Melatonin and nitric oxide modulate glutathione content and glutathione reductase activity in sunflower seedling cotyledons accompanying salt stress

Nitric Oxide - Biology and Chemistry

Volumn 59, Issue , 2016, Pages 42-53

  Kaur, Harmeet ^a   Bhatla, Satish C ^a  

^a UNIVERSITY OF DELHI   (India)

Author keywords

Glutathione; Glutathione reductase; Melatonin; Nitric oxide; Salt stress; Sunflower

Indexed keywords

2 (4 CARBOXYPHENYL) 4,4,5,5 TETRAMETHYLIMIDAZOLINE 1 OXYL 3 OXIDE; ACETYLSEROTONIN METHYLTRANSFERASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; MELATONIN; NITRIC OXIDE; NITROPRUSSIDE SODIUM; 1,3-DIHYDROXY-4,4,5,5-TETRAMETHYL-2-(4-CARBOXYPHENYL)TETRAHYDROIMIDAZOLE; BENZOIC ACID DERIVATIVE; IMIDAZOLE DERIVATIVE; NITRIC OXIDE DONOR; REACTIVE OXYGEN METABOLITE;

ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; COTYLEDON; DOWN REGULATION; ENZYME ACTIVITY; HELIANTHUS ANNUUS; HOMEOSTASIS; HOMOGENATE; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; SALT STRESS; SEEDLING; UPREGULATION; DRUG EFFECTS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SALINITY; SUNFLOWER;

ACETYLSEROTONIN O-METHYLTRANSFERASE; BENZOATES; COTYLEDON; GLUTATHIONE; GLUTATHIONE REDUCTASE; HELIANTHUS; IMIDAZOLES; MELATONIN; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROPRUSSIDE; REACTIVE OXYGEN SPECIES; SALINITY; SEEDLINGS; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84978887908     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2016.07.001     Document Type: Article

References (58)

