Oxidative Stress and Salt Tolerance in Plants

  • Cai-Hong Pang
  • Bao-Shan Wang
Part of the Progress in Botany book series (BOTANY, volume 69)

Salt stress can induce ionic stress and osmotic stress in plant cells. A direct result of these primary effects is the enhanced accumulation of reactive oxygen species (ROS) that are harmful to plant cells at high concentrations. To cope with the oxidative stress resulting from the ROS, higher plants have developed a complex scavenging system including enzymatic and non-enzymatic (antioxidants) system. In plant cells, specific ROS producing and scavenging systems are found in different organelles such as chloroplasts, mitochondria, and peroxisomes; and the ROS-scavenging pathways from different cellular compartments are coordinated. Relatively low levels of ROS can be used for signaling molecules to control abiotic stress responses. Coordinated work of ROS-scavenging pathways from different cellular compartments in modulating the level of ROS in cells preventing cellular damage and controlling ROS signaling may play a key role in plant salt tolerance. Here we attempt to summarize the recent researches on ROS and the mechanism of salt tolerance of plants under salt stress, and we also propose some perspectives involved in ROS and plant salt tolerances in the future.


Salt Stress Salt Tolerance Plant Mitochondrion Scavenge System Plant Salt Tolerance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–99.CrossRefPubMedGoogle Scholar
  2. Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639.CrossRefPubMedGoogle Scholar
  3. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287.Google Scholar
  4. Avsian-Kretchmer O, Gueta-Dahan Y, Lev-Yadun S, Gollop R, Ben-Hayyim G (2004) The salt-stress signal transduction pathway that activates the gpx1 promoter is mediated by intra-cellular H2O2, different from the pathway induced by extracellular H2O2. Plant Physiol 135:1685–1696.CrossRefPubMedGoogle Scholar
  5. Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004) Overexpression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121:231–238.CrossRefPubMedGoogle Scholar
  6. Baker A, Graham I (2002) Plant peroxisomes. Biochemistry, cell biology and biotechnological applications. Kluwer, Dordrecht.Google Scholar
  7. Beyer R (1991) An analysis of the role of coenzyme Q in free radical generation and as an anti-oxidant. Biochem Cell Biol 70:390–343.CrossRefGoogle Scholar
  8. Bolwell GP, Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence–broad perspective. Physiol Mol Plant Pathol 51:347–366.CrossRefGoogle Scholar
  9. Boveris A, Chance B (1977) Mitochondrial production of superoxide radical and hydrogen peroxide. In: Reivich M, Coburn R, Lahiri S, Chance B (eds) Tissue hypoxia and ischemia. Plenum, New York, pp 67–82.Google Scholar
  10. Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723–1732.PubMedGoogle Scholar
  11. Buettner GR, Jurkiewicz BA (1996) Chemistry and biochemistry of ascorbic acid. In: Cadenas E, Packer L (eds) Handbook of antioxidants. Dekker, New York, pp 91–115.Google Scholar
  12. Castillo FJ, Greppin H (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. after ozone exposure. Environ Exp Bot 28:231–238.CrossRefGoogle Scholar
  13. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate–glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877.CrossRefPubMedGoogle Scholar
  14. Corpas FJ, Pedrajas JR, Sandalio LM, León AM, Carreras A, Palma JM, Valderrama R, Río LA del, Barroso JB (2003) Localization of peroxiredoxin in peroxisomes from pea leaves. Free Radical Res 37[Suppl 2]:19.CrossRefGoogle Scholar
  15. Dat J, Vandenabeele S, Vranová E, Montagu MV, Inzé D, Breusegem FV (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795.CrossRefPubMedGoogle Scholar
  16. Davletova S, Rizhsky L, Liang HJ, Zhong SQ, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281.CrossRefPubMedGoogle Scholar
  17. Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107.CrossRefPubMedGoogle Scholar
  18. Elstner EF, Oßwald W (1994) Mechanisms of oxygen activation during plant stress. Proc R Soc Edin B 102:131–154.Google Scholar
  19. Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants. Where next? Aust J Plant Physiol 22:875–884.CrossRefGoogle Scholar
  20. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254.CrossRefPubMedGoogle Scholar
