Transgenic Plants for Higher Antioxidant Content and Drought Stress Tolerance

  • Chandrama Prakash UpadhyayaEmail author
  • Mohammad Anwar Hossain


Climate change is a major global concern that can make agriculture even more risk-prone, especially in the developing world. Environmental stresses caused by climate change, such as drought, high salinity, low and high temperatures are predicted to become more severe and widespread. One of the most acute environmental stresses presently affecting agriculture is drought, which has pronounced adverse effects on the growth and development of crop plants. The effects of drought stress are expected to increase further with increases in climate change and a growing water crisis. Drought stress usually leads to reductions in crop yield, which can result from many drought-induced morphological, physiological, and metabolic changes that occur in plants. A key sign of drought stress at the molecular level is the accelerated production of reactive oxygen species (ROS) such as singlet oxygen (1O2), superoxide (O 2 ), hydrogen peroxide (H2O2), and hydroxyl radicals ( OH). The excess production of ROS is common in many abiotic stresses, including drought stress, and results from impaired electron transport processes in the chloroplasts and mitochondria. One of the major causes of ROS production under drought stress is photorespiration, which accounts for more than 70 % of the total H2O2 produced. Plants have endogenous mechanisms for adapting to ROS production and are thought to respond to drought stress by strengthening these defense mechanisms. Therefore, enhancement of the functions of the naturally occurring antioxidant components (enzymatic and nonenzymatic) may be one strategy for reducing or preventing oxidative damage and improving the drought resistance of plants. In this chapter, we review the most recent reports on drought-induced responses in plants, focusing on the role of oxidative stress as well as on other possible mechanisms and examining how different components of the antioxidant defense system may confer tolerance to drought-induced oxidative stress. Transgenic approaches are one of the many tools available for modern crop improvement programs. Gene discovery and functional genomics projects have revealed multitudinous mechanisms and gene families that confer improved productivity and adaptation to drought stresses. The overall aim of genetically improving crops for drought resistance is to develop plants able to obtain water and use it to produce sufficient yields for human needs under drought conditions. Although advances have been made in developing crops that are genetically improved with traits such as herbicide and pesticide resistance, attempts to improve plant drought resistance have been hindered by the complexity of plant drought resistance mechanisms at the whole plant, cellular, metabolic, and genetic levels. Interactions between these mechanisms and the complex nature of drought itself adds another layer of intricacy to this problem. The transgenic plants developed via transformation of several different genes that leads to enhanced antioxidant content and consequently their role in the drought stress tolerance are taken into account.


Transgenic plants Drought stress Reactive oxygen species Antioxidants 



We wish to thank Dr. Deepak Kumar, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India for providing several supporting articles and suggestions for improving the chapter. We are also highly thankful to Dr. Ram Prasad, Amity University, Uttar Pradesh, India for critical reading of the chapter.


  1. 1.
    Achary VMM, Parinandi NL, Panda BB (2012) Aluminum induces oxidative burst, cell wall NADH peroxidase activity, and DNA damage in root cells of Allium cepa L. Environ Mol Mutagen 53:550–560PubMedCrossRefGoogle Scholar
  2. 2.
    Acquaah G (2007) Principles of plant genetics and breeding. Blackwell, OxfordGoogle Scholar
  3. 3.
    Adam AL, Bestwick CS, Barna B, Mansfield JW (1995) Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola. Planta 197:240–249CrossRefGoogle Scholar
  4. 4.
    Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173CrossRefGoogle Scholar
  5. 5.
    Alia P, Saradhi P (1991) Proline accumulation under heavy metal stress. J Plant Physiol 138:554–558CrossRefGoogle Scholar
  6. 6.
    Ali AA, Alqurainy F (2006) Activities of antioxidants in plants under environmental stress. In: Motohashi N (ed) The lutein-prevention and treatment for diseases. Transworld Research Network, India, pp 187–256Google Scholar
  7. 7.
    Alscher RG, Hess JL (1993) Antioxidants in higher plants. CRC Press, Boca Raton, FLGoogle Scholar
  8. 8.
    Alscher RG, Erturk N, Heatrh LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefGoogle Scholar
  9. 9.
    Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784PubMedCrossRefGoogle Scholar
  10. 10.
    Apel K, Hirt H (2004) Reactive oxygen species metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  11. 11.
    Arasimowicz-Jelonek M, Floryszak- Wieczorek J, Kubis J (2009) Involvement of nitric oxide in water stressinduced responses of cucumber roots. Plant Sci 177:682–690CrossRefGoogle Scholar
  12. 12.
    Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In Kyle DJ et al. (eds) Photoinhibition. Elsevier, pp 227–287Google Scholar
  13. 13.
    Asada K (1994) Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton FL, p. 77–104Google Scholar
  14. 14.
    Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefGoogle Scholar
  15. 15.
    Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93PubMedCrossRefGoogle Scholar
  17. 17.
    Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Env Exp Bot 59:206–216CrossRefGoogle Scholar
  18. 18.
    Athar HR, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Env Exp Bot. 63:224–231CrossRefGoogle Scholar
  19. 19.
    Azpilicueta CE, Benavides MP, Tomaro ML, Gallego SM (2007) Mechanism of CATA3 induction by cadmium in sunflower leaves. Plant Physiol Biochem. 45:589–595Google Scholar
  20. 20.
    Baek KH, Skinner DZ (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Sci 165(6):1221–1227Google Scholar
  21. 21.
    Bai J, Xu DH, Kang HM, Chen K, Wang G (2008) Photoprotective function of photorespiration in Kreaumuria soongorica during different levels of drought stress in natural high irradiance. Photosynthetica 46:232–237CrossRefGoogle Scholar
  22. 22.
    Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928CrossRefGoogle Scholar
  23. 23.
    Bowler M, Montagu V, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116Google Scholar
  24. 24.
    Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33:299–321PubMedCrossRefGoogle Scholar
  25. 25.
    Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montald 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
  26. 26.
    Bhattachrjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plant. Curr Sci 89:1113–1121Google Scholar
  27. 27.
    Biehler K, Fock H (1996) Evidence for the contribution of the Mehler peroxidase reaction in dissipating excess electrons in drought stressed wheat. Plant Physiol 112:265–272PubMedPubMedCentralGoogle Scholar
  28. 28.
    Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Bolwell GP (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47:851–863PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Boo YC, Jung J (1999) Water deficit-induced oxidative stress and antioxidative defenses in rice plants. J Plant Physiol 155:255–261CrossRefGoogle Scholar
  30. 30.
    Buhler DR, Cristobal M (2000) Antioxidant activities of flavonoids.
  31. 31.
    Briviba K, Klotz LO, Sies H (1997) Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. J Biol Chem 378:1259–1265Google Scholar
  32. 32.
    Bunkelmann JR, Trelease RN (1995) Molecular cloning and characterization of ascorbate peroxidase localized to the glyoxysome membranes of cotton cotyledons. Plant Physiol 108:8–67Google Scholar
  33. 33.
    Ceccarelli S, Grando S, Maatougui M, Michael M, Slash M, Haghparast R, Rahmanian M, Taheri A, Al-Yassin A, Benbelkacem A, Labdi M, Mimoun H, Nachit M (2010) Plant breeding and climate changes. J Agric Sci 148:1–11CrossRefGoogle Scholar
  34. 34.
    Cela J, Chang C, Munné-Bosch S (2011) Accumulation of γ- rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52:1389–1400PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Chalapathi Rao ASV, Reddy AR (2008) Glutathione reductase: a putative redox regulatory system in plant cells. In: Khan NA, Singh S, Umar S (eds) Sulfur assimilation and abiotic stresses in plants. Springer, The Netherlands, pp 111–147Google Scholar
  36. 36.
    Cheeseman JM (2007) Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 1:4–15Google Scholar
  37. 37.
    Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Olletotrichum trifolii. PNAS 102:3459–3464PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Contour-Ansel D, Torres-Franklin ML, De Carvalho MHC, D’arcy-Lameta A, Zuily-Fodil Y (2006) Glutathione reductase in leaves of cowpea: cloning of two cDNAs, expression and enzymatic activity under progressive drought stress, desiccation and abscisic acid treatment. Ann Bot 98:1279–1287PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Creissen GP, Broadbent P, Kular B, Reynolds H, Wellburn AR, Mullineaux PM (1994) Manipulation of glutathione reductase in transgenic plants: implications for plant responses to environmental stress. Proc R Soc Edin B 102:167–175Google Scholar
  40. 40.
    Creissen G, Firmin J, Fryer M, Kular B, Leyland N, Reynolds H, Pastori G, Wellburn F, Baker N, Wellburn A, Mullineaux P (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 12:1277–1291CrossRefGoogle Scholar
  41. 41.
    Dai A-H, Nie Y-X, Yu B, Li Q, Lu L-Y, Bai J-G (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10CrossRefGoogle Scholar
  42. 42.
    Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795PubMedCrossRefGoogle Scholar
  43. 43.
    de Carvalho MCH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165CrossRefGoogle Scholar
  44. 44.
    del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272PubMedCrossRefGoogle Scholar
  45. 45.
    del Río LA, Sandalio LM, Altomare DA, Zilinskas BA (2003) Mitochondrial and peroxisomal magnese superoxide dismutase: differential expression during leaf senescence. J Exp Bot 54:923–933PubMedCrossRefGoogle Scholar
  46. 46.
    del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    DelLongo OT, Gonzalez CA, Pastori GM, Trippi VS (1993) Antioxidant defences under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028Google Scholar
  48. 48.
