Nitric oxide triggers a concentration-dependent differential modulation of superoxide dismutase (FeSOD and Cu/ZnSOD) activity in sunflower seedling roots and cotyledons as an early and long distance signaling response to NaCl stress

Plant Signaling and Behavior

Volumn 10, Issue 10, 2015, Pages

  Arora, Dhara ^a   Bhatla, Satish C ^a  

^a UNIVERSITY OF DELHI   (India)

Author keywords

Cu Zn SOD; FeSOD; Helianthus annuus; NaCl stress; Nitric oxide crosstalk; Seedling growth; Superoxide dismutase (SOD)

Indexed keywords

ANTIOXIDANT; ISOPROTEIN; NITRIC OXIDE; NITROPRUSSIDE SODIUM; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE;

COTYLEDON; METABOLISM; OXIDATIVE STRESS; PLANT ROOT; SALT TOLERANCE; SEEDLING; SIGNAL TRANSDUCTION; SUNFLOWER;

ANTIOXIDANTS; COTYLEDON; HELIANTHUS; NITRIC OXIDE; NITROPRUSSIDE; OXIDATIVE STRESS; PLANT ROOTS; PROTEIN ISOFORMS; SALT-TOLERANCE; SEEDLINGS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE;

EID: 84954556817     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.1080/15592324.2015.1071753     Document Type: Article

References (50)

1. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stress. Plant Cell Env 2010; 33:453-467; http://dx.doi.org/10.1111/j.1365-3040.2009.02041.x
2. Hernandez JA, Jimenez A, Mullineaux P, Sevilla F. Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Env 2000; 23:853-862; http://dx.doi.org/10.1046/j.1365-3040.2000.00602.x
3. Bose J, Moreno AR, Shabala S. ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 2013, doi:10.1093/jxb/ert430; PMID:AMBIGUOUS
4. Tanou G, Molassiotis A, Diamantidis G. Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Env Exp Bot 2009; 65:270281; http://dx.doi.org/10.1016/j.envexpbot.2008.09.005
5. Karray-Bouraoui N, Harbaoui F, Rabhi M, Jallali I, Ksouri R, Attia H, Msilini N, Lachaal M. Different antioxidant responses to salt stress in two different provenances of Carthamus tinctorius L. Acta Physiol Plant 2011; 33:1435-1444; http://dx.doi.org/10.1007/s11738-010-0679-3
6. Gupta B, Huang B. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014; Article ID 701596, http://dx.doi.org/10.1155/2014/701596; PMID:24804192
7. Scandalios JG. Oxygen stress and superoxide dismutases. Plant Physiol 1993; 101: 7-12; PMID:12231660
8. Meloni DA, Oliva MA, Carlos AM, Cambraia . Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Env Exp Bot 2003; 49:69-76; http://dx.doi.org/10.1016/S0098-8472(02)00058-8
9. Asada D, Takahashi M. Production and scavenging of active oxygen in chloroplasts. In DJ Kyle, CB Osmond, CJ Arntzen eds, Photoinhibition. Elsevier, Amsterdam, 227-287
10. Wang B, Luttge U, Ratajczak R. Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L. J Plant Physiol 2004; 161:285-293; PMID:15077627; http://dx.doi.org/10.1078/0176-1617-01123
11. David A, Yadav S, Bhatla SC. Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol Plant 2010; 140: 34254.; PMID:20738803; http://dx.doi.org/10.1111/j.1399-3054.2010.01408.x
12. Monzon GC, Pinedo M, Rienzo JD, Novo-Uzal E, Pomar F, Lamattina L, de la Canal L. Nitric oxide is required for determining root architecture and lignin composition in sunflower. Supporting evidence from microarray analyses. Nitric oxide 2014; http://dx.doi.org/10.1016/j.niox.2014.04.004
13. Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H. Biological significance of nitric oxidemediated protein modifications. Am J Physiol Lung Cell Mol Physiol 2004; 287:262-268; http://dx.doi.org/10.1152/ajplung.00295.2003
14. Astier J, Lindermayr C. Nitric oxide-dependent posttranslational modification in plants: an update. Int J Mol Sci 2012; 13: 15193-15208; PMID:23203119; http://dx.doi.org/10.3390/ijms131115193
15. Wink DA, Mitchell JB. Chemical biology of NO: insights into regulation, protective and toxic mechanisms of nitric oxide. Free Rad Bio Med 1998; 25:434-456; http://dx.doi.org/10.1016/S0891-5849(98)00092-6
16. Stamler JS, Lamas S, Fang FC. Nitrosylation: the prototypic redox-based signalling mechanism. Cell 2001; 6:675-683; http://dx.doi.org/10.1016/S0092-8674(01)00495-0
17. Mannick JB, Schonhoff CM. NO means no and yes: regulation of cell signaling by protein nitrosylation. Free Rad Res 2004; 38:1-7; http://dx.doi.org/10.1080/10715760310001629065
18. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005; 6:150-166
19. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 2003; 30:776-783; PMID:15688001; http://dx.doi.org/10.1016/S0006-291X(03)00814-3
20. Joshi MS, Ponther JL, Lancaster JR. Cellular antioxidant and pro-oxidant actions of nitric oxide. Free Rad Bio Med 1999; 27:1357-1366; http://dx.doi.org/10.1016/S0891-5849(99)00179-3
21. Hummel SG, Fischer AJ, Martin SM, Schafer FQ, Buettner GR. Nitric oxide as a cellular antioxidant: A little goes a long way. Free Rad Bio Med 2006; 40: 501-506; http://dx.doi.org/10.1016/j.freeradbiomed.2005.08.047
22. Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 2002; 163:515-523; http://dx.doi.org/10.1016/S01689452(02)00159-0
23. Kopyra M, Gwozdz FA. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 2003; 41:1011-1017; http://dx.doi.org/10.1016/j.plaphy.2003.09.003
24. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002; 7:1360-1385; http://dx.doi.org/10.1016/S1360-1385(02)02312-9
25. Vranova E, Inze D, Breusegem FV. Signal transduction during oxidative stress. J Exp Bot 2002; 53:1227-1236; PMID:11997371; http://dx.doi.org/10.1093/jexbot/53.372.1227
26. Beligni MV, Lamattina L. Is nitric oxide toxic or protective? Trends Plant Sci 1999; 4:299-300; PMID:10431217; http://dx.doi.org/10.1016/S1360-1385(99)01451-X
27. Lin CC, Jih PJ, Lin HH, Lin JS, Chang LL, Shen YH, Jeng ST. Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol Biol 2011; 77:235249; PMID:21833542; http://dx.doi.org/10.1007/s11103-011-9805-x
28. Manai J, Kalai T, Gouia H, Corpas FJ. Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 2014; 14:433-446
