Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 103, Issue 2, pp 205–215 | Cite as

Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars

  • Jian Sun
  • Lisi Li
  • Meiqin Liu
  • Meijuan Wang
  • Mingquan Ding
  • Shurong Deng
  • Cunfu Lu
  • Xiaoyang Zhou
  • Xin Shen
  • Xiaojiang Zheng
  • Shaoliang Chen
Original Paper

Abstract

Using callus cells of a salt-tolerant Populus euphratica Oliver and a salt-sensitive P. popularis 35–44 (P. popularis), the effects of NaCl stress on hydrogen peroxide (H2O2) and nitric oxide (NO) production and the relevance to ionic homeostasis and antioxidant defense were investigated. Results show that P. euphratica exhibited a greater capacity to tolerate NaCl stress in terms of cell viability, membrane permeability and K+/Na+ relations. NaCl salinity (150 mM) caused a rapid increase of H2O2 and NO in P. euphratica cells, but not in P. popularis. Moreover, salinised P. euphratica cells retained a high and stable level of H2O2 and NO during the period of 24-h salt stress. Noteworthy, P. eupratica cells increased activities of superoxide dismutase, ascorbate peroxidase, catalase and glutathione reductase under salinity stress, but these antioxidant enzymes were significantly inhibited by the salt treatment in P. popularis cells. Pharmacological experiments proved that the NaCl-induced H2O2 and NO was interdependent and contributed to the mediation of K+/Na+ homeostasis and antioxidant defense in P. euphratica cells. Given these results, we conclude that the increased H2O2 and NO enable P. euphratica cells to regulate ionic and ROS (reactive oxygen species) homeostasis under salinity stress in the longer term.

Keywords

Salt tolerance Populus euphratica Populus popularis X-ray microanalysis Antioxidant enzymes Confocal microscopy 

