Uptake, Metabolism, and Detoxification of Sulfur Dioxide

  • Noriaki Kondo


Sulfur dioxide (SO2) is a major air pollutant that is artificially produced by fossil fuel combustion, mainly in the industrialized areas of both developed and developing countries, and also results from volcanic emission, biogenic emissions, etc. SO2 can also form aerosols, sulfate particles, in the atmosphere by photochemical reactions. Aerosols can then be incorporated into clouds and/or transported over long distances, thus causing severe acid precipitation as wet and dry depositions in surrounding countries.


Sulfur Dioxide Stomatal Closure Physiol Plant Sulfite Oxidase Sulfite Reductase 
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. Alscher R, Bower JL, Zipfel W (1987) The basis for different sensitivities to SO2 in two cultivars of pea. J Exp Bot. 38: 99–108CrossRefGoogle Scholar
  2. Amundson RG, Weinstein LH (1981) Joint action of sulfur dioxide and nitrogen dioxide on foliar injury and stomatal behavior in soybean. J Environ Qual 10: 204–206CrossRefGoogle Scholar
  3. Aono M, Kubo A, Saji H, Tanaka K, Kondo (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell Physiol 34: 129–135Google Scholar
  4. Asada K, Kiso K (1973) Initiation of aerobic oxidation of sulfite by illuminated spinach chloroplasts. Eur J Biochem 33: 253–257PubMedCrossRefGoogle Scholar
  5. Ashenden TW (1978) Growth reductions in cocksfoot (Dactylis glomerata L.) as a result of SO2 pollution. Environ Pollut 15: 161–166CrossRefGoogle Scholar
  6. Ashenden TW, Mansfield TA (1978) Extreme pollution sensitivity of grasses when SO2 and NO2 are present in the atmosphere together. Nature 273: 142–143CrossRefGoogle Scholar
  7. Ayazloo M, Garsed SG, Bell JNB (1982) Studies on the tolerance to sulphur dioxide of grass populations in polluted areas. II. Morphological and physiological investigations. New Phytol 90: 109–126CrossRefGoogle Scholar
  8. Bae GY, Kondo N, Nakajima N, Ishizuka K (1995) Ethylene production in tomato plants by SO2 in relation to leaf injury (in Japanese with English abstract). J Jpn Soc Atmos Environ 30: 367–373Google Scholar
  9. Bae GY, Nakajima N, Ishizuka K, Kondo N (1996) The role in ozone phytotoxicity of the evolution of ethylene upon induction of 1-aminocyclopropane-l-carboxylic acid synthase by ozone fumigation in tomato plants. Plant Cell Physiol 37: 129–134Google Scholar
  10. Bailey JL, Cole RD (1959) Studies on the reaction of sulfite with proteins. J Biol Chem 234: 1733–1739PubMedGoogle Scholar
  11. Barton JR, McLaughlin SB, McConathy RK (1980) The effects of SO2 on components of leaf resistance to gas exchange. Environ Pollut Ser A 21: 255–265CrossRefGoogle Scholar
  12. Baxter R, Emes MJ, Lee J A (1989) The relationship between extracellular metal accumulation and bisulphate tolerance in Sphangnum cuspidatum Hoffm. New Phytol 111: 463–472CrossRefGoogle Scholar
  13. Baxter R, Emes MJ, Lee JA (1991) Short term effects of bisulphite on pollution-tolerant and pollution sensitive populations of Sphangnum cuspidatum Ehrh. (ex. Hoffm. ). New Phytol 118: 425–431CrossRefGoogle Scholar
  14. Black CR, Black VJ (1979) The effects of low concentrations of sulphur dioxide on stomatal conductance and epidermal cell survival in field bean ( Vicia faba L. ). J Exp Bot 30: 291–298CrossRefGoogle Scholar
