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Plant Growth Regulation

, Volume 77, Issue 3, pp 265–277 | Cite as

Nitric oxide mediates hydrogen peroxide- and salicylic acid-induced salt tolerance in rice (Oryza sativa L.) seedlings

  • Mohammad Golam Mostofa
  • Masayuki Fujita
  • Lam-Son Phan Tran
Original paper

Abstract

Nitric oxide (NO), hydrogen peroxide (H2O2), and salicylic acid (SA) are well-known signaling molecules that play multifaceted roles in the stress tolerance of plants; however, their interactions during stress alleviation have not been well studied. We investigated the possible regulatory role of NO in H2O2- and SA-induced reduction of oxidative damage in salt-exposed rice seedlings. For this purpose, hydroponically grown 14-day-old seedlings were pretreated with 100 μM H2O2 or 100 μM SA in the presence or absence of 100 μM hemoglobin (Hb, a potent NO scavenger) for 24 h followed by salt stress (200 mM NaCl) for 72 h. Salt stress significantly increased the levels of H2O2, malondialdehyde, and proline whereas H2O2 and SA pretreatment reduced the values of these parameters. H2O2 and SA pretreatment also inhibited salt-induced loss of total chlorophyll and relative water content. Histochemical detection of reactive oxygen species [ROS: superoxide (O 2 ·− ) and H2O2] indicated evident oxidative burst in the seedlings stressed with salt alone. Salt stress modulated the non-enzymatic and enzymatic antioxidants differentially; however, H2O2 and SA treatment prior to salt stress enhanced these antioxidants compared with the salt-stressed seedlings alone. H2O2 and SA pretreated salt-stressed seedlings also showed higher induction of the methylglyoxal (MG) detoxification system. Endogenous NO content was elevated following H2O2 and SA pretreatment over the experimental period. Adding Hb reduced the level of NO and subsequently abolished the beneficial effects of H2O2 and SA. Our results, therefore, suggest that NO might be involved in H2O2- and SA-induced reduction of oxidative damage through the upregulation of the antioxidant defense and MG detoxification systems to confer salt tolerance in rice seedlings. The data are of considerable value in elucidating the biochemical mechanisms of salt-stress tolerance and will augment the goal of developing appropriate and efficient methods for crop protection in saline environment.

Keywords

Salinity Oxidative stress Hydrogen peroxide Salicylic acid Antioxidant system Glyoxalase Nitric oxide Salt tolerance Plant hormone signaling 

Notes

Acknowledgments

M. G. Mostofa gratefully acknowledges the funding from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10725_2015_61_MOESM1_ESM.pdf (200 kb)
Supplementary material 1 (PDF 199 kb)