  21. Gómez JM, Hernández JA, Jiménez A, Río LA del, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplast and mitochondria to long term NaCl stress of pea plants. Free Radical Res 31:S11–S18.CrossRefGoogle Scholar
  22. Grene R (2002) Oxidative stress and acclimation mechanisms in plants. In: Somerville CR, Myerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville. Available at:
  23. Gupta R, Luan S (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132:1149–1152.CrossRefPubMedGoogle Scholar
  24. Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, Oxford.Google Scholar
  25. Hernández JA, Corpas FJ, Gómez M, Río LA del, Sevilla F (1993) Salt induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol Plant 89:103–110.CrossRefGoogle Scholar
  26. Hernández JA, Jiménez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862.CrossRefGoogle Scholar
  27. Hernández JA, Ferrer MA, Jiménez A, Barcelo AR, Sevilla F (2001) Antioxidant systems and O2 ?/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831.CrossRefPubMedGoogle Scholar
  28. Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43:1154–1164.CrossRefPubMedGoogle Scholar
  29. Hourton-Cabassa C, Matos AR, Zachowski A, Moreau F (2004) The plant uncoupling protein homologues: a new family of energy-dissipating proteins in plant mitochondria. Plant Physiol Biochem 42:283–290.CrossRefPubMedGoogle Scholar
  30. Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu GH (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133:170–181.CrossRefPubMedGoogle Scholar
  31. Ichimura K, Mizoguchi T, Irie K, Morris P, Giraudat J, Matsumoto K, Shinozaki K (1998) Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem Biophys Res Commun 253:532–543.CrossRefPubMedGoogle Scholar
  32. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24:655–665.CrossRefPubMedGoogle Scholar
  33. Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309.CrossRefPubMedGoogle Scholar
  34. Jiménez A, Hernández JA, Río LA del, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284.PubMedGoogle Scholar
  35. Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650.CrossRefPubMedGoogle Scholar
  36. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945.CrossRefPubMedGoogle Scholar
  37. Krasnovsky AA Jr (1998) Singlet molecular oxygen in photobiochemical systems: IR phosphorescence studies. Membr Cell Biol 12:665–690.PubMedGoogle Scholar
  38. Kurepa J, Hérouart D, Van Montagu M, Inzé D (1997) Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress and hormonal treatments. Plant Cell Physiol 38:463–470.PubMedGoogle Scholar
  39. Kuniak E, Skodowska M (2005) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222:192–200.CrossRefGoogle Scholar
  40. Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, Allen RD, Kwak SS (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant Cell Environ 25:873–882.CrossRefGoogle Scholar
  41. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593.CrossRefPubMedGoogle Scholar
  42. López-Huertas E, Corpas FJ, Sandalio LM, Río LA del (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536.CrossRefPubMedGoogle Scholar
  43. Luwe M (1996) Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentration in air. Plant Cell Environ 19:321–328.CrossRefGoogle Scholar
  44. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276.CrossRefPubMedGoogle Scholar
  45. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410.CrossRefPubMedGoogle Scholar
  46. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498.CrossRefPubMedGoogle Scholar
  47. 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. Plant Cell Environ 26:845–85 6.CrossRefPubMedGoogle Scholar
  48. 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.Google Scholar
  49. Miyagawa Y, Tamoi M, Shigeoka S (2000) Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol 41:311–320.Google Scholar
  50. Miyake C, Asada K (1994) Ferredoxin-dependent photoreduction of monodehydroascorbate radicals in spinach thylakoids. Plant Cell Physiol 35:539–549.Google Scholar
  51. Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 93:765–769.CrossRefPubMedGoogle Scholar
  52. Murgia I, Tarantino D, Vannini C, Bracale M, Carrabvieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–995.CrossRefPubMedGoogle Scholar
  53. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591.CrossRefPubMedGoogle Scholar
  54. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346.CrossRefPubMedGoogle Scholar