  15. Black VJ, Unsworth MN (1979) Effects of low concentrations of sulphur dioxide on net photosynthesis and dark respiration. J Exp Bot 30: 473–483CrossRefGoogle Scholar
  16. Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li C, Herschbach C, Rennenberg H, Pimenta MJ, Shen T-L, Gage DA, Hanson AD (1999) S- Methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11: 1485–1497PubMedCrossRefGoogle Scholar
  17. Bressan RA, Wilson LG, L, Filner P (1978) Mechanisms of resistance to sulfur dioxide in the Cucurbitaceae. Plant Physiol 61: 761–767PubMedCrossRefGoogle Scholar
  18. Bressan RA, LeCureux L, Wilson LG, L, Filner P (1979) Emission of ethylene and ethane by leaf tissue exposed to injurious concentrations of sulfur dioxide or bisulfite ion. Plant Physiol 63: 924–930PubMedCrossRefGoogle Scholar
  19. Clarke K, Murray F (1990) Stimulatory effects of SO2 on growth of Eucalyptus rudis Endl. New Phytol 115: 633–637CrossRefGoogle Scholar
  20. Cohen HJ, Drew RT, Johnson JL, Rajagopalan KV (1973) Molecular basis of the biological function of molybdenum. The relationship between sulfite oxidase and the acute toxicity of bisulfite and SO2. Proc Natl Acad Sci USA 70: 3655–3659PubMedCrossRefGoogle Scholar
  21. Cornic G (1987) Interaction between sublethal pollution by sulphur dioxide and drought stress. The effect on photosynthetic capacity. Physiol Plant 71: 115–119Google Scholar
  22. Cowan IR, Raven JA, Hartung W, Farquhar GD (1982) A possible role for abscisic acid in coupling stomatal conductance and photosynthetic carbon metabolism in leaves. Aust J Plant Physiol 9: 489–498CrossRefGoogle Scholar
  23. Cowling DW, Lockyer DR (1978) The effect of SO2 on Lolium perenne L. grown at different levels of sulphur and nitrogen nutrition. J Exp Bot 29: 257–265CrossRefGoogle Scholar
  24. Cram WJ (1983) Sulphate accumulation is regulated at the tonoplast. Plant Sci Lett 31: 329–338CrossRefGoogle Scholar
  25. Deepak SS, Agrawal M (1999) Growth and yield responses of wheat plants to elevated levels of CO2 and SO2, singly and in combination. Environ Pollut 104: 411–419CrossRefGoogle Scholar
  26. Dittrich APM, Pfanz H, Heber U (1992) Oxidation and reduction of sulfite by chloroplasts and formation of sulfite addition compounds. Plant Physiol 98: 738–744PubMedCrossRefGoogle Scholar
  27. Fridovich I, Handler P (1961) Detection of free radicals generated during enzymic oxidations by the initiation of sulfite oxidation. J Biol Chem 236: 1836–1840PubMedGoogle Scholar
  28. Furukawa A, Isoda O, Iwaki H, Totsuka T (1979) Interspecific difference in responses of transpiration to SO2. Environ Control Biol 17: 153–159CrossRefGoogle Scholar
  29. Furukawa A, Isoda O, Iwaki H, Totsuka T (1980a) Interspecific difference in resistance to sulfur dioxide. In: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Res. Rep. Natl. Inst. Environ. Stud. Jpn No.11, pp 113–126Google Scholar
  30. Furukawa A, Natori T, Totsuka T (1980b) The effect of SO2 on net photosynthesis in sunflower leaf. In: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Res. Rep. Natl. Inst. Environ. Stud. Jpn No.11, pp 113–126Google Scholar
  31. Furukawa A, Katase M, Ushijima T, Totsuka T (1984) Inhibition of photosynthesis of poplar species and sunflower by O3. In: Studies on effects of air pollutant mixtures on plants, Part 1. Res. Rep. Natl. Inst. Environ. Stud. Jpn No. 65, pp 77–87Google Scholar
