Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system

Australian Journal of Crop Science

Volumn 6, Issue 8, 2012, Pages 1314-1323

  Hasanuzzaman, Mirza ^a,b   Nahar, Kamrun ^a,b   Alam, Mahabub ^a   Fujita, Masayuki ^a  

^a KAGAWA UNIVERSITY   (Japan)

^b SHER E BANGLA AGRICULTURAL UNIVERSITY   (Bangladesh)

Author keywords

Abiotic stress; Glutathione; Heat stress; Reactive oxygen species; Signaling molecules; Sodium nitroprusside

Indexed keywords

TRITICUM AESTIVUM;

EID: 84865774249     PISSN: 18352693     EISSN: 18352707     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Addinsoft XLSTAT 2010: Data analysis and statistics software for Microsoft Excel. Addinsoft, Paris, France (2010)
2. Ahmad P, Prasad MNV (2012), Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability. Springer, New York
3. Aien A, Khetarpal S, Pal M (2011) Photosynthetic characteristics of potato cultivars grown under high temperature. Am-Eurs J Agric Environ Sci 11: 633-639
4. Anjali A, Shantha N, Pathak PC (2006) Effect of high temperature on hydrogen peroxide scavenging enzymes during reproductive phase in aromatic rice cultivars. Indian J Plant Physiol 11:427-431
5. Arnon DT (1949) Copper enzymes in isolated chloroplasts polyphenaloxidase in Beta vulgaris. Plant Physiol 24:1-15
6. 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 Roton, FL, pp. 77-104
7. Balla K, Bencze S, Janda T, Veisz O (2009) Analysis of heat stress tolerance in winter wheat. Acta Agron Hung 57:437-444
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
9. Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604-611
10. Creighton DJ, Hamilton DS (2001) Brief history of glyoxalase I and what we have learned about metal ion-dependent, enzyme-catalyzed isomerizations. Arch Biochem Biophys 387:1-10
11. 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 79:1-10
12. Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338-350
13. Efeoglu B, Terzioglu S (2009) Photosynthetic responses of two wheat varieties to high temperature. EurAsia J Biosci 3:97-106
14. Egli DB, Tekrony DM, Heitholt JJ, Rupe J (2005) Air temperature during seed filling and soybean seed germination and vigor. Crop Sci 45:1329-1335
15. Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162-167
16. El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85-96
17. Eltayeb AE, Kawano N, Badawi G, Kaminaka H, Sanekata T, Morishima I (2006) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant 127: 57-65
18. Eltayeb AL, Kawano N, Badawi GH, 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. Planta 225:1255-1264
19. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21-25
20. Garg N, Manchanda G (2009) ROS generation in plants: Boon or bane? Plant Biosyst 143:81-96
21. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909-930
22. Guilioni L, Wery J, Tardieu F (1997) Heat stress-induced abortion of buds and flowers in pea: Is sensitivity linked to organ age or to relations between reproductive organs? Ann Bot 80:159-168
23. Hall AE (1992) Breeding for heat tolerance. Plant Breed Rev 10:129-168
24. Hasanuzzaman M, Fujita M (2011) Selenium pretreatment upregulates the antioxidant defense and methylglyoxal
25. detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol Trace Elem Res 143:1758-1776
26. Hasanuzzaman M, Gill SS, Fujita M (2012c) 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 (In press).
27. Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012a) Plant Responses and tolerance to abiotic oxidative stress: Antioxidant defenses is a key factors. In: Bandi V, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: Perspectives and strategies. Springer, Berlin. pp. 261-316
28. Hasanuzzaman M, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am J Plant Physiol 5:295-324
29. Hasanuzzaman M, Hossain MA, Fujita M (2011a) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5: 353-365
30. Hasanuzzaman M, Hossain MA, Fujita M (2011b) Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704-1721
31. Hasanuzzaman M, Hossain MA, Fujita M (2012b) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res. DOI: 10.1007/s12011-012-9419-4
32. Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147-151
33. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198
34. Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385-395
35. 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
36. 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
37. Innocenti G, Pucciariello C, Gleuher ML, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597-1602
38. Ismail AM, Hall AE (1999) Reproductive-stage, heat tolerance, leaf membrane thermostability and plant morphology in cowpea. Crop Sci 39:1762-1768