  55. Pang CH, Zhang SJ, Gong ZZ, Wang BS (2005) NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa. Physiol Plant 125:490–499.Google Scholar
  56. Polle A, Chakrabarti K, Schümann W, Rennenberg H (1990) Composition and properties of hydrogen peroxide decomposing systems in extracellular and total extracts from needles of Norway Spruce (Picea abies L., Karst.). Plant Physiol 94:312–319.CrossRefPubMedGoogle Scholar
  57. Popov VN, Simonina RA, Skulachev VP, Starkov AA (1997) Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria. FEBS Lett 415:87–90.CrossRefPubMedGoogle Scholar
  58. Puntarulo S, Sánchez RA, Boveris A (1988) Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiol 86:626–630.CrossRefPubMedGoogle Scholar
  59. Purvis AC (1997) Role of the alternative oxidase in limiting superoxide production in plant mitochondria. Physiol Plant 100:165–170.CrossRefGoogle Scholar
  60. Purvis AC, Shewfelt RL (1993) Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiol Plant 88:712–718.CrossRefGoogle Scholar
  61. Raha S, Robinson BH (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25:502–508.CrossRefPubMedGoogle Scholar
  62. Reumann S, Bettermann M, Benz R, Heldt HW (1997) Evidence for the presence of a porin in the membrane of glyoxysomes of castor bean. Plant Physiol 115:891–899.PubMedGoogle Scholar
  63. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366.CrossRefPubMedGoogle Scholar
  64. Río LA del, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200.CrossRefPubMedGoogle Scholar
  65. Río LA del, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272.CrossRefPubMedGoogle Scholar
  66. Río LA del, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335.CrossRefPubMedGoogle Scholar
  67. Scandalios JC (1993) Oxygen stress and superoxide dismutases. Plant Physiol 101:7–12.PubMedGoogle Scholar
  68. Sluse FE, Jarmuszkiewicz W (2004) Regulation of electron transport in the respiratory chain of plant mitochondria. In: Day DA, Millar AH, Whelan J (eds) Plant mitochondria: from genome to function, vol 1. (Advances in photosynthesis and respiration) Kluwer, Dordrecht, pp 229–245.Google Scholar
  69. Smirnoff N (1993) The role of active oxygen in response of plants to water deficit and desiccation. New Phytol 125:27–58.CrossRefGoogle Scholar
  70. Sweetlove LJ, Foyer CH (2004) Roles for reactive oxygen species and antioxidants in plantmitochondria. In: Day DA, Millar AH, Whelan J (eds) Plant mitochondria: from genome to function, vol 1. (Advances in photosynthesis and respiration) Kluwer, Dordrecht, pp 307–320.Google Scholar
  71. Takeshiga K, Minakami S (1979) NADH and NADPH dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparation. Biochem J 180:129–135.Google Scholar
  72. Tarantino D, Vannini C, Bracale M, Camp M, Soave C, Murgia I (2005) Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances paraquat-induced photooxidative stress and nitric oxide induced cell death. Planta 221:757–765.CrossRefPubMedGoogle Scholar
  73. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152.CrossRefPubMedGoogle Scholar
  74. Vanacker H, Carver TLW, Foyer CH (1998a) Pathogen induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114.CrossRefPubMedGoogle Scholar
  75. Vanacker H, Harbinson J, Carver TLW, Foyer CH (1998b) Antioxidant defenses of the apoplast. Protoplasma 205:129–140.CrossRefGoogle Scholar
  76. Wang BS, Lüttge U, Ratajczak R (2004) Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L. J Plant Physiol 161:285–293.CrossRefPubMedGoogle Scholar
  77. Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40:725–732.PubMedGoogle Scholar
  78. Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107.CrossRefPubMedGoogle Scholar
  79. Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816.CrossRefPubMedGoogle Scholar
  80. Yabuta Y, Motoki T, Yoshimura K, Takada T, Ishikawa T, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J 32:912–925.CrossRefGoogle Scholar
  81. Zhang QF, Li YY, Pang CH, Lu CM, Wang BS (2005) NaCl enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L. Plant Sci 168:423–430.CrossRefGoogle Scholar
  82. Zhu D, Scandalios JG (1992) Expression of the maize MnSod (Sod3) gene in MnSOD-deficient yeast rescues the mutant yeast under oxidative stress. Genetics 131:803–809.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Cai-Hong Pang
    • 1
  • Bao-Shan Wang
    • 1
  1. 1.College of Life SciencesShandong Normal UniversityShandong ProvincePR China

Personalised recommendations