda SS, Sethi GS, Behl RK (2004) Indices of drought tolerance in wheat genotypes at early stages of plant growth. Journal of Agronomy and Crop Science 190, 6-12.
| Crossref | Google Scholar |

Drira M, Saibi W, Brini F, Gargouri A, Masmoudi K, Hanin M (2013) The K-segments of the wheat dehydrin DHN-5 are essential for the protection of lactate dehydrogenase and β-glucosidase activities in vitro. Molecular Biotechnology 54, 643-650.
| Crossref | Google Scholar |

El-Kereamy A, Bi Y-M, Ranathunge 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, e52030.
| Crossref | Google Scholar |

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. Frontiers in Plant Science 8, 1147.
| Crossref | Google Scholar |

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In ‘Sustainable agriculture’. (Eds E Lichtfouse, M Navarrete, P Debaeke, S Véronique, C Alberola) pp. 153–188. (Springer)

Fathi A, Tari DB (2016) Effect of drought stress and its mechanism in plants. International Journal of Life Sciences 10, 1-6.
| Crossref | Google Scholar |

Fowler DB, Breton G, Limin AE, Mahfoozi S, Sarhan F (2001) Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiology 127, 1676-1681.
| Crossref | Google Scholar |

Fromm H, Snedden WA (1997) Role of Ca2+/calmodulin in plant response to abiotic stresses: a review. Acta Horticulturae 447, 431-438.
| Crossref | Google Scholar |

Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environmental and Experimental Botany 45, 105-114.
| Crossref | Google Scholar |

Ganeva G, Korzun V, Landjeva S, Popova Z, Christov NK (2010) Genetic diversity assessment of Bulgarian durum wheat (Triticum durum Desf.) landraces and modern cultivars using microsatellite markers. Genetic Resources and Crop Evolution 57, 273-285.
| Crossref | Google Scholar |

Garg AK, Kim J-K, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences 99, 15898-15903.
| Crossref | Google Scholar |

Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant Journal 16, 433-442.
| Crossref | Google Scholar |

Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochemical Journal 388, 151-157.
| Crossref | Google Scholar |

Güler NS, Terzi R (2020) Dehydrins: an overview of current approaches and advancement. Turkish Journal of Botany 44, 481-492.
| Crossref | Google Scholar |

Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signaling & Behavior 6, 1503-1509.
| Crossref | Google Scholar |

Harb AM, Lahham JN (2013) Response of three accessions of Jordanian Aegilops crassa Boiss. and durum wheat to controlled drought. Jordan Journal of Biological Sciences 6(2), 151-158.
| Crossref | Google Scholar |

Hassan NM, El-Bastawisy ZM, El-Sayed AK, Ebeed HT, Nemat Alla MM (2015) Roles of dehydrin genes in wheat tolerance to drought stress. Journal of Advanced Research 6, 179-188.
| Crossref | Google Scholar |

Hsiao TC, Xu L-K (2000) Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. Journal of Experimental Botany 51, 1595-1616.
| Crossref | Google Scholar |

Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S, Wang L (2018) Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Frontiers in Plant Science 9, 393.
| Crossref | Google Scholar |

Jain D, Chattopadhyay D (2010) Analysis of gene expression in response to water deficit of chickpea (Cicer arietinum L.) varieties differing in drought tolerance. BMC Plant Biology 10, 24-14.
| Crossref | Google Scholar |

Jaleel CA, Gopi R, Sankar B, Gomathinayagam M, Panneerselvam R (2008) Differential responses in water use efficiency in two varieties of Catharanthus roseus under drought stress. Comptes Rendus Biologies 331, 42-47.
| Crossref | Google Scholar |

Jiang J, Zhuang J-Y, Fan Y-Y, Shen B (2009) Mapping of QTLs for leaf malondialdehyde content associated with stress tolerance in rice. Rice Science 16, 72-74.
| Crossref | Google Scholar |

Kavas M, Baloğlu MC, Akca O, Köse FS, Gökçay D (2013) Effect of drought stress on oxidative damage and antioxidant enzyme activity in melon seedlings. Turkish Journal of Biology 37, 491-498.
| Crossref | Google Scholar |

Kim SK, Son TK, Park SY, Lee IJ, Lee BH, Kim HY, Lee SC (2006) Influences of gibberellin and auxin on endogenous plant hormone and starch mobilization during rice seed germination under salt stress. Journal of Environmental Biology 27, 181-186.
| Google Scholar |