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefPubMedGoogle Scholar
  2. Apse MP, Aharon GS, Sneddon WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiporter in Arobidopsis. Science 285:1256–1258CrossRefPubMedGoogle Scholar
  3. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochem 72:248–254CrossRefGoogle Scholar
  4. Chen S, Polle A (2010) Salinity tolerance of Populus. Plant Biol 12:317–333CrossRefPubMedGoogle Scholar
  5. Chen S, Fritz E, Wang S, Hüttermann A, Liu Q, Jiang X (2000) Cellular distribution of ions in salt-stressed cells of Populus euphratica and Populus tomentosa. For Stud China 2:8–16Google Scholar
  6. Chen S, Li J, Fritz E, Wang S, Hüttermann A (2002) Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. For Ecol Manage 168:217–230CrossRefGoogle Scholar
  7. Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565CrossRefPubMedGoogle Scholar
  8. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875CrossRefPubMedGoogle Scholar
  9. Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochica H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146–159CrossRefPubMedGoogle Scholar
  10. Giannopolits CN, Ries SK (1977) Superoxide dismutases: occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  11. Hernandez M, Fernandez-Garcia N, Diaz-Vivancos P, Olmos E (2010) A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots. J Exp Bot 61:521–535CrossRefPubMedGoogle Scholar
  12. Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410CrossRefPubMedGoogle Scholar
  13. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:566–589CrossRefGoogle Scholar
  14. Mittova V, Tal M, Volokita M, Guy M (2003) 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 26:845–856CrossRefPubMedGoogle Scholar
  15. Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann Rev Plant Physiol Plant Mol Biol 52:561–591CrossRefGoogle Scholar
  16. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  17. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  18. 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 59:165–176CrossRefPubMedGoogle Scholar
  19. Orton TJ (1980) Comparison of salt tolerance between Hordeum v ulgare and H. jubatum in whole plants and callus cultures. Z Pflanzenphysiol 98:105–118Google Scholar
  20. Ottow EA, Polle A, Brosché M, Kangasjärvi J, Dibrov P, Zörb C, Teichmann T (2005) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:73–86CrossRefGoogle Scholar
  21. Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246CrossRefPubMedGoogle Scholar
  22. Qiao W, Xiao S, Yu L, Fan LM (2009) Expression of a rice gene OsNOA1 re-establishes nitric oxide synthesis and stress-related gene expression for salt tolerance in Arabidopsis nitric oxide-associated 1 mutant Atnoa1. Environ Exp Bot 65:90–98CrossRefGoogle Scholar
  23. Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012CrossRefPubMedGoogle Scholar
  24. Shabala S, Cuin TA (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:651–669CrossRefPubMedGoogle Scholar
  25. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 99:8436–8441Google Scholar
  26. Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85CrossRefPubMedGoogle Scholar
  27. Shi QH, Fei Ding, Wang XF, Wei M (2007) Exogenous nitric oxide pretect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550CrossRefPubMedGoogle Scholar
  28. Silva P, Facanha AR, Tavares RM, Geros H (2010) Role of tonoplast proton pumps and Na+/H+ antiport system in salt tolerance of Populus euphratica Oliv. J Plant Growth Regul 29:23–34CrossRefGoogle Scholar
  29. Smith MK, McComb JA (1981) Effects of NaCl on the growth of whole plants and their corresponding callus culture. Aust J Plant Physiol 8:267–275CrossRefGoogle Scholar
  30. Sun J, Chen S, Dai S, Wang R, Li N, Shen X, Zhou X, Lu C, Zheng X, Hu Z, Zhang Z, Song J, Xu Y (2009a) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar sepecies. Plant Physiol 149:1141–1153CrossRefPubMedGoogle Scholar
  31. Sun J, Dai S, Wang R, Chen S, Li N, Zhou X, Lu C, Shen X, Zheng X, Hu Z, Zhang Z, Song J, Xu Y (2009b) Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiol 29:1175–1186CrossRefPubMedGoogle Scholar
  32. Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ, Lu CF, Zhou XY, Shen X, Zheng XJ, Zhang ZK, Song J, Hu ZM, Xu Y, Chen SL (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958CrossRefPubMedGoogle Scholar
  33. Tanou G, Molassiotis A, Diamantidis G (2009) Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913CrossRefPubMedGoogle Scholar
  34. Wang R, Chen S, Deng L, Fritz E, Hüttermann A, Polle A (2007) Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees 21:581–591CrossRefGoogle Scholar
  35. Wang R, Chen S, Zhou X, Shen X, Deng L, Zhu H, Shao J, Shi Y, Dai S, Fritz E, Hüttermann A, Polle A (2008) Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol 28:947–957PubMedGoogle Scholar
  36. Wang HH, Liang XL, Wan Q, Wan Q, Wang XM, Bi YR (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307CrossRefPubMedGoogle Scholar
  37. Warren RS, Gould AR (1982) Salt tolerance expressed as a cellular trait in suspension cultures developed from the halophytic grass Distichlis spicata. Z. Pflanzenphysiol 107:347–356Google Scholar
  38. Wu Y, Ding N, Zhao X, Zhao M, Chang Z, Liu J, Zhang L (2007) Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Mol Biol 65:1–11CrossRefPubMedGoogle Scholar
  39. Xie Y, Ling T, Han Y, Liu K, Zheng Q, Huang L, Yuan X, He Z, Hu B, Fang L, Shen Z, Yang Q, Shen W (2008) Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant Cell Environ 31:1864–1881CrossRefPubMedGoogle Scholar
  40. 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
  41. Yang Y, Zhang F, Zhao M, An L, Zhang L, Chen N (2007) Properties of plasma membrane H+-ATPase in salt-treated Populus euphratica callus. Plant Cell Rep 26:229–235CrossRefPubMedGoogle Scholar
  42. Zhang YY, Wang LL, Liu YL, Zhang Q, Wei QP, Zhang WH (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555CrossRefPubMedGoogle Scholar
  43. Zhang F, Wang Y, Yang YL, Wu H, Wang D, Liu JQ (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785CrossRefPubMedGoogle Scholar
  44. Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857CrossRefPubMedGoogle Scholar
  45. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217CrossRefPubMedGoogle Scholar
  46. Zheng CF, Jiang D, Liu FL, Dai TB, Liu WC, Jing Q, Cao WX (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67:222–227CrossRefGoogle Scholar
  47. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar
  48. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:1–5CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Jian Sun
    • 1
  • Lisi Li
    • 1
  • Meiqin Liu
    • 1
  • Meijuan Wang
    • 1
  • Mingquan Ding
    • 1
  • Shurong Deng
    • 1
  • Cunfu Lu
    • 1
  • Xiaoyang Zhou
    • 1
  • Xin Shen
    • 1
  • Xiaojiang Zheng
    • 2
  • Shaoliang Chen
    • 1
    • 2
  1. 1.National Engineering Laboratory for Tree Breeding, College of Biological Sciences and TechnologyBeijing Forestry UniversityBeijingPeople’s Republic of China
  2. 2.Key Laboratory of Biological Resources Protection and Utilization in Hubei ProvinceHubei University for NationalitiesEnshiPeople’s Republic of China

Personalised recommendations