1. [1] Mukherjee, S., David, A., Yadav, S., Baluska, F., Bhatla, S.C., Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol. Plant 152 (2014), 714–728.
2. [2] David, A., Yadav, S., Bhatla, S.C., Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol. Plant 140 (2010), 342–354.
3. [3] Mukherjee, S., Bhatla, S.C., A novel fluorescence imaging approach to monitor salt stress-induced modulation of ouabain-sensitive ATPase activity in sunflower seedling roots. Physiol. Plant 150 (2014), 540–549.
4. [4] Jain, P., Bhatla, S.C., Signaling role of phospholipid hydroperoxide glutathione peroxidase (PHGPX) accompanying sensing of NaCl stress in etiolated sunflower seedling cotyledons. Plant Signal Behav., 9, 2014, 10.4161/15592324.2014.977746.
5. [5] Arora, D., S.C. Bhatla 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 Signal Behav., 10, 2015, 10.1080/15592324.2015.1071753.
6. [6] David, A., Yadav, S., Baluska, F., Bhatla, S.C., Nitric oxide accumulation and protein tyrosine nitration as a rapid and long distance signalling response to salt stress in sunflower seedlings. Nitric Oxide 50 (2015), 28–37.
7. [7] Foyer, C.H., Halliwell, B., The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133 (1976), 21–25.
8. [8] Loewus, F.A., Ascorbic acid and its metabolic products. Preiss, J., (eds.) The Biochemistry of Plants, 1988, Academic Press, New York, NY, USA, 85–107 1988.
9. [9] Pastore, A., Federici, G., Bertini, E., Piemonte, F., Analysis of glutathione: implication in redox and detoxification. Clin. Chim. Acta 333 (2003), 19–39.
10. [10] Foyer, C.H., Lopez-Delgado, H., Dat, J.F., Scott, I.M., Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol. Plant 100 (1997), 241–254.
11. [11] Xiang, C., Werner, B.L., Christensen, E.M., Oliver, D.J., The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol. 126 (2001), 564–574.
12. [12] Mullineaux, P.M., Rausch, T., Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res. 86 (2005), 459–474.
13. [13] Foyer, C.H., Theodoulou, F.L., Serge, D., The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci. 6 (2001), 486–492.
14. [14] Carlberg, I., Mannervik, B., Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J. Biol. Chem. 250 (1975), 5475–5480.
15. [15] Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M., Reactive oxygen species, oxidative damage, and antioxidative defense mechanisms in plants under stressful conditions. J. Bot., 2012, 1–26, 10.1155/2012/217037.
16. [16] Arnao, M.B., Hernandez-Ruiz, J., Melatonin: plant growth regulator and/or biostimulator during stress?. Trends Plant Sci. 19 (2014), 789–797.
17. [17] Reiter, R.J., Tan, D.X., Osuna, C., Gitto, E., Actions of melatonin in the reduction of oxidative stress. J. Biomed. Sci. 7 (2000), 444–458.
18. [18] Zhang, H.-M., Zhang, Y., Melatonin: a well-documented antioxidant with conditional pro-oxidants actions. J. Pineal Res. 57 (2014), 131–146.
19. [19] Rodriguez, C., Mayo, J.C., Sainz, R.M., Antolin, I., Herrera, F., Martin, V., Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 36 (2004), 1–9.
20. 4 interaction in cucumber (Cucumis sativus L.). J. Pineal Res. 57 (2014), 269–279.
21. [21] Zhang, N., Sun, Q., Zhang, H., Cao, Y., Weeda, S., Ren, S., Guo, Y., Roles of melatonin in abiotic stress resistance in plants. J. Exp. Bot., 2014, 10.1093/jxb/eru336.
22. [22] Urata, Y., Honma, S., Goto, S., Todoroki, S., Iida, T., Cho, S., Honma, K., Kondo, T., Melatonin induces γ-glutamylcysteine synthetase mediated by activator protein-1 in human vascular endothelial cells. Free Radic. Bio Med. 27 (1999), 838–847.
23. [23] Byeon, Y., Back, K., Melatonin synthesis in rice seedlings in vivo is enhanced at high temperatures and under dark conditions due to increased serotonin acetyltransferase and N-acetylserotonin methyltransferase activities. J. Pineal Res. 56 (2014), 189–195.
24. [24] Byeon, Y., Choi, G.-H., Lee, H.Y., Back, K., Melatonin biosynthesis requires N-acetylserotonin methyltransferase activity of caffeic acid O-methyltransferase in rice. J. Exp. Bot. 66 (2015), 6917–6925.
25. [25] Neill, S.J., Desikan, R., Hancock, J.T., Nitric oxide signalling in plants. New Phytol. 159 (2003), 11–35.
26. [26] Ferreira, L.C., Cataneo, A.C., Nitric oxide in plants: a brief discussion on this multifunctional molecule. Sci. Agric. 67 (2010), 236–243.
27. [27] Innocenti, G., Pucciariello, C., Gleuher, M., Hopkins, J., Stefano, M., Delledonne, M., Puppo, A., Baudouin, E., Frendo, P., Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225 (2007), 1597–1602.
28. [28] Xiong, Y., Uys, J.D., Tew, K.D., Townsend, D.M., S-glutathionylation: from molecular mechanisms to health outcomes. Antioxid. Redox Signal 15 (2011), 233–270.
29. [29] Song, L., Ding, W., Zhao, M., Sun, B., Zhang, L., Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci. 171 (2006), 449–458.
30. [30] Aravind, P., Prasad, M.N.V., Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate–glutathione cycle and glutathione metabolism. Plant Physiol. Biochem. 43 (2001), 107–116.
31. [31] Sairam, R.K., Rao, K.V., Srivastava, G.C., Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 163 (2002), 1037–1046.