    Desikin R, A-H-Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptosome by oxidative stress. Plant Physiol 127:159–172CrossRefGoogle Scholar
  49. 49.
    Desel C, Hubbermann EM, Schwarz K, Krupinska K (2007) Nitration of g-tocopherol in plant tissues. Planta 226:1311–1322PubMedCrossRefGoogle Scholar
  50. 50.
    Ding S, Lu Q, Zhang Y, Yang Z, Wen X, Zhang L, Lu C (2009) Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol Biol 69:577–592PubMedCrossRefGoogle Scholar
  51. 51.
    Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. doi: 10.1016/j.phytochem.2009.12.012
  52. 52.
    Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037PubMedPubMedCentralGoogle Scholar
  53. 53.
    Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284PubMedCrossRefGoogle Scholar
  54. 54.
    Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Morishima I, Shibahara T, Inanaga S, Tanaka K (2006) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant 127:57–65CrossRefGoogle Scholar
  55. 55.
    Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225(5):1255–1264PubMedCrossRefGoogle Scholar
  56. 56.
    Eltayeb AE, Yamamoto S, Habora MEE, Yin L, Tsujimoto H, Tanaka K (2011) Transgenic potato overexpressing Arabidopsis cytosolic AtDHAR1 showed higher tolerance to herbicide, drought and salt stresses. Breed Sci 61:3–10CrossRefGoogle Scholar
  57. 57.
    Espinoza A, Martín AS, López-Climent M, Ruiz-Lara S, Gómez-Cadenas A, Casaretto JA (2013) Engineered drought-induced biosynthesis of α-tocopherol alleviates stress-induced leaf damage in tobacco. J Plant Physiol 170:1285–1294PubMedCrossRefGoogle Scholar
  58. 58.
    Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62:2599–2613PubMedCrossRefGoogle Scholar
  59. 59.
    Fischer EM, Schfar C (2010) Consistent geographical patterns of changes in high impact European heatwaves. Nat Geosci 3:398–403CrossRefGoogle Scholar
  60. 60.
    Ferreira RR, Fornazier RF, Vitoria AP, Lea PJ, Azevedo RA (2002) Changes in antioxidant enzyme activities in soybean under cadmium stress. J Plant Nutr 25:327–342CrossRefGoogle Scholar
  61. 61.
    Filippou P, Antoniou C, Fotopoulos V (2011) Effect of drought and rewatering on the cellular status and antioxidant response of Medicago truncatula plants. Plant Signal Behav 6:270–277PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK (2008) Altered stomatal dynamics in ascorbate oxidase over–expressing tobacco plants suggest a role for dehydroascorbate signalling. J Exp Bot 59:729–737PubMedCrossRefGoogle Scholar
  63. 63.
    Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25PubMedCrossRefGoogle Scholar
  64. 64.
    Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388Google Scholar
  65. 65.
    Foyer CH (2001) Prospects for enhancement the soluble antioxidants ascorbate and glutathione. Biofactors 15:75–78PubMedCrossRefGoogle Scholar
  66. 66.
    Foyer CH, Noctor G (2005) Redox homeostis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Gaber A, Yoshimura K, Yamamoto T, Yabuta Y, Takeda T, Miyasaka H, Nakano Y, Shigeoka S (2006) Glutathione peroxidase-like protein of synechocystis PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis. Physiol Plant 128:251–262CrossRefGoogle Scholar
  68. 68.
    Galle A, Csiszar J, Secenji M, Tari I, Gyorgyey D, Erdei L (2005) Changes of glutathione Stransferase activities and gene expression in Triticum aestivum during polyethylene-glycol induced osmotic stress. Acta Biol Szeged 49:95–96Google Scholar
  69. 69.
    Gao D, Gao Q, Xu HY, Ma F, Zhao CM, Liu JQ (2009) Physiological responses to gradual drought stress in the diploid hybrid Pinus densata and its two parental species. Trees 23:717–728CrossRefGoogle Scholar
  70. 70.
    Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141:341–345PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosys 143:8–96CrossRefGoogle Scholar
  72. 72.
    George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318PubMedCrossRefGoogle Scholar
  73. 73.
    Gichner T, Patkova Z, Szakova J, Demnerova K (2004) Cadmium induces DNA damages in tobacco roots, but no DNA damage, somatic mutations or homologous recombinations in tobacco leaves. Mutat Res Genet Toxicol Environ Mut 559:49–57CrossRefGoogle Scholar
  74. 74.
    Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  75. 75.
    Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  76. 76.
    Guo Z, OuW LuS, Zhong Q (2006) Differential response of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836PubMedCrossRefGoogle Scholar
  77. 77.