39. Jiang Y, Huang B (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52: 341-349
40. Jin, JW, Xu YF, Huang YF (2010) Protective effect of nitric oxide against arsenic-induced oxidative damage in tall fescue leaves. Afr J Biotechnol 9:1619-1627
41. Kim K, Portis J (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Lett 571:124-128
42. Kocsy G, Szalai G, Galiba G (2002) Effect of heat stress on glutathione biosynthesis in wheat. Acta Biol Szeged 46:71-72
43. Kong W, Huang C, Chen Q, Zou Y, Zhang J (2011) Nitric oxide alleviates heat stress-induced oxidative damage in Pleurotus eryngii var. tuoliensis. Fung Genet Biol 49:15-20
44. Kühn H, Borchert A (2002) Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes. Free Rad Biol Med 33:154-172
45. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress, Plant Sci. 169: 323-330
46. Leterrier M, Valderrama R, Chaki M, Airaki M, Palma JM, Barroso JB, Corpas FJ (2012) Function of nitric oxide under environmental stress conditions. In: Khan NA, Nazar R, Iqbal N, Anjum NA (eds) Phytohormones and abiotic Stress tolerance in plants. Springer, Berlin. pp. 99-113
47. Lu P, Sang W-G, Ma K-P (2007) Activity of stress-related antioxidative enzymes in the invasive plant crofton weed (Eupatorium adenophorum). J Integr Plant Biol 49:1555-1564
48. Ma Y-H, Ma F-W, Zhang J-K, Li M-J, Wang Y-H, 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
49. 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
50. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405-410
51. Monjardino P, Smith AG, Jones RJ (2005) Heat stress effects on protein accumulation of maize endosperm. Crop Sci 45:1203-1210
52. Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylacoidal ascorbate peroxidase show increased resistance to paraquat-induced photo-oxidative stress to nitric oxide-induced cell death. Plant J 38: 940-953
53. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867-880
54. Noctor G, Foyer CH (1998) Ascorbate and glutathione: Keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249-279
55. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454-484
56. Paradiso A, Berardino R, de Pinto M, di Toppi LS, Storelli FT, de Gara L (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362-374
57. 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
58. Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. Biochem Biophys Acta 911:349-355
59. Reda F, Mandoura HMH (2011) Response of enzymes activities, photosynthetic pigments, proline to low or high
60. temperature stressed wheat plant (Triticum aestivum L.) in the presence or absence of exogenous proline or cysteine. Int J Acad Res 3:108-115 Rivero RM, Ruiz JM, Romero L Oxidative metabolism in tomato plants subjected to heat stress. J Hortic Sci Biotechnol 79: 560-564 2004
61. Sánchez-Casas P, Klessig DF (1994) A salicylic acidbinding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species. Plant Physiol 106:1675-1779
62. Sheokand S, Bhankar V, Sawhney V (2010) Ameliorative effect of exogenous nitric oxide on oxidative metabolism in NaCl treated chickpea plants. Braz J Plant Physiol 22:81-90
63. Singh AK, Singhal GS (2001) Effect of irradiance on the thermal stability of thylakoid membrane isolated from acclimated wheat leaves. Photosynthetica 39:23-27
64. Song L, Ding W, Zhao M, Sun B, Zhang L (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci 171:449-458
65. Tanou G, Job C, Rajjou L, Arc E, Belghzi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveal the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795-804
66. Thornalley PJ (2003) Glyoxalase I - structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans 31:1343-1348
67. 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
68. Vander Jagt DL (1993) Glyoxalase II: Molecular characteristics, kinetics and mechanism. Biochem Soc Trans 21:522-527
69. Wahid A (2007) Physiological implications of metabolites biosynthesis in net assimilation and heat stress tolerance of sugarcane (Saccharum officinarum) sprouts. J Plant Res 120:219-228
70. Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321-330
71. 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
72. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61-67
73. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005b) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265-6271
74. Yin H, Chen QM, Yi MF (2008) Effects of short-term heat stress on oxidative damage and responses of antioxidant system in Lilium longiflorum. Plant Growth Regul 54:45-54
75. 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
76. Zhang JX, Kirkham MB (1994) Drought stress induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785-791