Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings

Plant Biotechnology Reports

Volumn 5, Issue 4, 2011, Pages 353-365

  Hasanuzzaman, Mirza ^a,b   Hossain, Mohammad Anwar ^a,c   Fujita, Masayuki ^a  

^a KAGAWA UNIVERSITY   (Japan)

^b SHER E BANGLA AGRICULTURAL UNIVERSITY   (Bangladesh)

^c BANGLADESH AGRICULTURAL UNIVERSITY   (Bangladesh)

Author keywords

Antioxidant defense; Ascorbate glutathione cycle; Glyoxalase system; Reactive oxygen species; Salt stress; Sodium nitroprusside

Indexed keywords

TRITICUM AESTIVUM;

EID: 80053896950     PISSN: 18635466     EISSN: 18635474     Source Type: Journal    
DOI: 10.1007/s11816-011-0189-9     Document Type: Article

References (81)

1. Amor NB, Jiménez A, Megdiche W, Lundqvist M, Sevilla F, Abdelly C (2006) Response of antioxidant systems to NaCl stress in the halophyte Cakile maritime. Physiol Plant 126: 446-457.
2. Aravind PA, Prasad MNV (2005) Modulation of cadmium induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 45: 107-116.
3. Bandeoglu E, Eyidogan F, Yucel M, Oktem HA (2004) Antioxidant responses of shoots and roots of lentil to NaCl-stress. Plant Growth Regul 42: 69-77.
4. Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208: 337-344.
5. 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.
6. Brigelius-Flohé R, Flohé L (2003) Is there a role of glutathione peroxidases in signaling and differentiation? BioFactors 17: 93-102.
7. Da Costa PHA, de Azevedo Neto AD, Bezerra MA, Prisco JT, Gomes-Filho E (2005) Antioxidant-enzymatic system of two sorghum genotypes differing in salt tolerance. Braz J Plant Physiol 17: 353-361.
8. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci USA 83: 3811-3815.
9. de Azevedo Neto AD, Prisco JT, Filho JE, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56: 87-94.
10. 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.
11. 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.
12. Eltayeb AE, Kawano N, Badawi G, Kaminaka H, Sanekata T, Morishima I (2006) Enhanced tolerance to ozone and drought in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant 127: 57-65.
13. 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.
14. Fujita M, Hossain MZ (2003) Modulation of pumpkin glutathione S-transferases by aldehydes and related compounds. Plant Cell Physiol 44: 481-490.
15. Ghosh N, Adak MK, Ghosh PD, Gupta S, Sen Gupta DN, Mandal C (2011) Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep 5: 89-103.
16. Halušková L, Valentovičová K, Huttová J, Mistrík I, Tamás L (2009) Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tops. Plant Physiol Biochem 47: 1069-1074.
17. 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. doi: 10. 1007/s12011-011-8998-9.
18. 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.
19. Hasanuzzaman M, Hossain MA, Fujita M (2011) Selenium-induced upregulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res. doi: 10. 1007/s12011-011-8958-4.
20. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198.
21. Hernandez JA, Jimenez A, Mullineaux PM, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23: 853-862.
22. Hoque MA, Banu MN, Nakamura Y, Shimoishi Y, Murata Y (2007) Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165: 813-824.
23. Hossain MA, Fujita M (2009) Purification of glyoxalase I from onion bulbs and molecular cloning of its cDNA. Biosci Biotechnol Biochem 73: 2007-2013.
24. Hossain MA, Fujita M (2010) Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. Physiol Mol Biol Plant 16: 19-29.
25. 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.
26. 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.
27. Hossain MA, Hossain MZ, Fujita M (2009) Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3: 53-64.
28. Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plant 26: 259-272.
29. Hossain MA, Hasanuzzaman M, Fujita M (2011) Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. Front Agric China 5: 1-14.
30. Hu Y, Ge Y, Zhang C, Ju T, Cheng W (2009) Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment. Plant Growth Regul 59: 51-61.
31. 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.
32. 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.
33. Jain M, Choudhary D, Kale RK, Sarin NB (2002) Salt- and glyphosate-induced increase in glyoxalase I activity in cell lines of groundnut (Arachis hypogaea). Physiol Plant 114: 499-505.
34. 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.
35. Kalapos MP, Garzo T, Antoni F, Mandl J (1992) Accumulation of S-d-lactoylglutathione and transient decrease of glutathione level caused by methylglyoxal load in isolated hepatocytes. Biochim Biophys Acta 1135: 159-164.
36. Kim JM, Kim H, Kwon SB, Lee SY, Chung SC, Jeong DW, Min BM (2004) Intracellular glutathione status regulates mouse bone marrow monocyte-derived macrophage differentiation and phagocytic activity. Biochem Biophys Res Commun 325: 101-108.
37. Kuźniak E, Sklodowska M (2005) Compartment-specific role of the ascorbate-glutathione cycle in the response to tomato leaf cells to Botrytis cinerea infection. J Exp Bot 413: 921-933.
38. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169: 323-330.
39. Li QY, Niu HB, Yin J, Wang MB, Shao HB, Deng DZ, Chen XX, Ren JP, Li YC (2008) Protective role of exogenous nitric oxide against oxidative-stress induced by salt stress in barley (Hordeum vulgare). Colloids Surf B Biointerfaces 65: 220-225.
40. May MJ, Vernoux T, Leaver C, van Montagu M, Inze D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49: 649-667.
41. Miller G, Sujuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity. Plant Cell Environ 33: 453-467.
42. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
43. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498.
44. Mittova V, Tal M, Volokita M, Guy M (2003a) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26: 845-856.
45. Mittova V, Theodoulou FL, Kiddle G, Gomez L, Volokita M, Tal M (2003b) Co-ordinate induction of glutathione biosynthesis and glutathione metabolizing enzymes is correlated with salt tolerance. FEBS Lett 554: 417-442.
46. Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55: 1105-1113.
47. Moellering D, McAndrew J, Patel RP, Cornwell T, Lincoln T, Cao X, Messina JL, Forman HJ, Jo H, Darley-Usmar VM (1998) Nitric oxide-dependent induction of glutathione synthesis through increased expression of gamma-glutamylcysteine synthetase. Arch Biochem Biophys 358: 74-82.
48. MSTAT-C (1990) Microcomputer statistical program for experiment design and analysis. Russell Freed (ed). MSTAT/Michigan State University, East Lansing.
49. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880.
50. Neill SJ, Desikan R, Clarke A, Hurat RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53: 1237-1247.
51. 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.
52. 2. Physiol Plant 135: 29-42.
53. Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact 16: 1084-1105.
54. 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.
55. Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M (2008) Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. J Integr Plant Biol 50: 231-243.
56. Sekmen AH, Turkan I, Takio S (2007) Differential responses to antioxidant enzymes and lipid peroxidation of salt stress in salt-tolerant Plantago maritime and salt-sensitive Plantago media. Physiol Plant 131: 399-411.
57. Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant 112: 487-494.
58. Sheokand S, Kumari A, Sawhney V (2008) Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants. Physiol Mol Biol Plant 14: 355-362.
59. Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45: 542-550.
60. Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20: 289-297.
61. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140: 613-623.
62. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2008) Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Trans Res 17: 171-180.
63. Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multifaceted molecule. Curr Opin Plant Biol 3: 229-235.
64. Sung CH, Hong JK (2010) Sodium nitroprusside mediates seedling development and attenuation of oxidative stresses in Chinese cabbage. Plant Biotechnol Rep 4: 243-251.
65. Takatsume Y, Izawa S, Inoue Y (2006) Methylglyoxal as a signal initiator for activation of the stress-activated protein kinase cascade in the fission yeast Schizosaccharomyces pombe. J Biol Chem 281: 9086-9092.
66. Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009a) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60: 795-804.
67. Tanou G, Molassiotis A, Diamantidis G (2009b) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot 65: 270-281.
68. Tian X, Lei Y (2006) Nitric oxide treatment alleviates drought stress in wheat seedlings. Biol Plant 50: 775-778.
69. Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67: 2-9.
70. Veena, Reddy VS, Sopory SK (1999) Glyoxalase I from Brassica juncea: molecular cloning, regulation and its over-expression confer tolerance in transgenic tobacco under stress. Plant J 17: 385-395.
71. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stressing the roots of Cassia tora L. Plant Cell Physiol 46: 1915-1923.
72. Wang Z, Zhang L, Xiao Y, Chen W, Tang K (2010) Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol 52: 400-409.
73. Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28: 325-353.
74. Xu Y, Sun X, Jin J, Zhou H (2010) Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fescue. J Plant Physiol 167: 512-518.
75. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) 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.
76. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005b) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337: 61-67.
77. 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.
78. Zhang F, Wang Y, Yang Y, Wu H, Wang D, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30: 775-785.
79. 2 and antioxidant system of strawberry leaves. Agric J 3: 286-291.
80. Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67: 222-227.
81. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167: 527-533.