  32. Garsed SG, Read DJ (1977) Sulphur dioxide metabolism in soybean, Glycine max var. biloxi. I. The effects of light and dark on the uptake and translocation of 35SO2. New Fhytol 78: 111–119CrossRefGoogle Scholar
  33. Gezeilus K, Hallgren J-E (1980) Effect of SO32- on the activity of ribulose bisphosphate carboxylase from seedlings of Pinus sivestris. Physiol Plant 49: 354–358CrossRefGoogle Scholar
  34. Gould RP, Minchin PEH, Young PC (1988) The effects of sulphur dioxide on phloem transport in two cereals. J Exp Bot 39: 997–1007CrossRefGoogle Scholar
  35. Gries C, Romagni JG, Nash TH III, Kuhn U, Kesselmeier J (1997) The relation of H2S release to SO2 fumigation of lichens. New Phytol 136: 703–711CrossRefGoogle Scholar
  36. Grill D, Esterbauer H, Klosch U (1979) Effect of sulphur dioxide on glutathione in leaves of plants. Environ Pollut Ser A 19: 187–194Google Scholar
  37. Grill D, Esterbauer H, Scharner M, Felgitsh C (1980) Effect of sulphur dioxide on protein-SH in needles of Picea abies. Eur J For Pathol 10: 263–267CrossRefGoogle Scholar
  38. Hällgren J-E, Frederiksson S-A (1982) Emission of hydrogen sulfide from sulfur dioxide-fumigated pine trees. Plant Physiol 70: 456–459PubMedCrossRefGoogle Scholar
  39. Hampp R, Ziegler I (1977) Sulfate and sulfite translocation via the phosphate translocator of the inner envelope membrane of chloroplasts. Planta 137: 309–312CrossRefGoogle Scholar
  40. Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202: 138–148PubMedCrossRefGoogle Scholar
  41. Herschbach C, De Kok LJ, Rennenberg H (1995) Net uptake of sulphate and its transport to the shoot in tobacco plants fumigated with H2S or SO2. Plant Soil 175: 75–84CrossRefGoogle Scholar
  42. Hogetsu T, Shishikura M (1994) Effects of sulfur dioxide and ozone on intact leaves and isolated mesophyll cells of groundnut plants ( Arachis hypogaea L. ). J Plant Res 107: 229–235CrossRefGoogle Scholar
  43. Jensen KF, Roberts BR (1986) Changes in yellow poplar ( Liriodendron tulipifera) stomatal resistance with sulfur dioxide and ozone fumigation. Environ Pollut Ser A 41: 235–246CrossRefGoogle Scholar
  44. Kaiser G, Martinoia E, Schroppel-Meier G, Heber U (1989) Active transport of sulfite into the vacuole of plant cells provides halotorelance and can detoxify SO2. J Plant Physiol 133: 756–763Google Scholar
  45. Kaiser WM (1979) Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145: 377–382CrossRefGoogle Scholar
  46. Kaiser WM, Höfler M, Heber U (1993) Can plants exposed to SO2 excrete sulfuric acid through the roots? Physiol Plant 87: 61–67CrossRefGoogle Scholar
  47. Kimmerer TW, Kozlowski TT (1981) Stomatal conductance and sulfur uptake of five clones of Populus tremuloides exposed to sulfur dioxide. Plant Physiol 67: 990–995PubMedCrossRefGoogle Scholar
  48. Klebanoff SJ (1961) The sulfite-activated oxidation of reduced pyrimidine nucleotides by peroxidase. Biochim Biophys Acta 48: 93–103PubMedCrossRefGoogle Scholar
  49. Kondo N (1987) Changes in transpiration rate caused by air pollutants and contents of phytohormones. In: Studies on the role of vegetation as a sink of air pollutants. Res. Rep. Natl. Inst. Environ. Stud. No. 108, pp 187–197 (in Japanese)Google Scholar