    Gururani MA, Upadhyaya CP, Strasser RJ, Woong YJ, Park SW (2012) Physiological and biochemical responses of transgenic potato plants with altered expression of PSII manganese stabilizing protein. Plant Physiol Biochem 58:182–194PubMedCrossRefGoogle Scholar
  78. 78.
    Haber F, Weiss J (1994) The catalytic decomposition of hydrogen peroxide by iron salts. Proc R Soc Lond A 147:332–351CrossRefGoogle Scholar
  79. 79.
    Haluskova L, Valentovicova K, Huttova J, Mistrik I, Tamas L (2009) Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tips. Plant Physiol Biochem 47:1069–1074PubMedCrossRefGoogle Scholar
  80. 80.
    Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  82. 82.
    Harding SA, Oh SH, Roberts DM (1997) Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species. EMBO J 16:1137–1144PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Hasanuzzaman M, Fujita M, Islam MN, Ahamed KU, Nahar K (2009) Performance of four irrigated rice varieties under different levels of salinity stress. Int J Integr Biol 6:85–90Google Scholar
  84. 84.
    Hasanuzzaman M, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am. J. Plant Physiol. 5:295–324CrossRefGoogle Scholar
  85. 85.
    Hasanuzzaman 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 143:1758–1776PubMedCrossRefGoogle Scholar
  86. 86.
    Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365CrossRefGoogle Scholar
  87. 87.
    Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2012) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323Google Scholar
  88. 88.
    Hasanuzzaman M, Gill SS, Fujita M (2013) Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 269–322CrossRefGoogle Scholar
  89. 89.
    Hasanuzzaman M, Nahar K, Gill SS, Fujita M (2014) Drought stress responses in plants, oxidative stress and antioxidant defense. In: Gill SS, Tuteja N (eds) Climate change and plant abiotic stress tolerance. Wiley, Weinheim, pp 209–249Google Scholar
  90. 90.
    Hemavathi, Upadhyaya CP, Young KE, Akula N, Kim HS, Heung JJ, Oh MH, Reddy AC, Chun SC, Kim DH, Park SW (2009) Over-expression of strawberry D-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance. Plant Sci 177:659–667CrossRefGoogle Scholar
  91. 91.
    Hemavathi, Upadhyaya CP, Young KE, Akula N, Chun SC, Kim DH, Park SW (2010) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol Lett 32:321–330PubMedCrossRefGoogle Scholar
  92. 92.
    Hemavathi, Upadhyaya CP, Akula N, Kim HS, Jeon JH, Oh MH, Chun SC, Kim DH, Park SW (2011) Biochemical analysis of enhanced tolerance in transgenic potato plants overexpressing d-galacturonicacidreductase gene in response to various abiotic stresses. Mol Breed 28:105–115CrossRefGoogle Scholar
  93. 93.
    Hollander-Czytko H, Grabowski J, Sandorf I, Weckermann K, Weiler EW (2005) Tocopherol content and activities of tyrosine aminotransferase and cysteine lyase in Arabidopsis under stress conditions. J Plant Physiol 162:767–770PubMedCrossRefGoogle Scholar
  94. 94.
    Hoque MA, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defence and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165:813–824Google Scholar
  95. 95.
    Hossain MA, Hoque MA, Burritt DJ, Fujita M (2013) Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Ahmad P (ed) Oxidative damage to plants. Elsevier, USA, pp 477–522Google Scholar
  96. 96.
    Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide-priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420Google Scholar
  97. 97.
    Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in an ascorbate–deficient Arabidopsis mutant. J Exp Bot 56:3041–3049PubMedCrossRefGoogle Scholar
  98. 98.
    Hutchinson F (1957) The distance that a radical formed by ionizing radiation can diffuse in a yeast cell. Radiat Res 7:473–483PubMedCrossRefGoogle Scholar
  99. 99.
    IPCC (2009) Observations: surface and atmospheric climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averty KB, Tignor M, Miller HL (eds) Climate change 2009: 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 (chapter 3)Google Scholar
  100. 100.
    Jimenez A, Hernandez JA, Del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284Google Scholar
  101. 101.
    Jimenez A, Hernandez JA, Pastori G, del Rio LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Jing X, Xiao JX, Yong ST, Ri HP, Yong X, Wei Z, Quan HY (2015) Transgenic arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS One. doi: 10.1371/journal.pone.0136960 Google Scholar
  103. 103.
    Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8:1865–1879PubMedCrossRefGoogle Scholar
  104. 104.
    Jubany-Marí T, Munné-Bosch S, López-Carbonell M, Alegre L (2009) Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot 60:107–120PubMedCrossRefGoogle Scholar
  105. 105.
    Kamal-Eldin A, Appelqvist LA (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701PubMedCrossRefGoogle Scholar
  106. 106.
    Kingston-Smith AH, Foyer CH (2000) Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures. J Exp Bot 51:123–130PubMedCrossRefGoogle Scholar
  107. 107.