Kumar M, Lee S-C, Kim J-Y, Kim S-J, Aye SS, Kim S-R (2014) Over-expression of dehydrin gene, OsDhn1, improves drought and salt stress tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Journal of Plant Biology 57, 383-393.
| Crossref | Google Scholar |

Kumar N, Dubey AK, Upadhyay AK, Gautam A, Ranjan R, Srikishna S, Sahu N, Behera SK, Mallick S (2017a) GABA accretion reduces Lsi-1 and Lsi-2 gene expressions and modulates physiological responses in Oryza sativa to provide tolerance towards arsenic. Scientific Reports 7, 8786.
| Crossref | Google Scholar |

Kumar S, Beena AS, Awana M, Singh A (2017b) Physiological, biochemical, epigenetic and molecular analyses of wheat (Triticum aestivum) genotypes with contrasting salt tolerance. Frontiers in Plant Science 8, 1151.
| Crossref | Google Scholar |

Landi S, Hausman J-F, Guerriero G, Esposito S (2017) Poaceae vs. abiotic stress: focus on drought and salt stress, recent insights and perspectives. Frontiers in Plant Science 8, 1214.
| Crossref | Google Scholar |

Lee S-J, Kang J-Y, Park H-J, Kim MD, Bae MS, Choi H-I, Kim SY (2010) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiology 153, 716-727.
| Crossref | Google Scholar |

Li Z, Peng Y, Zhang X-Q, Ma X, Huang L-K, Yan Y-H (2014) Exogenous spermidine improves seed germination of white clover under water stress via involvement in starch metabolism, antioxidant defenses and relevant gene expression. Molecules 19, 18003-18024.
| Crossref | Google Scholar |

Li MF, Guo SJ, Yang XH, Meng QW, Wei XJ (2016) Exogenous gamma-aminobutyric acid increases salt tolerance of wheat by improving photosynthesis and enhancing activities of antioxidant enzymes. Biologia Plantarum 60, 123-131.
| Crossref | 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. Journal of Plant Growth Regulation 36, 436-449.
| Crossref | 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 creeping bentgrass (Agrostis stolonifera). International Journal of Molecular Sciences 19, 1623.
| Crossref | Google Scholar |

Lindsey BE, III, Rivero L, Calhoun CS, Grotewold E, Brkljacic J (2017) Standardized method for high-throughput sterilization of Arabidopsis seeds. Journal of Visualized Experiments: JoVE e56587.
| Crossref | Google Scholar |

Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 1391-1406.
| Crossref | Google Scholar |

Liu Q, Zhao N, Yamaguch-Shinozaki K, Shinozaki K (2000) Regulatory role of DREB transcription factors in plant drought, salt and cold tolerance. Chinese Science Bulletin 45, 970-975.
| Crossref | Google Scholar |

Liu Y, Xu H, Wen X-X, Liao Y-C (2016) Effect of polyamine on seed germination of wheat under drought stress is related to changes in hormones and carbohydrates. Journal of Integrative Agriculture 15, 2759-2774.
| Crossref | Google Scholar |

Lv A, Su L, Liu X, Xing Q, Huang B, An Y, Zhou P (2018) Characterization of Dehydrin protein, CdDHN4-L and CdDHN4-S, and their differential protective roles against abiotic stress in vitro. BMC Plant Biology 18, 299.
| Crossref | Google Scholar |

Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Archives of Biochemistry and Biophysics 444, 139-158.
| Crossref | Google Scholar |

Mahmud JAL, 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.
| Crossref | Google Scholar |

Manfre AJ, Lanni LM, Marcotte WR, Jr. (2006) The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development. Plant Physiology 140, 140-149.
| Crossref | Google Scholar |

Manickavelu A, Nadarajan N, Ganesh SK, Gnanamalar RP, Chandra Babu R (2006) Drought tolerance in rice: morphological and molecular genetic consideration. Plant Growth Regulation 50, 121-138.
| Crossref | 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, e0212411.
| Crossref | 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. Journal of Experimental Botany 57, 3755-3766.
| Crossref | Google Scholar |

Mekonnen DW, Flügge U-I, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Science 245, 25-34.
| Crossref | Google Scholar |

Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Frontiers in Plant Science 6, 419.
| Crossref | Google Scholar |

Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248, 565-577.
| Crossref | Google Scholar |