29. Shi Q, Ding F, Wang X, Wei M. Exogenous nitric oxide protects cucumber roots oxidative stress induced by salt stress. Plant Physio Biochem 2007; 45:542-550; http://dx.doi.org/10.1016/j.plaphy.2007.05.005
30. Sehrawat A, Abat JK, Deswal R. RuBisCO depletion improved proteome coverage of cold responsive Snitrosylated targets in Brassica juncea. Frontiers Plant Sci 2013; 4:1-14; http://dx.doi.org/10.3389/fpls.2013.00342
31. Martinez A, Peluffo G, Petruk AA, Hugo M, Pineyro D, Demicheli V, Moreno DM, Lima A, Batthyany C, Duran R, Robello C, Marti MA, Larrieux N, Buschiazzo A, Trujillo M, Radi R, Piacenza L. Structural and molecular basis of the peroxynitrite-mediated nitration and inactivation of Trypanosoma cruzi ironsuperoxide dismutases (Fe-SODs) A and B. J Biol Chem 2014; 269:12760-12778; http://dx.doi.org/10.1074/jbc.M113.545590
32. Singh RJ, Hogg N, Goss SPA, Antholine WE, Kalyanaraman B. Mechanism of superoxide dismutase/ H2O2-mediated nitric oxide release from S-nitrosoglutathione-role of glutamate. Arch. Biochem Biophy 1999; 372:8-15; http://dx.doi.org/10.1006/abbi.1999.1447
33. Laspina NV, Groppa MD, Tomaro ML, Benavides MP. Nitric oxide protects sunflower leaves against Cdinduced oxidative stress. Plant Sci 2005; 169:323-330; http://dx.doi.org/10.1016/j.plantsci.2005.02.007
34. Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G. Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 2003; 54:109-136; PMID:14502987; http://dx.doi.org/10.1146/annurev.arplant.54.031902.134752
35. Hasanuzzaman M, Nahar K, Alam MM, Fujita M. Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 2012; 6:1314-1323
36. Abreu IA, Cabelli DE. Superoxide dismutases-a review of the metal-associated mechanistic variations. Biochim Biophys Acta 2010, 1804:263-274; http://dx.doi.org/10.1016/j.bbapap.2009.11.005
37. Jelonek MA, Wieczorek JF. Understanding the fate of peroxynitrite in plant cells-from physiology to pathophysiology. Phytochem 2011; 72:681-688; http://dx.doi.org/10.1016/j.phytochem.2011.02.025
38. Khan MN, Mohammad F, Mobin M, Saqib MA. Tolerance of plants to abiotic stress: a role of nitric oxide and calcium, in: M.N. Khan, M. Mobin, F. Mohammad, F.J. Corpas (Eds.), Nitric oxide in plants: Metabolism and role in stress physiology, Springer International Pub., Switzerland, 2014, 225-242
39. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol. (1996) Nov;271(5 Pt 1):C1424-37
40. Chavez MD, Lakshmanan N, Kavida M. Impact of superoxide dismutase on nitric oxide and peroxynitrite levels in the microcirculation-a computational model, Proc. 29th Ann. Internatl. Conf. of the IEEE EMBS, August 23-26, 2007
41. Arita NO, Cohen MF, Tokuda G, Yamaski H. Fluorometric detection of nitric oxide with diaminofluoresceins (DAFs): applications and limitations for plant NO research. Plant Cell Monogr 2006; 5:269-80
42. Vandelle E, Delledonne M. Peroxynitrite formation and function in plants. Plant Sci 2011; 181:534-539.; PMID:21893249; http://dx.doi.org/10.1016/j.plantsci.2011.05.002
43. MacMillan-Crow LA, Crow JP, Kerby JD, Beckman JS. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci USA 1996; 93:11853-11858; PMID:8876227; http://dx.doi.org/10.1073/pnas.93.21.11853
44. Bayir H, Kagan VE, Clark RSB, Janesko-Feldman K, Rafikov R, Huang Z, Zhang X, Vagni V, Billiar TR, Kochanek PM. Neuronal NOS-mediated nitration and inactivation of manganese superoxide dismutase in brain after experimental and human brain injury. J Neurochem 2007; 101:168-181; PMID:17394464; http://dx.doi.org/10.1111/j.1471-4159.2006.04353.x
45. Chaki M, Valderrama R, Fernandez-Ocana AM, Carreras A, Lopez-Jaramillo J, Luque F, Palma JM, Pedrajas JR, Begara-Morales JC, Sanchez-Calvo B, et al. Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 2009; 60:4221-4234; PMID:19717529; http://dx.doi.org/10.1093/jxb/erp263
46. Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C. Differential inhibition of Arabidopsis superoxide dismutases by peroxynitritemediated tyrosine nitration. J Exp Bot 2015; 66 (3):989-99; http://dx.doi.org/10.1093/jxb/eru458
47. Nishikimi M, Rao NA, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 1972; 46(2):849-854; PMID:4400444; http://dx.doi.org/10.1016/S0006-291X(72)80218-3
48. McCord JM. Assay of superoxide dismutase activity. Curr Protoc Toxicol 1999; Chapter 7 Unit 7.3:7.3.17.3.9
49. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-54; PMID:942051; http://dx.doi.org/10.1016/0003-2697(76)90527-3
50. Jain P, Bhatla SC. Signaling role of phospholipid hydroperoxide gltathione peroxide (PHGPX) accompanying sensing of NaCl stress in etiolated sunflower seedling cotyledons. Plant Signal Behav 2014; 9:12; http://dx.doi.org/10.4161/15592324.2014.977746