    Kim YH, Kim CY, Song WK, Park DS, Kwon SY, Lee HS, Bang JW, Kwak SS (2008) Overexpression of sweetpotato swpa4 peroxidase results in increased hydrogen peroxide production and enhances stress tolerance in tobacco. Planta 227:867–881PubMedCrossRefGoogle Scholar
  108. 108.
    Kliebenstein DJ, Dietrich RA, Martin AC, Last RL, Dangl JL (1999) Salicylic acid regulates induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol Plant-Microbe Interac 12:1022–1026CrossRefGoogle Scholar
  109. 109.
    Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiol Plant 34:75–86CrossRefGoogle Scholar
  111. 111.
    Kumar S, Kaur R, Kaur N, Bhandhari K, Kaushal N, Gupta K, Bains T, Nayyar H (2011) Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiol Plant 33:2091–2101CrossRefGoogle Scholar
  112. 112.
    Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2013) Modulation of antioxidant machinery in α-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma. doi: 10.1007/s00709-013-0484-0 Google Scholar
  113. 113.
    Larson RA (1988) The antioxidants of higher plants. Phytochemistry 27:969–978CrossRefGoogle Scholar
  114. 114.
    Lata C, Yadav A, Prasad M (2011) Role of plant transcription factors in abiotic stress tolerance. In: Shanker A (ed) Physiological, biochemical and genetic perspectives. In-Tech, Shanghai.
  115. 115.
    Lee H, Jo J (2004) Increased tolerance to methyl viologen by transgenic tobacco plants that overexpress the cytosolic glutathione reductase gene from Brassica campestris. J Plant Biol 47:111–116CrossRefGoogle Scholar
  116. 116.
    Le Martret B, Poage M, Shiel K, Nugent GD, Dix PJ (2011) Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered antioxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J 9:661–673PubMedCrossRefGoogle Scholar
  117. 117.
    Lei Y, Yin C, Li C (2006) Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus prezwalskii. Physiol Plant 127:187–191CrossRefGoogle Scholar
  118. 118.
    Leshem YY, Kuiper PJC (1996) Is there a gas (general adaptation syndrome) response to various types of environmental stress? Biol Plant 38:1–18CrossRefGoogle Scholar
  119. 119.
    Li CH, Li Y, Wuyun TN, Wu GL, Jiang GM (2010) Effects of high concentration ozone on soybean growth and grain yield. Ying Yong Sheng Tai Xue Bao 21:2347–2352PubMedGoogle Scholar
  120. 120.
    Li CH, Li Y, Wuyun TN, Wu GL, Jiang GM (2010) Effects of high concentration ozone on soybean growth and grain yield. Ying Yong Sheng Tai Xue Bao 21:2347–2352PubMedGoogle Scholar
  121. 121.
    Lindahl M, Yang DH, Andersson B (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by light-induced membrane associated enzymic system. Eur J Biochem 213:503–509CrossRefGoogle Scholar
  122. 122.
    Liu X, Hua X, Guo J, Qi D, Wang L, Liu Z (2008) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnol Lett 30:1275–1280PubMedCrossRefGoogle Scholar
  123. 123.
    Liu D, Liu Y, Rao J, Wang G, Li H, Ge F, Chen C (2013) Overexpression of the glutathione S-transferase gene from Pyrus pyrifolia fruit improves tolerance to abiotic stress in transgenic tobacco plants. Mol Biol 47(4):515–523CrossRefGoogle Scholar
  124. 124.
    Lu C, Zhang J (1999) Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants. J Exp Bot 50:1199–1206CrossRefGoogle Scholar
  125. 125.
    Mahan JR, Gitz DC, Payton PR, Allen R (2009) Overexpression of glutathione reductase in cotton does not alter emergence rates under temperature stress. Crop Sci 49:272–280CrossRefGoogle Scholar
  126. 126.
    Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  127. 127.
    Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410PubMedCrossRefGoogle Scholar
  128. 128.
    Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Meehl GA, Karl T, Easterling DR, Changnon S, Pielke R, Changnon D, Evans J, Groisman PY, Knutson TR, Kunkel KE, Mearns LO, Parmesan C, Pulwarty R, Root T, Sylves RT, Whetton P, Zwiers F (2000) An introduction to trends in extreme weather and climate events: observations, socioeconomic impacts, terrestrial ecological impacts, and model projections. Bull Am Meteorol Soc 81:413–416CrossRefGoogle Scholar
  130. 130.
    Melchiorre M, Robert G, Trippi V, Racca R, Lascano HR (2009) Superoxide dismutase and glutathione reductase overexpression in wheat protoplast: photooxidative stress tolerance and changes in cellular redox state. Plant Growth Regul 57:57–68CrossRefGoogle Scholar
  131. 131.
    Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implication for stress responses. Plant Physiol 133:443–447PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Miller G, Suzuki N, Ciftci-yilmaz S, Mittler S (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedCrossRefGoogle Scholar
  133. 133.
    Minkov IN, Jahoubjan GT, Denov ID, Toneva AT (1999) Photooxidative stress in higher plants. In: Pessarakli M, Dekker M (eds) Plant and crop stress, 2nd edn. New York: by Inc, Basel, pp 499–525Google Scholar
  134. 134.
    Mittler R, Zilinskas BA (1992) Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J Biol Chem 267:21802–21807PubMedGoogle Scholar
  135. 135.
    Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(2002):405–410PubMedCrossRefGoogle Scholar
  136. 136.
    Melchiorre M, Robert G, Trippi V, Racca R, Lascano HR (2009) Superoxide dismutase and glutathione reductase overexpression in wheat protoplast: photooxidative stress tolerance and changes in cellular redox state. Plant Growth Regul 57:57–68CrossRefGoogle Scholar
  137. 137.
    Molinari HBC, Marur CJ, Daros E, de Campos MKF, de Carvalho JFRP, Filho JCB, Pereira LFP, Vieira LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plant 130:218–229CrossRefGoogle Scholar
  138. 138.
    Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481PubMedCrossRefGoogle Scholar
  139. 139.
    Moran JF, Becana M, Iturbeormaetxe I, Frechilla S, Klucas RV, Apariciotejo P (1994) Drought induces oxidative stress in pea-plants. Planta 194:346–352CrossRefGoogle Scholar
  140. 140.
    Montillet JL, Chamnongpol S, Rust-erucci C, Dat J, van deCotte B, Agnel JP, Battesti C, Inz-e D, VanBreusegem F, Triantaphylides C (2005) Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol 138:1516–1526PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Monakhova OF, Chernyadev II (2002) Protective role of kartolin-4 in wheat plants exposed to soil drought. Appl Environ Microbiol 38:373–380Google Scholar
  142. 142.
    Munné-Bosch S, Schwarz K, Alegre L (1999) Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in waterstressed rosemary plants. Plant Physiol 121:1047–1052PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Munné-Bosch S, Alegre L (2002) Interplay between ascorbic acid and lipophilic antioxidant defences in chloroplasts of water–stressed Arabidopsis plants. FEBS Lett 524:145–148PubMedCrossRefGoogle Scholar
  144. 144.
    Munné-Bosch S (2005) The role of a-tocopherol in plant stress tolerance. J Plant Physiol 162(2005):743–748PubMedCrossRefGoogle Scholar
  145. 145.
    Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48PubMedCrossRefGoogle Scholar
  146. 146.
    Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthetic Res 86:459–474CrossRefGoogle Scholar
  147. 147.
    Navrot N, Rouhier N, Gelhaye E, Jaquot JP (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185–195CrossRefGoogle Scholar
  148. 148.
    Nayar H, Gupta D (2006) Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants. Environ Exp Bot 58:106–113CrossRefGoogle Scholar
  149. 149.
    Noctor G, Foyer CH (1998) A re-evaluation of the ATP: NADPH budget during C3 photosynthesis. A contribution from nitrate assimilation and its associated respiratory activity? J Exp Bot 49:1895–1908Google Scholar
  150. 150.
    Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation, and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283–1304PubMedCrossRefGoogle Scholar
  151. 151.
    Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer C (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    O’Brien JA, Daudi A, Butt VS, Paul Bolwell G (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779PubMedCrossRefGoogle Scholar
  153. 153.
    Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Patakas AA, Zotos A, Beis AS (2010) Production, localisation and possible roles of nitric oxide in drought stressed grapevines. Aust J Grape Wine Res 16:203–209CrossRefGoogle Scholar
  155. 155.
    Pei Z-M, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734Google Scholar
  156. 156.
    Pennisi E (2008) The blue revolution, drop by drop, gene by gene. Science 32:171–173CrossRefGoogle Scholar
  157. 157.
    Peltzer D, Dreyer E, Polle A (2002) Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiol Biochem 40:141–150CrossRefGoogle Scholar
  158. 158.
    Polidoros NA, 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 106:112–120CrossRefGoogle Scholar
  159. 159.
    Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/ zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res 17:281–291PubMedCrossRefGoogle Scholar
  160. 160.
    Price AH, Atherton N, Hendry GA (1989) Plants under drought-stress generate activated oxygen. Free Radic Res Commun 8:61–66PubMedCrossRefGoogle Scholar
  161. 161.
    Rang ZW, Jagadish SVK, Zhou QM, Craufurd PQ, Heuer S (2011) Effect of heat and drought stress on pollen germination and spikelet fertility in rice. Environ Exp Bot 70:58–65CrossRefGoogle Scholar
  162. 162.
    Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defense operations. Trends Plant Sci 10:503–509PubMedCrossRefGoogle Scholar
  163. 163.