Molina-Rueda JJ, Pascual MB, Cánovas FM, Gallardo F (2010) Characterization and developmental expression of a glutamate decarboxylase from maritime pine. Planta 232, 1471-1483.
| Crossref | Google Scholar |

Muhammad K (2010) Performance of wheat genotypes under osmotic stress at germination and early seedling growth stage. Caderno de Pesquisa Serie Biologia 22, 5-12.
| Google Scholar |

Mustroph A, Barding GA, Jr, Kaiser KA, Larive CK, Bailey-Serres J (2014) Characterization of distinct root and shoot responses to low-oxygen stress in Arabidopsis with a focus on primary C- and N-metabolism. Plant, Cell & Environment 37, 2366-2380.
| Crossref | Google Scholar |

Passioura JB (2002) Soil conditions and plant growth. Plant, Cell & Environment 25, 311-318.
| Crossref | Google Scholar |

Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47, 493-500.
| Crossref | Google Scholar |

Pirdashti H, Sarvestani ZT, Nematzadeh GH, Ismail A (2003) Effect of water stress on seed germination and seedling growth of rice (Oryza sativa L.) genotypes. Journal of Agronomy 2, 217-222.
| Crossref | Google Scholar |

Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicology and Environmental Safety 104, 202-208.
| Crossref | Google Scholar |

Rajashekar CB (2000) Cold response and freezing tolerance in plants. In ‘Plant-environment interactions’. (Ed. RE Wilkinson) pp. 321–341. (Marcel Dekker)

Ramos-Ruiz R, Poirot E, Flores-Mosquera M (2018) GABA, a non-protein amino acid ubiquitous in food matrices. Cogent Food & Agriculture 4, 1534323.
| Crossref | Google Scholar |

Ramos-Ruiz R, Martinez F, Knauf-Beiter G (2019) The effects of GABA in plants. Cogent Food & Agriculture 5, 1670553.
| Crossref | Google Scholar |

Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biology 10, 20.
| Crossref | Google Scholar |

Rorat T (2006) Plant dehydrins – tissue location, structure and function. Cellular and Molecular Biology Letters 11, 536-556.
| Crossref | Google Scholar |

Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Science 160, 869-875.
| Crossref | Google Scholar |

Sairam RK, Chandrasekhar V, Srivastava GC (2001) Comparison of hexaploid and tetraploid wheat cultivars in their responses to water stress. Biologia Plantarum 44, 89-94.
| Crossref | Google Scholar |

Sallam A, Alqudah AM, Dawood MFA, Baenziger PS, Börner A (2019) Drought stress tolerance in wheat and barley: advances in physiology, breeding and genetics research. International Journal of Molecular Sciences 20, 3137.
| Crossref | Google Scholar |

Samarah NH (2005) Effects of drought stress on growth and yield of barley. Agronomy for Sustainable Development 25, 145-149.
| Crossref | Google Scholar |

Samarah NH, Mullen RE, Cianzio SR, Scott P (2006) Dehydrin-like proteins in soybean seeds in response to drought stress during seed filling. Crop Science 46, 2141-2150.
| Crossref | Google Scholar |

Scholz SS, Reichelt M, Mekonnen DW, Ludewig F, Mithöfer A (2015) Insect herbivory-elicited GABA accumulation in plants is a wound-induced, direct, systemic, and jasmonate-independent defense response. Frontiers in Plant Science 6, 1128.
| Crossref | Google Scholar |

Schuppler U, He P-H, John PCL, Munns R (1998) Effect of water stress on cell division and Cdc2-like cell cycle kinase activity in wheat leaves. Plant Physiology 117, 667-678.
| Crossref | Google Scholar |

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 Science 161, 1135-1144.
| Crossref | Google Scholar |

Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012, 217037.
| Crossref | Google Scholar |

Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science 4, 446-452.
| Crossref | Google Scholar |

Shelp BJ, Bozzo GG, Trobacher CP, Chiu G, Bajwa VS (2012a) Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. I. Pathway structure. Botany 90, 651-668.
| Crossref | Google Scholar |

Shelp BJ, Mullen RT, Waller JC (2012b) Compartmentation of GABA metabolism raises intriguing questions. Trends in Plant Science 17, 57-59.
| Crossref | Google Scholar |

Shewry PR (2009) Increasing the health benefits of wheat. The FEBS Journal 276, 71.
| Google Scholar |