  50. Kondo N, Sugahara K (1978) Changes in transpiration rate of SO2-resistant and -sensitive plants with SO2 fumigation and the participation of abscisic acid. Plant Cell Physiol 19: 365–373Google Scholar
  51. Kondo N, Sugahara K (1984) Effects of air pollutants on transpiration rate in relation to abscisic acid content. In: Studies on effects of air pollutant mixtures on plants, Part 1. Res. Rep. Natl. Inst. Environ. Stud. Jpn No. 65, pp 1–8Google Scholar
  52. Kondo N, Akiyama Y, Fujiwara M, Sugahara K (1980a) Sulfite oxidizing activities in plants. In: Studies on the effects of air pollutants on plants. Res. Rep. Natl. Inst. Environ. Stud. No.11, pp 137–150Google Scholar
  53. Kondo N, Maruta I, Sugahara K (1980b) Effects of sulfite and pH on abscisic acid-dependent transpiration and on stomatal opening. Plant Cell Physiol 21: 817–828Google Scholar
  54. Koziol MJ, Jordan CF (1978) Changes in carbohydrate levels in red kidney bean ( Phaseolus vulgaris L.) exposed to sulphur dioxide. J Exp Bot 29: 1057–1043Google Scholar
  55. Kropff MJ (1987) Physiological effects of sulfur dioxide: 1. The effect of sulfur dioxide on photosynthesis and stomatal regulation of Vicia faba L. Plant Cell Environ 10: 753–760Google Scholar
  56. Laisk A, Pfanz H, Heber U (1988) Sulfur dioxide fluxes into different cellular compartments of leaves photosynthesizing in a polluted atmosphere: II. Consequences of sulfur dioxide uptake as revealed by computer analysis. Planta 173: 241–252CrossRefGoogle Scholar
  57. Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120: 637–643PubMedCrossRefGoogle Scholar
  58. Libera W, Ziegler I, Ziegler H (1975) The action of sulfite on the HCO3 fixation and the fixation pattern of isolated chloroplasts and leaf tissue slices. Z Pflanzenphysiol 74: 420–433Google Scholar
  59. Lorenc-Plucinska G, Ziegler H (1987) The effect of sulphite on sucrose uptake and translocation in the cotyledons of castor bean ( Ricinus communis L. ). J Plant Physiol 127: 97–110Google Scholar
  60. Lucas PW (1990) The effects of prior exposure to sulfur dioxide and nitrogen dioxide on the water relations of timothy grass (Phleum pratense) under drought conditions. Environ Pollut 66: 117–138PubMedCrossRefGoogle Scholar
  61. Lüttge U, Osmond CB, Ball E, Brinckmann E, Kinze G (1972) Bisulfite compounds as metabolic inhibitors: nonspecific effects on membranes. Plant Cell Physiol 13: 505–514Google Scholar
  62. Maas FM, De Kok LJ (1988) In vitro NADH oxidation as an early indicator for growth reduction in spinach exposed to H2S in the ambient air. Plant Cell Physiol 29: 523–526Google Scholar
  63. Maas FM, De Kok LJ, Strik-Timmer W, Kuiper PJC (1987) Plant responses to H2S and SO2 fumigation. II. Differences in metabolism of H2S and SO2 in spinach. Physiol Plant 70: 722–728CrossRefGoogle Scholar
  64. Maas FM, van Loo EN, van Hasselt PR (1988) Effect of long-term H2S fumigation on photosynthesis in spinach. Correlation between CO2 fixation and chlorophyll a fluorescence. Physiol Plant 72: 77–83CrossRefGoogle Scholar
  65. Majernik O, Mansfield TA (1970) Direct effect of SO2 pollution on the degree of opening of stomata. Nature 227: 377–378PubMedCrossRefGoogle Scholar
  66. Malhotra SS, Hocking D (1976) Biochemical and cytological effects of sulphur dioxide on plant metabolism. New Phytol 76: 227–237CrossRefGoogle Scholar
  67. Mansfield TA, Majernik O (1970) Can stomata play a part in protecting plants against air pollutants? Environ Pollut 1: 149–154CrossRefGoogle Scholar
  68. Martin C, Thimann K (1972a) The role of protein synthesis in the senescence of leaves. 1. The formation of protease. Plant Physiol 49: 64–71PubMedCrossRefGoogle Scholar
  69. Martin C, Thimann K (1972b) The role of protein synthesis in the senescence of leaves. II. The influence of amino acids on senescence. Plant Physiol 50: 432–437PubMedCrossRefGoogle Scholar
  70. Maurousset L, Bonnemain J-L (1990) Mechanism of the inhibition of phloem loading by sodium sulfite: effect of the pollutant on the transmembrane potential difference. Physiol Plant 80: 233–237CrossRefGoogle Scholar
  71. Maurousset L, Raymond P, Gaudillere M, Bonnemain J-L (1992) Mechanism of the inhibition of phloem loading by sodium sulfite: effect of the pollutant on respiration, photosynthesis and energy charge in the leaf tissues. Physiol Plant 84: 101–105CrossRefGoogle Scholar
  72. Mehlhorn H (1990) Ethylene-promoted ascorbate peroxidase activity protects against hydrogen peroxide, ozone and paraquat. Plant Cell Environ 13: 971–976CrossRefGoogle Scholar
  73. Mehlhorn H, Wellburn AR (1987) Stress ethylene formation determines plant sensitivity to ozone. Nature 327: 417–418CrossRefGoogle Scholar
  74. Mejstrik V (1980) The influence of low SO2 concentrations on growth reduction of Nicotiana tabacum L. cv. Samsun and Cucumis sativus L. cv. Unikat. Environ Pollut Ser A 21: 73–76CrossRefGoogle Scholar
  75. Menser HA, Heggestad HE (1966) Ozone and sulfur dioxide synergism: injury to tobacco plants. Science 153: 424–435PubMedCrossRefGoogle Scholar
  76. Miller JE, Xerikos PB (1979) Residence time of sulfite in SO2 ‘sensitive’ and ‘tolerant’ soybean cultivars. Environ Pollut 18: 259–264CrossRefGoogle Scholar
  77. Minchin PEH, Gould R (1986) Effect of SO2 on phloem loading. Plant Sci 43: 179–183CrossRefGoogle Scholar
  78. Miszalski Z, Ziegler I (1979) Increase in chloroplastic thiol groups by SO2 and its effects on light modulation of NADP-dependent glyceraldehyde-3-phosphate dehydrogenase. Planta 145: 383–387CrossRefGoogle Scholar
  79. Mukerji SK, Yang SF (1974) Phosphoenolpyruvate carboxylase from spinach leaf tissue. Plant Physiol 53: 829–834PubMedCrossRefGoogle Scholar
  80. Murray F (1985) Changes in growth and quality characteristics of Lucerne (Medicago sativa L.) in response to sulphur dioxide exposure under field conditions. J Exp Bot 36: 449–457CrossRefGoogle Scholar
  81. Murray F, Wilson S (1990) Growth responses of barley exposed to SO2. New Phytol 114: 537–541CrossRefGoogle Scholar
  82. Nakamura S (1970) Initiation of sulfite oxidation by spinach ferredoxin-NADP reductase and ferredoxin system: a model experiment on the superoxide anion radical production by metalloflavoproteins. Biochem Biophys Res Commun 41: 177–183PubMedCrossRefGoogle Scholar
  83. Navari-Izzo F, Izzo R, Quartacci MF, Lorenzini G (1989) Growth and solute leakage in Hordeum vulgaris exposed to long-term fumigation with low concentrations of SO2. Physiol Plant 76: 445–450Google Scholar
  84. Neighbour EA, Cottam DA, Mansfield TA (1988) Effects of sulphur dioxide and nitrogen dioxide on the control of water loss by birch ( Betula spp. ). New Phytol 108: 149–157CrossRefGoogle Scholar
  85. Okupodu CM, Alscher RG, Grabau EA, Cramer CL (1996) Physiological, biochemical and molecular effects of sulfur dioxide. J Plant Physiol 148: 309–316CrossRefGoogle Scholar
  86. Omasa K, Abo F, Natori T, Totsuka T (1980) Analysis of air pollutant sorption by plants. (3) Sorption under fumigation with NO2, O3 or NO2 + O3. In: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Res. Rep. Natl. Inst. Environ. Stud. Jpn No. 11, pp 213–224Google Scholar
  87. Omasa K, Hashimoto Y, Aiga I (1981) A quantitative analysis of the relationships between SO2 or NO2 sorption and their acute effects on plant leaves using image instrumentation. Environ Control Biol 19: 59–67CrossRefGoogle Scholar
  88. Omasa K, Hashimoto Y, Aiga I (1983) Observation of stomatal movements of intact plants using an image instrumentation system with a light microscope. Plant Cell Physiol 24: 281–288Google Scholar
  89. Omasa K, Hashimoto Y, Kramer PJ, Strain BR, Aiga I, Kondo J (1985) Direct observation of reversible and irreversible stomatal responses of attached sunflower leaves to SO2. Plant Physiol 79: 153–158PubMedCrossRefGoogle Scholar
  90. Oren A, Padan E, Malkin S (1979) Sulfide inhibition of photosystem II in Cyanobacteria (blue-green algae) and tobacco chloroplasts. Biochim Biophys Acta 546: 270–279PubMedCrossRefGoogle Scholar
  91. Osmond CB, Avadhani PN (1970) Inhibition of the ß -carboxylation pathway of CO2 fixation by bisulfite compounds. Plant Physiol 45: 228–230PubMedCrossRefGoogle Scholar
  92. Peiser GD, Yang SF (1979) Ethylene and ethane production from sulfur dioxide-injured plants. Plant Physiol 63: 142–145PubMedCrossRefGoogle Scholar
  93. Peiser GD, Lizada MCC, Yang SF (1982) Sulfite-induced lipid peroxidation in chloroplasts as determined by ethane production. Plant Physiol 70: 994–998PubMedCrossRefGoogle Scholar
  94. Pfanz H, Martinoia E, Lange O-T, Heber U (1987a) Mesophyll resistance to SO2 fluxes into leaves. Plant Physiol. 85: 922–927PubMedCrossRefGoogle Scholar
  95. Pfanz H, Martinoia E, Lange O-T, Heber U (1987b) Flux of SO2 into leaf cells and cellular acidification by SO2. Plant Physiol 85:928–933Google Scholar
  96. Pierre M, Queiroz O (1981) Enzymic and metabolic changes in bean leaves during continuous pollution by subnecrotic leaves of SO2. Environ. Pollut Ser A 21: 41–51CrossRefGoogle Scholar
  97. Pierre M, Queiroz O (1982) Modulation by leaf age and SO2 concentration of the enzymic response to subnecrotic SO2 pollution. Environ Pollut Ser A 28: 209–217CrossRefGoogle Scholar
  98. Pierre M, Queiroz O (1988) Air pollution by SO2 amplifies the effects of water stress on enzymes and total proteins of spruce needles. Physiol Plant 73: 412–417CrossRefGoogle Scholar
  99. Price S, Long SP (1989) An in vivo analysis of the effect of SO2 fumigation on photosynthesis in Zea mays. Physiol. Plant 76: 193–200CrossRefGoogle Scholar
  100. Priebe A, Klein H, Jäger H-J (1978) Role of polyamines in SO2-polluted pea plants. J Exp Bot 29: 1045–1050CrossRefGoogle Scholar
  101. Robinson MF, Heath J, Mansfield TA (1998) Disturbances in stomatal behaviour caused by air pollutants. J Exp Bot 49: 461–469CrossRefGoogle Scholar
  102. Rothermel B, Alscher R (1985) A light-enhanced metabolism of sulfite in cells of Cucumis sativus L. cotyledons. Planta 166: 105–110CrossRefGoogle Scholar
  103. Sakaki T, Kondo N (1984) Sulfite inhibition of uptake and fixation of inorganic carbon in mesophyll protoplasts isolated from Vicia faba L. In: Studies on effects of air pollutant mixtures on plants, Part 1. Res. Rep. Natl. Inst. Environ. Stud. Jpn No. 65, pp 35–43Google Scholar
  104. Sakaki T, Kondo N (1985) Inhibition of photosynthesis by sulfite in mesophyll protoplasts isolated from Vicia faba L. in relation to intracellular sulfite accumulation. Plant Cell Physiol 26: 1045–1055Google Scholar
  105. Schiff JA, Hodson RC (1973) The metabolism of sulfate. Annu Rev Plant Physiol 24: 381–414CrossRefGoogle Scholar
  106. Sekiya J, Schmidt A, Wilson LG, Filner P (1982a) Emission of hydrogen sulfide by leaf tissue in response to L-cysteine. Plant Physiol 70: 430–436PubMedCrossRefGoogle Scholar
  107. Sekiya J, Wilson LG, Filner P (1982b) Resistance to injury by sulfur dioxide. Correlation with its reduction to, and emission of, hydrogen sulfide in Cucurbitaceae. Plant Physiol 70: 437–441PubMedCrossRefGoogle Scholar
  108. Shimazaki K, Sugahara K (1979a) Specific inhibition of photosystem II activity in chloroplasts by fumiation of spinach leaves with SO2. Plant Cell Physiol 20: 947–955Google Scholar
  109. Shimazaki K, Sugahara K (1979b) Inhibition site of the electron transport system in lettuce chloroplasts by fumigation of leaves with SO2. Plant Cell Physiol 21: 125–135Google Scholar
  110. Shimazaki K, Sakaki T, Kondo N, Sugahara K (1980) Active oxygen participation in chlorophyll destruction and lipid peroxidation in SO2-fumigated leaves of spinach. Plant Cell Physiol 21: 1193–1204Google Scholar
  111. Shimazaki K, Nakamachi K, Kondo N, Sugahara K (1984a) Sulfite inhibition of photosystem II in illuminated spinach leaves. Plant Cell Physiol 25: 337–341Google Scholar
  112. Shimazaki K, Ito K, Kondo N, Sugahara K (1984b) Reversible inhibition of the photosynthetic water-splitting enzyme system by SO2-fumigation assayed chlorophyll fluorescence and EPR signal in vivo. Plant Cell Physiol 25: 795–803Google Scholar
  113. Silvius JE, Ingle M, Baer CH (1975) Sulfur dioxide inhibition of photosynthesis in isolated spinach chloroplasts. Plant Physiol. 56: 434–437PubMedCrossRefGoogle Scholar
  114. Slovik S, Siegmund A, Kindermann G, Riebeling R, Balazs A (1995) Stomatal SO2 uptake and sulfate accumulation in needles of Norway spruce stands (Picea abies) in Central Europe. Plant Soil 168-169: 405–419CrossRefGoogle Scholar
  115. Slovik S, Hiive K, Kinderman G, Kaiser WM (1996) SO2-dependent cation competition and compartmentalization in Norway spruce needles. Plant Cell Environ 19: 813–824CrossRefGoogle Scholar
  116. Soldatini GF, Ranieri A, Lencioni L, Lorenzini G (1992) Effects of continuous SO2 fumigation on SH-containing compounds in two wheat cultivars of different sensitivities. J Exp Bot 43: 797–801CrossRefGoogle Scholar
  117. Sugahara K, Uchida S, Takimoto M (1980) Effects of sulfite ions on water-soluble chlorophyll proteins. In: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Res. Rep. Natl. Inst. Environ. Stud. Jpn No. 11, pp 103–112Google Scholar
  118. Takahama U, Veljovic-Iovanovic S, Heber U (1992) Effects of the air pollutant SO2 on leaves. Inhibition of sulfite oxidation in the apoplast by ascorbate and of apoplastic peroxidase by sulfite. Plant Physiol 100: 261–266PubMedCrossRefGoogle Scholar
  119. Takahashi S, Yoshida Y, Tamura G (1996) Purification and characterization of ferredoxin-sulfite reductases from leek ( Allium tuberosum) leaves. J Plant Res 109: 45–52CrossRefGoogle Scholar
  120. Tanaka H, Takanashi T, Yatazawa M (1972) Experimental studies on sulphur dioxide injuries in higher plants. I. Formation of glyoxylate bisulphite in plant leaves exposed to sulphur dioxide. Water Air Soil Pollut 1: 205–211Google Scholar
  121. 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
  122. Tanaka K, Kondo N, Sugahara K (1982a) Accumulation of hydrogen peroxide in chloroplasts of SO2-fumigated spinach leaves. Plant Cell Physiol 23: 999–1007Google Scholar
  123. Tanaka K, Otsubo T, Kondo N (1982b) Participation of hydrogen peroxide in the inactivation of Calvin cycle SH enzymes in SO2-fumigated spinach leaves. Plant Cell Physiol 23: 1009–1018Google Scholar
  124. Tanaka K, Suda Y, Kondo N, Sugahara K (1985) O3 tolerance and the ascorbate-dependent H2O2 decomposing system in chloroplasts. Plant Cell Physiol 26: 1425–1431Google Scholar
  125. Thomas FM, Runge M (1992) Proton neutralization in the leaves of English oak ( Quercus robur L.) exposed to sulphur dioxide. J Exp Bot 43: 803–809CrossRefGoogle Scholar
  126. Thomas MD, Hendricks RH, Collier TR, Hill GR (1943) The utilization of sulfate and sulfur dioxide for the nutrition of alfalfa. Plant Physiol 18: 345–371PubMedCrossRefGoogle Scholar
  127. Thomas MD, Hill GR Jr (1935) Absorption of sulphur dioxide by alfalfa and its relation to leaf injury. Plant Physiol 10: 291–307PubMedCrossRefGoogle Scholar
  128. Tschanz A, Landolt W, Bleuler P, Brunold C (1986) Effect of SO2 on the activity of adenosine 5’-phosphosulfate sulfotransferase from spruce trees ( Picea abies) in fumigation chambers and under field conditions. Physiol Plant 67: 235–241CrossRefGoogle Scholar
  129. Veeranjaneyulu K, Soukpo£-Kossi CN, Leblanc RM (1994) Emission of sulfur dioxide from sulfite-treated birch leaves. J Plant Physiol 144: 420–423Google Scholar
  130. Veljovic-Jovanovic S, Bilger W, Heber U (1993) Inhibition of photosynthesis, acidification and stimulation of zeaxanthin formation in leaves by sulfur dioxide and reversal of these effects. Planta 191: 365–376CrossRefGoogle Scholar
  131. Weigl J, Ziegler H (1962) Die Raumliche Verteilung von 35S und die Art der Markierten Verbindungen in Spinatblattern nach Begasung mit 35SO2. Planta 58: 435–447CrossRefGoogle Scholar
  132. Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiol 61: 184–189PubMedCrossRefGoogle Scholar
  133. Wyss H-R, Brunold C (1980) Regulation of adenosine 5’-phosphosulfate sulfotransferase by sulfur dioxide in primary leaves of beans ( Phaseolus vulgaris ). Physiol Plant 50: 161–165CrossRefGoogle Scholar
  134. Yang SF (1967) Biosynthesis of ethylene. Ethylene formation from methional by horseradish peroxidase. Arch Biochem Biophys 122: 481–487PubMedCrossRefGoogle Scholar
  135. Zelitch I (1957) a-Hydroxysulfonates as inhibitors of the enzymatic oxidation of glycolic and lactic acids. J Biol Chem 224:251–260Google Scholar
  136. Ziegler I (1972) The effect of SO3 on the activity of ribulose-l,5-diphosphate carboxylase in isolated spinach chloroplasts. