Abstract
High-temperature stress induces cellular changes leading to over-production of highly reactive oxygen species (ROS) which damage macromolecules and cell organelles, eventually resulting in cell death. Antioxidative metabolism in plants comprising of enzymatic and non-enzymatic antioxidants imparts tolerance by scavenging or detoxification of excess ROS. We investigated the response of major H2O2-detoxifying system, the AsA–GSH cycle in four genotypes of maize differing in heat sensitivity. Stress was imposed by staggered sowing so that one set of plants faced high-temperature stress at their anthesis-silking stage. The concentrations of H2O2 increased across the genotypes by high temperature; however, the increase was lesser in tolerant genotypes: NSJ 189 and NSJ 221. High-temperature stress led to an increase in the level of GSH and GSSG in all the genotypes, whereas GSH/GSSG decreased in sensitive genotypes: PSRJ 13099 and RJR 270. The glutathione S-transferase activity increased significantly under heat stress. APX, MDHAR and DHAR activities decreased under heat stress in the sensitive group. Under high temperature, GR activity remained unchanged in sensitive genotypes, while it increased significantly in tolerant genotypes. Ascorbate levels increased in tolerant genotypes, while a decline was observed in sensitive genotypes. Isoforms of APX showed some new bands in tolerant genotypes as well as higher intensity of the existing ones as compared to sensitive genotypes under stress conditions. Isoforms of GR did not show any genotypic differences under heat stress. Findings emphasized the importance and complexity of the AsA–GSH system in fine-tuning the redox metabolism under heat stress in maize. The study also suggested that the antioxidative enzymes of AsA–GSH cycle play a key role in sustaining the ROS homeostasis in cells, thus minimizing the potential toxic effects of ROS.
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References
Ahmad P, Prasad MNV (2012) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York
Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85:235–241
Asada K (1994) Production of active oxygen species in photosynthetic tissue. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 77–101
Balla K, Bencze S, Janda T, Veisz O (2009) Analysis of heat stress tolerance in winter wheat. Acta Agron Hung 57:437–444
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273
Bradford MM (1976) Arapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cetinkaya H, Tasci F, SeckinDinler B (2014) Regulation of glutathione S-transferase enzyme activity with salt pre-treatment under heat stress in maize leaves. Res Plant Biol 4:45–56
Dai AH, Nie YX, Yu B, Li Q, Lu LY, Bai JG (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10
Dixon DP, Skipsey M, Edwards R (2010) Roles of glutathione transferase in plant secondary metabolism. Phytochemistry 71:338–350
Eltayeb AE, Kawano N, Badawi G, Kaminaka H, Sanekata T, Morishia I (2006) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant 127:57–65
Eltayeb AE, Kawano N, Badawi G, Kaminaka H, Sanekata T, Shibahar T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Plants 225:1255–1264
Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:8–96
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Hall AE (1992) Breeding for heat tolerance. Plant Breed Rev 10:129–168
Hasnuzzaman M, Fujita M (2011) Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol Trace Elem Res 143:1758–1776
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
Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in ascorbate-deficient Arabidopsis mutant. J Exp Bot 56:3041–3049
Kocsy G, Szalai G, Galiba G (2002) Effect of heat stress on glutathione biosynthesis in wheat. Acta Biol Szeged 46:71–72
Kong W, Huang C, Chen Q, Zou Y, Zhang J (2011) Nitric oxide alleviates heat stress-induced oxidative damage in Pleurotuseryngii var. tuoliensis. Fungal Genet Biol 49:15–20
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophase T4. Nature 227:680–685
Ma YH, Ma FW, Zhang JK, Li MJ, Wang YH, Liang D (2008) Effects of high temperature on activities and gene expression of enzymes involved in ascorbate–glutathione cycle in apple leaves. Plant Sci 175:761–766
Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao ZC (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York, pp 749–845
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate dependent reduction of nitroblue tetrazolium. Anal Biochem 212:540–546
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279
Pastori GM, Trippi VS (1992) Oxidative stress induces high rate of glutathione reductase synthesis in a drought resistant maize strain. Plant Cell Physiol 33:957–961
Polidoros AN, Scandalios JG (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106:112–120
Prasad PVV, Bheemanhalli R, Jagadish SVK (2017) Field crops and the fear of heat stress-Opportunities, challenges and future directions. Field Crops Res 200:114–121
Rao MV, Paliyath G, Ormrod DP (1996) UV-B- and ozone induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136
Rivero RM, Ruiz JM, Romero L (2004) Oxidative metabolism in tomato plants subjected to heat stress. J Hortic Sci Biotechnol 79:560–564
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319
Singh AK, Singhal GS (2001) Effect of irradiance on the thermal stability of thylakoid membrane isolated from acclimated wheat leaves. Photosynthetica 39:23–27
Stark G (2005) Functional consequences of oxidative membrane damage. J Memb Biol 205:1–16
Tiroli-Cepeda AO, Ramos CHI (2010) Heat causes oligomeric disassembly and increases the chaperone activity of small heat shock proteins from sugarcane. Plant Physiol Biochem 48:108–116
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223
Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285
Yadav SK, Tiwari YK, Darala PK, Shanker AK, Jyothi Lakshmi N, Vanaja M, Maheswari M (2015) Genotypic variation in physiological traits under high temperature stress in maize. Agric Res 5:119–126
Yadav SK, Tiwari YK, Singh V, Patil AA, Shanker AK, Jyothi Lakshmi N, Vanaja M, Maheswari M (2016) Physiological and biochemical basis of extended and sudden heat stress tolerance in maize. Proc Natl Acad Sci India Sect B Biol Sci 88:249–263
Yin H, Chen QM, Yi MF (2008) Effects of short-term heat stress on oxidative damage and responses of antioxidant system in Liliumlongiflorum. Plant Growth Regul 54:45–54
Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963
Acknowledgements
Authors gratefully acknowledge the financial support provided by National Innovations on Climate Resilient Agriculture (NICRA) implemented by Indian Council of Agriculture Research (ICAR), New Delhi. Authors are also thankful to the Director, NBPGR, New Delhi, for providing maize germplasm.
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Tiwari, Y.K., Yadav, S.K. Effect of High-Temperature Stress on Ascorbate–Glutathione Cycle in Maize. Agric Res 9, 179–187 (2020). https://doi.org/10.1007/s40003-019-00421-x
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DOI: https://doi.org/10.1007/s40003-019-00421-x