    Reddy AR, Raghavendra AS (2006) Photooxidative stress. In: Madhava Rao KV, Raghavendra AS, Reddy KJ (eds) Physiology and molecular biology of stress tolerance in plants. Springer, The Netherlands, pp 157–186Google Scholar
  164. 164.
    Rodríguez M, Canales E, and Borr_as- Hidalgo O (2005) Molecular aspects of abiotic stress in plants. Biotechnol. Appl. 22, 1–10Google Scholar
  165. 165.
    Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodriguez-Serrano M, del Rio LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170:43–52PubMedCrossRefGoogle Scholar
  166. 166.
    Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991Google Scholar
  167. 167.
    Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234PubMedCrossRefGoogle Scholar
  168. 168.
    Rubio MC, Gonzalez EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115:531–540PubMedCrossRefGoogle Scholar
  169. 169.
    Samuel MA, Miles GP, Ellis BE (2000) Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J. 22:367–376PubMedCrossRefGoogle Scholar
  170. 170.
    Scandalias JG (1990) Response of plant antioxidant defense genes to environmental stress. Adv Genet 28:1–41Google Scholar
  171. 171.
    Schfar C, Vidale PL, Luthi D, Frei C, Haberli C, Liniger MA, Appenzeller C (2004) The role of increasing temperature variability in European summer heatwaves. Nature 427:332–336CrossRefGoogle Scholar
  172. 172.
    Selote DS, Khanna-Chopra R (2006) Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings. Physiol Plant 127:494–506CrossRefGoogle Scholar
  173. 173.
    Sgherri CLM, Pinzino C, Navari- Izzo F (1996) Sunflower seedlings subjected to increasing stress by water deficit: changes in O2 production related to the composition of thylakoid membranes. Physiol Plant 96:446–452CrossRefGoogle Scholar
  174. 174.
    Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221CrossRefGoogle Scholar
  175. 175.
    Shu D-F, Wang L-Y, Duan M, Deng Y-S, Meng Q-W (2011) Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress. Plant Physiol Biochem 49:1228–1237PubMedCrossRefGoogle Scholar
  176. 176.
    Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde JA (2006) Stress induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biol Plant 50:793–796CrossRefGoogle Scholar
  177. 177.
    Smith MD (2011) The ecological role of climate extremes: current understanding and future prospects. J Ecol 99:651–655CrossRefGoogle Scholar
  178. 178.
    Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060CrossRefGoogle Scholar
  179. 179.
    Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58CrossRefGoogle Scholar
  180. 180.
    Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multifaceted molecule. Curr Opin Plant Biol 3:229–235PubMedCrossRefGoogle Scholar
  181. 181.
    Smirnoff N (2005) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing Ltd., Oxford, pp 53–86Google Scholar
  182. 182.
    Sorkheha K, Shirana B, Rouhia V, Khodambashia M, Sofob A (2011) Regulation of the ascorbate-glutathione cycle in wild almond during drought stress. Russ J Plant Physiol 58:76–84CrossRefGoogle Scholar
  183. 183.
    Su J, Wu R (2004) Stress inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than with constitutive synthesis. Plant Sci 166:941–948CrossRefGoogle Scholar
  184. 184.
    Sun WH, Duan M, Shu DF, Yang S, Meng QW (2010) Over-expression of StAPX in tobacco improves seed germination and increases early seedling tolerance to salinity and osmotic stresses. Plant Cell Rep 29:917–926PubMedCrossRefGoogle Scholar
  185. 185.
    Szarka A, Horemans N, Kovacs Z, Grof P, Mayer M, Banhegyi G (2007) Dehydroascorbate reduction in plant mitochondria is coupled to the respiratory electron transfer chain. Physiol Plant 129:225–232CrossRefGoogle Scholar
  186. 186.
    Tan W, Brestic M, Olsovska K, Yang X (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 168:2063–2071PubMedCrossRefGoogle Scholar
  187. 187.
    Tanaka M, Murai M, Tokunaga H, Kimura T, Okada S (1990) Tocopherol succinate reference standard (control 881) of National Institute of Hygienic Sciences. Eisei Shikenjo Hokoku 108:156–158PubMedGoogle Scholar
  188. 188.
    Tausz T, Sircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress response concept valid? J Exp Bot 55:1955–1962PubMedCrossRefGoogle Scholar
  189. 189.
    Torres-Franklin ML, Contour-Ansel D, Zuily-Fodil Y, Pham-Thi A-T (2008) Molecular cloning of glutathione reductase cDNAs and analysis of GR gene expression in cowpea and common bean leaves during recovery from moderate drought stress. J Plant Physiol 165:514–521PubMedCrossRefGoogle Scholar
  190. 190.
    Trebst A (2003) Function of b-carotene and tocopherol in photosystem II. Z. Naturforsch 58:609–620Google Scholar
  191. 191.
    Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rendiconti Lincei 19:325–346CrossRefGoogle Scholar
  192. 192.
    Upadhyaya CP, Venkatesh J, Gururani MA, Asnin L, Sharma K, Ajappala H, Park SW (2011) Transgenic potato overproducing L-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol Lett 33:2297–2307PubMedCrossRefGoogle Scholar
  193. 193.
    Uzildaya B, Turkana I, Sekmena AH, Ozgura R, Karakayab HC (2012) Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C4) and Cleome spinosa (C3) under drought stress. Plant Sci 182:59–70CrossRefGoogle Scholar
  194. 194.
    Uzildaya B, Turkana I, Sekmena AH, Ozgura R, Karakayab HC (2012) Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C4) and Cleome spinosa (C3) under drought stress. Plant Sci 182:59–70CrossRefGoogle Scholar
  195. 195.
    Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376PubMedCrossRefGoogle Scholar
  196. 196.
    Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759PubMedCrossRefGoogle Scholar
  197. 197.
    Vera-Estrella R, Blumwald E, Higgins TJV (1992) Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells. Evidence for the involvement of active oxygen species. Plant Physiol 99:1208–1215PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Vierstra RD, John TR, Proff KL (1982) Kaempferol 3-O-galactoside 7-O-rhamnoside is the major green fluorescing compound in the epidermis of Vicia faba. Plant Physiol 69:522–532Google Scholar
  199. 199.
    Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472PubMedCrossRefGoogle Scholar
  200. 200.
    Wang Y, Wisniewski M, Meilan R, Cui M, Webb R, Fuchigami L (2005) Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. J Am Soc Hortic Sci 130:167–173Google Scholar
  201. 201.
    Wang Y, Wisniewski M, Meilan R, Cui M, Fuchigami L (2006) Transgenic tomato (Lycopersicon esculentum) overexpressing cAPX exhibits enhanced tolerance to UV-B and heat stress. J Appl Horticult 8:87–90Google Scholar
  202. 202.
    Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816Google Scholar
  203. 203.
    Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975–1981PubMedCrossRefGoogle Scholar
  204. 204.
    Yan J, Wang J, Tissue D, Holaday AS, Allen R, Zhang H (2003) Photosynthesis and seed production under water-deficit conditions in transgenic tobacco plants that overexpress an arabidopsis ascorbate peroxidase gene. Crop Sci 43(2003):1477–1483CrossRefGoogle Scholar
  205. 205.
    Yang XD, Li WJ, Liu JY (2005) Isolation and characterization of a novel PHGPx gene in Raphanus sativus. Biochim Biophys Acta 1728:199–205PubMedCrossRefGoogle Scholar
  206. 206.
    Mohamed EA, Iwaki T, Munir I, Tamoi M, Shigeoka S, Wadano A (2003) Overexpression of bacterial catalase in tomato leaf chloroplasts enhances photo-oxidative stress tolerance. Plant Cell Environ 26:2037–2046Google Scholar
  207. 207.
    Yokota A, Kawasaki S, Iwano M, Nakamura C, Miyake C, Akashi K (2002) Citrulline and DRIP-1 protein (ArgE homologue) in drought tolerance of wild watermelon. Ann Bot 89:825–832PubMedPubMedCentralCrossRefGoogle Scholar
  208. 208.
    Yoon HS, Lee IA, Lee H, Lee BH, Jo J (2005) Overexpression of a eukaryotic glutathione reductase gene from Brassica campestris improved resistance to oxidative stress in Escherichia coli. Biochem Biophys Res Commun 326:618–623PubMedCrossRefGoogle Scholar
  209. 209.
    Yu T, Li YS, Chen XF, Hu J, Chang X, Zhu YG (2003) Transgenic tobacco plants overexpressing cotton glutathione S-transferase (GST) show enhanced resistance to methyl viologen. J Plant Physiol 160:1305–1311PubMedCrossRefGoogle Scholar
  210. 210.
    Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee C, Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Bioch et Bioph Acta 1797:1428–1438Google Scholar
  211. 211.
    Zhang C, Liu J, Zhang Y, Cai X, Gong P, Zhang J, Wang T, Li H, Ye Z (2011) Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep 30:389–398PubMedCrossRefGoogle Scholar
  212. 212.
    Zhang J (2011) China’s success in increasing per capita food production. J Exp Bot 62:3707–3711PubMedCrossRefGoogle Scholar
  213. 213.
    Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–527PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Chandrama Prakash Upadhyaya
    • 1
    Email author
  • Mohammad Anwar Hossain
    • 2
  1. 1.Department of BiotechnologyDR Harisingh Gour Central UniversitySagarIndia
  2. 2.Department of Genetics and Plant BreedingBangladesh Agricultural UniversityMymensinghBangladesh

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