References

  1. Álvarez Viveros MF, Inostroza-Blancheteau C, Timmermann T, González M, Arce-Johnson P (2013) Overexpression of Gly I and Gly II genes in transgenic tomato (Solanum lycopersicum Mill.) plants confers salt tolerance by decreasing oxidative stress. Mol Biol Rep 40:3281–3290CrossRefPubMedGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefPubMedGoogle Scholar
  3. Arnon DT (1949) Copper enzymes in isolated chloroplast polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedCentralCrossRefPubMedGoogle Scholar
  4. Ashfaque F, Khan MIR, Khan NA (2014) Exogenously applied H2O2 promotes proline accumulation, water relations, photosynthetic efficiency and growth of wheat (Triticum aestivum L.) under salt stress. Annu Res Rev Biol 4:105–120CrossRefGoogle Scholar
  5. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  6. 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 72:248–254CrossRefPubMedGoogle Scholar
  7. Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131:264–275PubMedCentralCrossRefPubMedGoogle Scholar
  8. Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167CrossRefPubMedGoogle Scholar
  9. 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 245:85–96CrossRefPubMedGoogle Scholar
  10. Esim N, Atici O (2014) Nitric oxide improves chilling tolerance of maize by affecting apoplastic antioxidative enzymes in leaves. Plant Growth Regul 72:29–38CrossRefGoogle Scholar
  11. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefPubMedGoogle Scholar
  12. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle Scholar
  13. Griffiths OW (1980) Determination of glutathione and glutathione disulphide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212CrossRefGoogle Scholar
  14. Han Y, Yin S, Huang L (2014) Towards plant salinity tolerance-implications from ion transporters and biochemical regulation. Plant Growth Regul. doi: 10.1007/s10725-014-9997-6 Google Scholar
  15. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefGoogle Scholar
  16. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stochiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  17. Hossain MA, Fujita M (2013) Hydrogen Peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.) seedlings. Plant Gene Trait 4:109–123Google Scholar
  18. 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 25:385–395Google Scholar
  19. 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 3:53–64Google Scholar
  20. Hossain MA, Ismail MR, Uddin MK, Islam MZ, Ashrafuzzaman M (2013a) Efficacy of ascorbate–glutathione cycle for scavenging H2O2 in two contrasting rice genotypes during salinity stress. Aust J Crop Sci 7:1801–1808Google Scholar
  21. Hossain MA, Mostofa MG, Fujita M (2013b) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70Google Scholar
  22. Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42CrossRefGoogle Scholar
  23. Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regul. doi: 10.1007/s10725-015-0028-z Google Scholar
  24. Kaur C, Ghosh A, Pareek A, Sopory SK, Singla-Pareek SL (2014) Glyoxalases and stress tolerance in plants. Biochem Soc Trans 42:485–490CrossRefPubMedGoogle Scholar
  25. Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27:210–218CrossRefPubMedGoogle Scholar
  26. Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74CrossRefPubMedGoogle Scholar
  27. Khare T, Kumar V, Kishor PBK (2014) Na+ and Cl− ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma. doi: 10.1007/s00709-014-0749-2 PubMedGoogle Scholar
  28. Klessig DF et al (2000) Nitric oxide and salicylic acid signaling in plant defense. PNAS 97:8849–8855PubMedCentralCrossRefPubMedGoogle Scholar
  29. 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 250:1079–1089CrossRefPubMedGoogle Scholar
  30. Lee MH, Cho EJ, Wi SG, Bae H, Kim JE, Cho JY, Lee S, Kim JH, Chung BY (2013) Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress. Plant Physiol Biochem 70:325–335CrossRefPubMedGoogle Scholar
  31. Li J-T, Qiu Z-B, Zhang X-W, Wang L-S (2011) Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress. Acta Physiol Plant 33:835–842CrossRefGoogle Scholar
  32. Lin Y, Liu Z, Shi Q, Wang X, Wei M, Yang F (2012) Exogenous nitric oxide (NO) increased antioxidant capacity of cucumber hypocotyl and radicle under salt stress. Sci Hortic 142:118–127CrossRefGoogle Scholar
  33. Liu S, Dong Y, Xu L, Kong J (2014) Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul 73:67–78CrossRefGoogle Scholar
  34. Lopez-Carrion AI, Castellano R, Rosales MA, Ruiz JM, Romero L (2008) Role of nitric oxide under saline stress: implications on proline metabolism. Biol Plant 52:587–591CrossRefGoogle Scholar
  35. Mishra P, Bhoomika K, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250:3–19CrossRefPubMedGoogle Scholar
  36. Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4PubMedCentralCrossRefPubMedGoogle Scholar
  37. Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973CrossRefPubMedGoogle Scholar
  38. Mostofa MG, Seraj ZI, Fujita M (2014a) Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings. Protoplasma 251:1373–1386CrossRefPubMedGoogle Scholar
  39. Mostofa MG, Yoshida N, Fujita M (2014b) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul 73:31–44CrossRefGoogle Scholar
  40. Mostofa MG, Hossain MA, Fujita M (2015) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252:461–475CrossRefPubMedGoogle Scholar
  41. Mustafiz A et al (2014) A unique Ni2+-dependent and methylglyoxal-inducible rice glyoxalase I possesses a single active site and functions in abiotic stress response. Plant J 78:951–963CrossRefPubMedGoogle Scholar
  42. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  43. Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815CrossRefPubMedGoogle Scholar
  44. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:65–176CrossRefGoogle Scholar
  45. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants. doi: 10.1093/aobpla/pls014 PubMedCentralPubMedGoogle Scholar
  46. Qiao WH, Li CN, Fan LM (2014) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:84–93CrossRefGoogle Scholar
  47. 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 41:1229–1234CrossRefPubMedGoogle Scholar
  48. Saito N, Nakamura Y, Mori IC, Murata Y (2009) Nitric oxide functions in both methyl jasmonate signaling and abscisic acid signaling in Arabidopsis guard cells. Plant Signal Behav 4:119–120PubMedCentralCrossRefPubMedGoogle Scholar
  49. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2008) Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Transgenic Res 17:171–180CrossRefPubMedGoogle Scholar
  50. Song F, Goodman RM (2001) Activity of nitric oxide is dependent on, but is particularly required for function of salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol Plant-Microbe Int 14:1458–1462CrossRefGoogle Scholar
  51. Sun LR, Hao FS, Lu BS, Ma LY (2010) AtNOA1 modulates nitric oxide accumulation and stomatal closure induced by salicylic acid in Arabidopsis. Plant Signal Behav 5:1022–1024PubMedCentralCrossRefPubMedGoogle Scholar
  52. Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599CrossRefPubMedGoogle Scholar
  53. Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9CrossRefGoogle Scholar
  54. Uchida A, Jagendorf AT, Hibino T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523CrossRefGoogle Scholar
  55. 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 33:2297–2307CrossRefPubMedGoogle Scholar
  56. Wang W, Vinocur B, Altman A (2007) Plant responses to drought, salinity and extreme temperatures towards genetic engineering for stress tolerance. Planta 218:1–14CrossRefGoogle Scholar
  57. Xu Q, Xu X, Zhao Y, Jiao K, Herbert SJ, Hao L (2008) Salicylic acid, hydrogen peroxide and calcium-induced saline tolerance associated with endogenous hydrogen peroxide homeostasis in naked oat seedlings. Plant Growth Regul 54:249–259CrossRefGoogle Scholar
  58. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. Fed Eur Biochem Soc Lett 579:6265–6271CrossRefGoogle Scholar
  59. Younis ME, Hasaneen MNA, Kazamel AMS (2010) Exogenously applied ascorbic acid ameliorates detrimental effects of NaCl and mannitol stress in Vicia faba seedlings. Protoplasma 239:39–48CrossRefPubMedGoogle Scholar
  60. Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50CrossRefPubMedGoogle Scholar
  61. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217PubMedCentralCrossRefPubMedGoogle Scholar
  62. Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228CrossRefPubMedGoogle Scholar
  63. Zottini M, Costa A, Michele RD, Ruzzene M, Carimi F, Schiavo FL (2007) Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot 58:1397–1405CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of AgricultureKagawa UniversityMikiJapan
  2. 2.Department of Biochemistry and Molecular BiologyBangabandhu Shiekh Mujibur Rahman Agricultural UniversityGazipurBangladesh
  3. 3.Signaling Pathway Research UnitRIKEN Center for Sustainable Resource ScienceYokohamaJapan

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