Detoxification of Active Oxygen Species and Tolerance in Plants Exposed to Air Pollutants and CO2

  • Shigeto Morita
  • Kunisuke Tanaka


With the increasing the combustion of fossil fuels, the ambient levels of air pollutants and carbon dioxide (CO2) have been steadily increasing. Air pollutants, ozone, and sulfur dioxide (SO2) are known to have damaging effects on plants. Ozone and SO2 cause visible foliar damages at high concentrations and inhibition of photosynthesis at lower concentrations (Schraudner et al. 1996; Tanaka 1994). Because the damages caused by these pollutants are dependent on oxygen, it has been proposed that active oxygen species (AOS) are involved in the toxicity of the pollutants (Tanaka 1994). Elevations in CO2 level are also of concern because they have various effects on plants directly and can also affect vegetation through climate changes. CO2 has been shown to affect the growth, photosynthesis, and yield of plants (Murray 1997) and even to affect plant stress sensitivity by influencing their antioxidative defense systems (see Section 4 of this chapter).


Active Oxygen Species Ozone Fumigation Ozone Injury Cytosolic Ascorbate Peroxidase Pathogen Defense Response 
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. Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radical Biol Med 23: 473–479CrossRefGoogle Scholar
  2. Aono M, Kubo A, Saji H, Tanaka K, Kondo N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell Physiol 34: 129–135Google Scholar
  3. Arisi A-CM, Cornic G, Jouanin L, Foyer CH (1998) Overexpression of iron superoxide dismutase in transformed poplar modifies the regulation of photosynthesis at low CO2 partial pressures or following exposure to the prooxidant herbicide methyl viologen. Plant Physiol 117: 565–574PubMedCrossRefGoogle Scholar
  4. Asada K (1997) The role of ascorbate peroxidase and monodehydroascorbate reductase in H2O2 scavenging in plants. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 715–735Google Scholar
  5. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601–639PubMedCrossRefGoogle Scholar
  6. Badiani M, Schenone G, Paolacci AR, Fumagalli I (1993) Daily fluctuations of antioxidants in bean ( Phaseolus vulgaris L.) leaves as affected by the presence of ambient air pollutants. Plant Cell Physiol 34: 271–279Google Scholar
  7. Beeor-Tzahar T, Ben-Hayyim G, Holland D, Faltin Z, Eshdat Y (1995) A stress-associated citrus protein is a distinct plant phospholipid hydroperoxide glutathione peroxidase. FEBS Lett 366: 151–155PubMedCrossRefGoogle Scholar
  8. Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43: 83–116CrossRefGoogle Scholar
  9. Broadbent P, Creissen GP, Kular B, Wellburn AR, Mullineaux PM (1995) Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J 8: 247–255CrossRefGoogle Scholar
  10. Conklin PL, Last RL (1995) Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109: 203–212PubMedCrossRefGoogle Scholar
  11. Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93: 9970–9974PubMedCrossRefGoogle Scholar
  12. Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116: 1351–1357PubMedCrossRefGoogle Scholar
  13. Edwards EA, Enard C, Creissen GP, Mullineaux PM (1994) Synthesis and properties of glutathione reductase in stressed peas. Planta 192: 137–143Google Scholar
  14. Foyer CH (1997) Oxygen metabolism and electron transport in photosynthesis. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 587–621Google Scholar
  15. Grimes HD, Perkins KK, Boss WF (1983) Ozone degrades into hydroxyl radical under physiological conditions. Plant Physiol 72: 1016–1020PubMedCrossRefGoogle Scholar
  16. Himelblau E, Mira H, Lin S-J, Culotta VC, Penarrubia L, Amasino RM (1998) Identification of a functional homolog of the yeast copper homeostasis gtmATXl from Arabidopsis. Plant Physiol 117: 1227–1234PubMedCrossRefGoogle Scholar
  17. Jabs T, Dietrich RA, Dangl JL (1996) initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273: 1853–1856Google Scholar
  18. Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea ( Pisum sativum L.) leaves. Plant Physiol 114: 275–284PubMedGoogle Scholar
  19. Kliebenstein DJ, Monde R-A, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118: 637–650PubMedCrossRefGoogle Scholar