32. [32] Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
33. [33] Foyer, C., Lelandais, M., Galap, C., Kunert, K.J., Effects of elevated cytosolic glutathione reductase activity on the cellular glutathione pool and photosynthesis in leaves under normal and stress conditions. Plant Physiol. 97 (1991), 863–872.
34. [34] Tausz, M., Sircelj, H., Grill, D., The glutathione system as a stress marker in plant ecophysiology: is a stresseresponse concept valid?. J. Exp. Bot. 55 (2004), 1955–1962.
35. [35] Noctor, G., Arisi, A.-C.M., Jouanin, L., Kunert, K.J., Rennenberg, H., Foyer, C.H., Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J. Exp. Bot. 49 (1998), 623–647.
36. [36] Foyer, C.H., Lelandais, M., Galap, C., Kunert, K.J., Effects of elevated glutathione reductase activity on the cellular glutathione pool and photosynthesis in leaves under normal and stress conditions. Plant Physiol. 97 (1991), 863–872.
37. [37] Gossett, D.R., Millhollon, E.P., Lucas, M.C., Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci. 34 (1993), 706–714.
38. [38] Rios-Gonzalez, K., Erdei, L., Lips, S.H., The activity of antioxidant enzymes in maize and sunflower seedlings as affected by salinity and different nitrogen sources. Plant Sci. 162 (2002), 923–930.
39. [39] Stepien, P., Klobus, G., Antioxidant defense in the leaves of C3 and C4 plants under salinity stress. Physiol. plant 125 (2005), 31–40.
40. [40] Hernandez, J.A., 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 Environ. 23 (2000), 853–862.
41. [41] Tan, D.X., Chen, L.D., Poeggeler, B., Manchester, L.C., Reiter, R.J., Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr. J. 1 (1993), 57–60.
42. [42] Tan, D.X., Manchester, L.C., Reiter, R.J., Plummer, B.F., Hardies, L.J., Weintraub, S.T., Vijayalaxmi, Shepherd, A.M.M., A novel melatonin metabolite, cyclic 3-hydroxymelatonin: a biomarker of in vivo hydroxyl radical generation. Biochem. Biophys. Res. Commun. 253 (1998), 614–620.
43. [43] Tan, D.X., Manchester, L.C., Reiter, R.J., Qi, W.B., Karbownik, M., Calvo, J.R., Significance of melatonin in antioxidative defence system: reactions and products. Biol. Signals Recept 9 (2000), 137–159.
44. [44] Reiter, R.J., Tan, D.X., Terron, M.P., Flores, L.J., Czarnocki, Z., Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim. Pol. 54 (2007), 1–9.
45. [45] Wang, P., Yin, L., Liang, D., Li, C., Ma, F., Yue, Z., Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate–glutathione cycle. J. Pineal Res. 53 (2012), 11–20.
46. [46] Wei, W., Li, Q.T., Chu, Y.N., Reiter, R.J., Yu, X.M., Zhu, D.H., Zhang, W.K., Ma, B., Lin, Q., et al. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J. Exp. Bot. 66 (2015), 695–707, 10.1093/jxb/eru392.
47. [47] Zhang, H., Squadrito, G.L., Pryor, W.A., The reaction of melatonin with peroxynitrite: formation of melatonin radical cation and absence of stable nitrated products. Biochem. Biophys. Res. Commun. 251 (1998), 83–87.
48. [48] Zhang, H., Squadrito, G.L., Uppu, R., Pryor, W.A., Reaction of peroxynitrite with melatonin: a mechanistic study. Chem. Res. Toxicol. 12 (1999), 526–534.
49. [49] Berchner-Pfannschmidt, U., Tug, S., Trinidad, B., Becker, M., Oehme, F., Flamme, I., Fandrey, J., Kirsch, M., The impact of N-nitrosomelatonin as nitric oxide donor in cell culture experiments. J. Pineal Res. 45 (2008), 489–496.
50. 3 at physiological pH. J. Biol. Chem. 278 (2003), 11931–11936.
51. [51] Kytzia, A., Korth, H.-G., Sustmann, R., De Groot, H., Priv-Doz, M.K., On the mechanism of the ascorbic acid-induced release of nitric oxide from nitrosated tryptophan derivatives. Scavenging of NO by ascorbyl radicals. Chem. Eur. J. 12 (2006), 8786–8797.
52. [52] Kytzia, A., Korth, H.-G., De Groot, H., Kirsch, M., Catecholamine-induced release of nitric oxide from N-nitrosotryptophan derivatives: a non-enzymatic way of catecholamine-oxidation. Org. Biomol. Chem. 4 (2006), 257–267.
53. [53] Muller, K., Korth, H.-G., De Groot, H., Priv-Doz, M.K., Reaction of Vitamin E compounds with N-nitrosated tryptophan derivatives and its analytical use. Chem. Eur. J. 13 (2007), 7532–7542.
54. [54] Kopczak, A., Korth, H.-G., De Groot, H., Kirsch, M., N-nitrosomelatonin releases nitric oxide in the presence of serotonin and its derivatives. J. Pineal Res. 43 (2007), 343–350.
55. [55] Arita, N.O., Cohen, M.F., Tokuda, G., Yamasaki, H., Fluorometric detection of nitric oxide with diaminofluoresceins (DAFs): applications and limitations for plant NO research. Plant Cell Monogr. 5 (2006), 269–280.
56. [56] Singh, N., Kaur, H., Yadav, S., Bhatla, S.C., Does N-Nitrosomelatonin compete with S-Nitrosothiols as a long distance nitric oxide carrier in plants?. Biochem. Anal. Biochem., 5, 2016, 10.4172/2161–1009.1000262.
57. [57] Becker, K., Savvides, S.N., Keese, M., Schirmer, R.H., Karplus, P.A., Enzyme inactivation through sulfhydryl oxidation by physiologic NO-carriers. Nat. Struct. Biol. 5 (1998), 267–271.
58. [58] Mayo, J.C., Sainz, R.M., Antolína, I., Herreraa, F., Martina, V., Rodriguez, C., Melatonin regulation of antioxidant enzyme gene expression. Cell. Mol. Life Sci. 59 (2002), 1706–1713.