Shi S-Q, Shi Z, Jiang Z-P, Qi L-W, Sun X-M, Li C-X, Liu J-F, Xiao W-F, Zhang S-G (2010) Effects of exogenous GABA on gene expression of Caragana intermedia roots under NaCl stress: regulatory roles for H2O2 and ethylene production. Plant, Cell & Environment 33, 149-162.
| Crossref | Google Scholar |

Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology 3, 217-223.
| Crossref | Google Scholar |

Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221-227.
| Crossref | Google Scholar |

Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) AnArabidopsisgene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochemical and Biophysical Research Communications 250, 161-170.
| Crossref | Google Scholar |

Siddique MRB, Hamid A, Islam MS (2000) Drought stress effects on water relations of wheat. Botanical Bulletin of Academia Sinica 41, 35-39.
| Google Scholar |

Sita K, Kumar V (2020) Role of Gamma Amino Butyric Acid (GABA) against abiotic stress tolerance in legumes: a review. Plant Physiology Reports 25, 654-663.
| Crossref | Google Scholar |

Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho T-HD, Qu R (2000) Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Science 155, 1-9.
| Crossref | Google Scholar |

Snedden WA, Chung I, Pauls RH, Bown AW (1992) Proton/L-glutamate symport and the regulation of intracellular pH in isolated mesophyll cells. Plant Physiology 99, 665-671.
| Crossref | Google Scholar |

Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regulation 64, 1-16.
| Crossref | Google Scholar |

Sultan MARF, Hui L, Yang LJ, Xian ZH (2012) Assessment of drought tolerance of some Triticum L. species through physiological indices. Czech Journal of Genetics and Plant Breeding 48, 178-184.
| Crossref | Google Scholar |

Tatar O, Gevrek MN (2008) Influence of water stress on proline accumulation, lipid peroxidation and water content of wheat. Asian Journal of Plant Sciences 7, 409-412.
| Crossref | Google Scholar |

Wahid A, Close TJ (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biologia Plantarum 51, 104-109.
| Crossref | Google Scholar |

Wahid A, Rasul E, Rao R, Iqbal R (2005) Photosynthesis in leaf, stem, flower and fruit. In ‘Handbook of photosynthesis.’ 2nd edn. (Ed. M Pessarakli) pp. 479–497. (CRC Press)

Xi J, Qiu Y, Du L, Poovaiah BW (2012) Plant-specific trihelix transcription factor AtGT2L interacts with calcium/calmodulin and responds to cold and salt stresses. Plant Science 185–186, 274-280.
| Crossref | Google Scholar |

Yamaguchi-Shinozaki K (2002) Biological mechanisms of drought stress response. JIRCAS Work Rep 23, 1-8.
| Google Scholar |

Yang Y, Han C, Liu Q, Lin B, Wang J (2008) Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiologiae Plantarum 30, 433-440.
| Crossref | Google Scholar |

Yong B, Xie H, Li Z, Li Y-P, Zhang Y, Nie G, Zhang X-Q, Ma X, Huang L-K, Yan Y-H, Peng Y (2017) Exogenous application of GABA improves PEG-induced drought tolerance positively associated with GABA-shunt, polyamines, and proline metabolism in white clover. Frontiers in Physiology 8, 1107.
| Crossref | Google Scholar |

Youssef S, Riad G, Abu El-Azm NAI, Ahmed E (2018) Amending sandy soil with biochar or/and superabsorbent polymer mitigates the adverse effects of drought stress on green pea. Egyptian Journal of Horticulture 45, 169-183.
| Crossref | Google Scholar |

Yu Z, Wang X, Zhang L (2018) Structural and functional dynamics of dehydrins: a plant protector protein under abiotic stress. International Journal of Molecular Sciences 19, 3420.
| Crossref | Google Scholar |

Zeeshan M, Lu M, Sehar S, Holford P, Wu F (2020) Comparison of biochemical, anatomical, morphological, and physiological responses to salinity stress in wheat and barley genotypes deferring in salinity tolerance. Agronomy 10, 127.
| Crossref | Google Scholar |

Zhang G, Bown AW (1997) The rapid determination of γ-aminobutyric acid. Phytochemistry 44, 1007-1009.
| Crossref | Google Scholar |

Zheng M, Tao Y, Hussain S, Jiang Q, Peng S, Huang J, Cui K, Nie L (2016) Seed priming in dry direct-seeded rice: consequences for emergence, seedling growth and associated metabolic events under drought stress. Plant Growth Regulation 78, 167-178.
| Crossref | Google Scholar |

Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynthesis Research 117, 529-546.
| Crossref | Google Scholar |