  20. Kubo A, Saji H, Tanaka K, Kondo N (1995) Expression of arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Mol Biol 29: 479–489PubMedCrossRefGoogle Scholar
  21. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275PubMedCrossRefGoogle Scholar
  22. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H202 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593PubMedCrossRefGoogle Scholar
  23. Madamanchi NR, Alscher RG (1991) Metabolic bases for differences in sensitivity of two pea cultivars to sulfur dioxide. Plant Physiol 97: 88–93PubMedCrossRefGoogle Scholar
  24. Madamanchi NR, Donahue JL, Cramer CL, Alscher RG, Pedersen K (1994) Differential response of Cu,Zn superoxide dismutases in two pea cultivars during a short-term exposure to sulfur dioxide. Plant Mol Biol 26: 95–103PubMedCrossRefGoogle Scholar
  25. Marrs KA (1996) The functions and regulation of glutathione S-transferase. Annu Rev Plant Physiol Plant Mol Biol 47: 127–158PubMedCrossRefGoogle Scholar
  26. Mehlhorn H (1990) Ethylene-promoted ascorbate peroxidase activity protects against hydrogen peroxide, ozone and paraquat. Plant Cell Environ 13: 971–976CrossRefGoogle Scholar
  27. Mehlhorn H, Tabner BJ, Wellburn AR (1990) Electron spin resonance evidence for the formation of free radicals in plants exposed to ozone. Physiol Plant 79: 377–383CrossRefGoogle Scholar
  28. Morita S, Kaminaka H, Masumura T, Tanaka K (1999) Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; the involvement of hydrogen peroxide in oxidative stress signalling. Plant Cell Physiol 40: 417–422Google Scholar
  29. Murray DR (1997) Carbon dioxide and plant responses. Research Studies Press, Taunton, Somerset, EnglandGoogle Scholar
  30. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249–279PubMedCrossRefGoogle Scholar
  31. Ogawa K, Kanematsu S, Asada K (1996) Intra- and extra-cellular localization of “cytosolic” CuZn-superoxide dismutase in spinach leaf and hypocotyl. Plant Cell Physiol 37: 790–799Google Scholar
  32. Orvar BL, Ellis BE (1997) Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. Plant J 11: 1297–1305CrossRefGoogle Scholar
  33. Orvar BL, McPherson J, Ellis BE (1997) Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J 11: 203–212PubMedCrossRefGoogle Scholar
  34. Pasqualini S, Batini P, Ederli L, Antonielli M (1999) Reponses of the xanthophyll cycle pool and ascorbate-glutathione cycle to ozone stress in two tobacco cultivars. Free Radical Res 31: s67–s73CrossRefGoogle Scholar
  35. Pastori GM, Trippi VS (1992) Oxidative stress induces high rate of glutathione reductase synthesis in a drought-resistant maize strain. Plant Cell Physiol 33: 957–961Google Scholar
  36. Pellinen R, Palva T, Kangasjarvi J (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch ( Betula pendula) leaf cells. Plant J 20: 349–356PubMedCrossRefGoogle Scholar
  37. Pitcher LH, Zilinskas BA (1996) Overexpression of copper/zinc superoxide dismutase in the cytosol of transgenic tobacco confers partial resistance to ozone-induced foliar necrosis. Plant Physiol 110: 583–588PubMedGoogle Scholar
  38. Pitcher LH, Brennan E, Zilinskas BA (1992) The antiozonant ethylenediurea does not act via superoxide dismutase induction in bean. Plant Physiol 99: 1388–1392PubMedCrossRefGoogle Scholar
  39. Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6: 65–74PubMedCrossRefGoogle Scholar
  40. Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17: 603–614PubMedCrossRefGoogle Scholar
  41. Rao MV, Hale BA, Ormrod DP (1995) Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiol 109: 421–432PubMedGoogle Scholar
  42. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110: 125–136PubMedCrossRefGoogle Scholar
  43. Roeckner E (1992) Past, present and future levels of greenhouse gases in the atmosphere and model predictions of related climatic changes. J Exp Bot 43: 1097–1109CrossRefGoogle Scholar
  44. Sakaki T, Kondo N, Sugahara K (1983) Breakdown of photosynthetic pigments and lipids in spinach leaves with ozone fumigation: role of active oxygens. Physiol Plant 59: 28–34CrossRefGoogle Scholar
  45. Sandermann H Jr, Ernst D, Heller W, Langebartels C (1998) Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci 3: 47–50CrossRefGoogle Scholar
  46. Sandhu R, Li Y, Gupta G (1992) Sulphur dioxide and carbon dioxide induced changes in soybean physiology. Plant Sci 83: 31–34CrossRefGoogle Scholar
