Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 199–215 | Cite as

Role of Exogenous Glutathione in Alleviating Abiotic Stress in Maize (Zea mays L.)

  • Laming Pei
  • Ronghui Che
  • Linlin He
  • Xingxing Gao
  • Weijun Li
  • Hui LiEmail author


The role of exogenous GSH in improving abiotic stress tolerance in maize was investigated in this study. GSH-treated plants showed significantly higher germination percentage, survival rate, plant biomass, and grain yield per plant than control plants. The possible physiological mechanism underlying the tolerance phenotypes in GSH-treated plants were also analyzed in this study. GSH-treated plants showed reduced oxidative destruction, enhanced water retention, and increased activity of antioxidant enzyme, vacuolar H+-pyrophosphatase (V-H+-PPase), and H+-adenosine triphosphatase (V-H+-ATPase), compared to control plants. In addition, the accumulation of abscisic acid (ABA) and the expression of ABA-responsive genes were upregulated by GSH treatment. These results suggested that GSH played a role in relieving oxidative destruction, maintaining plant water content, and promoting higher ABA levels, which were responsible for GSH-enhanced tolerance to abiotic stresses in maize.


Maize Glutathione (GSH) Abiotic stress Yield ABA accumulation 



This work was supported by the National Natural Science Foundation of China (31771797, 31401388) and by the Natural Science Foundation of Shandong Province (ZR2017BC099).

Compliance with Ethical Standards

Conflict of interest

The authors have declared that no competing interests exist.

Supplementary material

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Supplementary material 1 (DOC 58 KB)
344_2018_9832_MOESM2_ESM.docx (364 kb)
Supplementary material 2 (DOCX 363 KB)
344_2018_9832_MOESM3_ESM.docx (19 kb)
Supplementary material 3 (DOCX 19 KB)


  1. Alia, Kondo Y, Sakamoto A, Nonaka H, Hayashi H, Saradhi PP, Chen Tony HH, Murata N (1999) Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol Biol 40:279–288CrossRefGoogle Scholar
  2. Baisak R, Rana D, Acharya BB, Kar M (1994) Alterations in the activities of active oxygen scavenging enzymes of wheat leaves subjected to water stress. Plant Cell Physiol 35:489–495Google Scholar
  3. Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 50::375–383CrossRefGoogle Scholar
  4. Bashandy T, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391CrossRefGoogle Scholar
  5. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  6. Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455CrossRefGoogle Scholar
  7. Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351CrossRefGoogle Scholar
  8. Cheng MC, Ko K, Chang WL, Kuo WC, Chen GH, Lin TP (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939CrossRefGoogle Scholar
  9. Cooper CE, Patel RP, Brookes PS, Darley Usmar VM (2002) Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem Sci 27:489–492CrossRefGoogle Scholar
  10. Dabbous A, Saad RB, Brini F, Farhat-Khemekhem A, Zorrig W, Abdely C, Hamed KB (2017) Over-expression of a subunit E1 of a vacuolar H+-ATPase gene (Lm VHA-E1) cloned from the halophyte Lobularia maritima improves the tolerance of Arabidopsis thaliana to salt and osmotic stresses. Environ Exp Bot 137:128–141CrossRefGoogle Scholar
  11. Dat JF, Foyer CH, Scott IM (1998) Changes in salicylic acid and antioxidants during induced thermo tolerance in mustard seedlings. Plant Physiol 118:1455–1461CrossRefGoogle Scholar
  12. De Michelis MI, Spanswick RM (1986) H-pumping driven by the vanadate-sensitive ATPase in membrane vesicles from corn roots. Plant Physiol 81:542–547CrossRefGoogle Scholar
  13. Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198CrossRefGoogle Scholar
  14. Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase Dα retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9:2183–2196Google Scholar
  15. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875CrossRefGoogle Scholar
  16. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18CrossRefGoogle Scholar
  17. Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109:1047–1057CrossRefGoogle Scholar
  18. Frottin F, Espagne C, Traverso JA, Mauve C, Valot B, Lelarge-Trouverie C, Zivy M, Noctor G, Meinnel T, Giglione C (2009) Cotranslational proteolysis dominates glutathione homeostasis to support proper growth and development. Plant Cell 21:3296–3314CrossRefGoogle Scholar
  19. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-Pump. Proc Natl Acad Sci USA 98:11444–11449CrossRefGoogle Scholar
  20. Giannopolitis CN, Ries SK (1977) Superoxide dismutase: I. occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  21. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  22. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212CrossRefGoogle Scholar
  23. Jia J, Fu J, Zheng J, Zhou X, Huai J, Wang J, Wang M, Zhang Y, Chen X, Zhang J (2006) Annotation and expression profile analysis of 2073 full length cDNAs from stress-induced maize (Zea mays L.) seedlings. Plant J 48:710–727CrossRefGoogle Scholar
  24. Kattab H (2007) Role of glutathione and polyadenylic acid on the oxidative defense systems of two different cultivars of canola seedlings grown under saline condition. Aust J Basic Appl Sci 1:323–334Google Scholar
  25. Kim MJ, Shin R, Schachtman DP (2009) A nuclear factor regulates abscisic acid responses in Arabidopsis. Plant Physiol 151:1433–1445CrossRefGoogle Scholar
  26. Kingston-Smith AH, Harbinson J, Foyer CH (1999) Acclimation of photosynthesis, H2O2 content and antioxidants in maize (Zea mays) grown at sub-optimal temperatures. Plant Cell Environ 22:1071–1083CrossRefGoogle Scholar
  27. Kocsy G, Ballmoos PV, Suter M, Rüegsegger A, Galli U, Szalai G, Galiba G, Brunold C (2000a) Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211:528–538CrossRefGoogle Scholar
  28. Kocsy G, Szalai G, Vágújfalvi A, Stéhli L, Orosz G, Galiba G (2000b) Genetic study of glutathione accumulation during cold hardening in wheat. Planta 210:295–301CrossRefGoogle Scholar
  29. Kocsy G, Ballmoos PV, Rüegsegger A, Szalai G, Galiba G, Brunold C (2001) Increasing the glutathione content in a chilling-sensitive maize genotype using safeners increased protection against chilling-induced injury. Plant Physiol 127:1147–1156CrossRefGoogle Scholar
  30. Kocsy G, Szalai G, Galiba G (2002) Induction of glutathione synthesis and glutathione reductase activity by abiotic stresses in maize and wheat. Sci World J 2:1699–1707CrossRefGoogle Scholar
  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  32. Lv S, Yang A, Zhang K, Wang L, Zhang J (2007) Increase of glycine betaine synthesis improves drought tolerance in cotton. Mol Breed 20:233–248CrossRefGoogle Scholar
  33. Maehly AC, Chance B (1954) Catalases and peroxidases, part II. Methods Biochem Anal 1:357–424Google Scholar
  34. Marrs KA, Walbot V (1997) Expression and RNA splicing of the maize glutathione S-transferase bronze2 gene is regulated by cadmium and other stresses. Plant Physiol 113:93–102CrossRefGoogle Scholar
  35. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54CrossRefGoogle Scholar
  36. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  37. Nieto-Sotelo J, Ho TH (1986) Effect of heat shock on the metabolism of glutathione in maize roots. Plant Physiol 82:1031–1035CrossRefGoogle Scholar
  38. Noctor G, Gomez L, Vanacker H, Foyer Ch (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283CrossRefGoogle Scholar
  39. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquezgarcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484CrossRefGoogle Scholar
  40. Ohara K, Kokado Y, Yamamoto H, Sato F, Yazaki K (2004) Engineering of ubiquinone biosynthesis using the yeast coq2 gene confers oxidative stress tolerance in transgenic tobacco. Plant J 40:734–743CrossRefGoogle Scholar
  41. Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci USA 102:18830–18835CrossRefGoogle Scholar
  42. Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012CrossRefGoogle Scholar
  43. Peever TL, Higgins VJ (1989) Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from cladosporium fulvum. Plant Physiol 90:867–875CrossRefGoogle Scholar
  44. Pei L, Jin Z, Li K, Yin H, Wang J, Yang A (2013) Identification and comparative analysis of low phosphate tolerance-associated microRNAs in two maize genotypes. Plant Physiol Biochem 70:221–234CrossRefGoogle Scholar
  45. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212CrossRefGoogle Scholar
  46. Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicators. Crop Sci 28:526–531CrossRefGoogle Scholar
  47. Singh V, Pallaghy CK, Singh D (2006) Phosphorus nutrition and tolerance of cotton to water stress. II. Water relations, free and bound water and leaf expansion rate. Field Crops Res 96:199–206CrossRefGoogle Scholar
  48. Smart LB, Vojdani F, Maeshima M, Wilkins TA (1998) Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiol 116:1539–1549CrossRefGoogle Scholar
  49. Taiz L (1992) The plant vacuole. J Exp Biol 172:113–122Google Scholar
  50. Tan BC, Schwartz SH, Zeevaart JA, Mccarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240CrossRefGoogle Scholar
  51. Thompson AJ, Andrews J, Mulholland BJ, Mckee JM, Hilton HW, Horridge JS, Farquhar GD, Smeeton RC, Smillie IR, Black CR (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143:1905–1917CrossRefGoogle Scholar
  52. Vanderauwera S, Block MD, Steene NV, Cotte BV, Metzlaff M, Breusegem FV (2007) Silencing of poly (ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 104:15150–15155CrossRefGoogle Scholar
  53. Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Montagu MV, Inzé D, May MJ, Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–109CrossRefGoogle Scholar
  54. Virlouvet L, Jacquemot MP, Gerentes D, Corti H, Bouton S, Gilard F, Valot B, Trouverie J, Tcherkez G, Falque M (2011) The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol 157:917–936CrossRefGoogle Scholar
  55. Wellburn FA, Creissen AG, Lake BJ, Mullineaux CP, Wellburn BA (1998) Tolerance to atmospheric ozone in transgenic tobacco over expressing glutathione synthetase in plastids. Physiol Plant 104:623–629CrossRefGoogle Scholar
  56. Yao L, Li Y, Zhang J, Xiao Y, Yue Y, Duan L, Zhang M, Li Z (2013) Overexpression of Arabidopsis molybdenum cofactor sulfurase gene confers drought tolerance in maize (Zea mays L.). PLoS ONE 8:e52126CrossRefGoogle Scholar
  57. Ying S, Zhang DF, Li HY, Liu YH, Shi YS, Song YC, Wang TY, Li Y (2011) Cloning and characterization of a maize SnRK2 protein kinase gene confers enhanced salt tolerance in transgenic Arabidopsis. Plant Cell Rep 30:1683–1699CrossRefGoogle Scholar
  58. Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151CrossRefGoogle Scholar
  59. Zechmann B, Koffler BE, Russell SD (2011) Glutathione synthesis is essential for pollen germination in vitro. BMC Plant Biol 11:1–11CrossRefGoogle Scholar
  60. Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378CrossRefGoogle Scholar
  61. Zheng J, Zhao J, Tao Y, Wang J, Liu Y, Fu J, Jin Y, Gao P, Zhang J, Bai Y (2004) Isolation and analysis of water stress induced genes in maize seedlings by subtractive PCR and cDNA macroarray. Plant Mol Biol 55:807–823CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological and Science TechnologyUniversity of JinanJinanChina

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