  47. Schraudner M, Langebartels C, Sandermann H Jr (1996) Plant defence systems and ozone. Biochem Soc Trans 24: 456–461PubMedGoogle Scholar
  48. Schraudner M, Moeder W, Wiese C, Van Camp W, Inze D, Langebartels C, Sandermann H Jr (1998) Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J 16: 235–245CrossRefGoogle Scholar
  49. Schwanz P, Picon C, Vivin P, Dreyer E, Guehl J-M, Polle A (1996) Response of antioxidative systems to drought stress in pendunculate oak and maritime pine as modulated by elevated CO2. Plant Physiol 110: 393–402PubMedGoogle Scholar
  50. Sen Gupta A, Alscher RG, McCune D (1991) Response of photosynthesis and cellular antioxidants to ozone in Populus leaves. Plant Physiol 96: 650–655PubMedCrossRefGoogle Scholar
  51. Sharma YK, Davis KR (1994) Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 105: 1089–1096Google Scholar
  52. Sharma YK, Leon J, Raskin I, Davis KR (1996) Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc Natl Acad Sci USA 93: 5099–5104PubMedCrossRefGoogle Scholar
  53. Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa K, Yokota A, Shigeoka S (1998) Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett 428: 47–51PubMedCrossRefGoogle Scholar
  54. Tanaka K (1994) Tolerance to herbicides and air pollutants. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 365–378Google Scholar
  55. Tanaka K, Sugahara K (1980) Role of superoxide dismutase in defense against SO2 toxicity and an increase in superoxide dismutase activity with SO2 fumigation. Plant Cell Physiol 21: 601–611Google Scholar
  56. Tanaka K, Suda Y, Kondo N, Sugahara K (1985) 03 tolerance and the ascorbate-dependent H2O2 decomposing system in chloroplasts. Plant Cell Physiol 26: 1425–1431Google Scholar
  57. Tanaka K, Saji H, Kondo N (1988a) Immunological properties of spinach glutathione reductase and inductive biosynthesis of the enzyme with ozone. Plant Cell Physiol 29: 637–642Google Scholar
  58. Tanaka K, Furusawa I, Kondo N, Tanaka K (1988b) SO2 tolerance of tobacco plants regenerated from paraquat-tolerant callus. Plant Cell Physiol 29: 743–746Google Scholar
  59. Tausz M, Bytnerowicz A, Arbaugh MJ, Weidner W, Grill D (1999) Antioxidants and protective pigments of Pinus ponderosa needles at gradients of natural stresses and ozone in the San Bernardino Mountains in California. Free Radical Res 31:sll3–sl20CrossRefGoogle Scholar
  60. Teramura AH, Sullivan JH, Ziska LH (1990) Interaction of elevated ultraviolet-B radiation and CO2 on productivity and photosynthetic characteristics in wheat, rice and soybean. Plant Physiol 94: 470–475PubMedCrossRefGoogle Scholar
  61. Torsethaugen G, Pitcher LH, Zilinskas BA, Pell EJ (1997) Overproduction of ascorbate peroxidase in the tobacco chloroplast does not provide protection against ozone. Plant Physiol 114: 529–537PubMedGoogle Scholar
  62. Van Camp W, Willekens H, Bowler C, Van Montagu M, Inze D, Reupold-Popp P, Sandermann H Jr, Langebartels C (1994) Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. Biotechnology 12: 165–168CrossRefGoogle Scholar
  63. Vanacker H, Carver TL, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117: 1103–1114PubMedCrossRefGoogle Scholar
  64. Wellburn AR, Wellburn FAM (1997) Air pollution and free radical protection responses of plants. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 861–876Google Scholar
  65. Willekens H, Van Camp W, Van Montagu M, Inze D, Langebartels C, Sandermann H Jr (1994) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol 106: 1007–1014PubMedGoogle Scholar
  66. Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inze D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16: 4806–4816PubMedCrossRefGoogle Scholar
  67. Ziska LH, Teramura AH (1992) CO2 enhancement of growth and photosynthesis in rice ( Oryza sativa ). Plant Physiol 99: 473–481PubMedCrossRefGoogle Scholar

Copyright information

© Springer -Verlag Tokyo 2002

Authors and Affiliations

  • Shigeto Morita
    • 1
    • 2
  • Kunisuke Tanaka
    • 1
    • 2
  1. 1.Faculty of AgricultureKyoto Prefectural UniversitySakyo-ku, KyotoJapan
  2. 2.Basic Research DivisionKyoto Prefectural Institute of Agricultural BiotechnologySeika, Soraku, KyotoJapan

Personalised recommendations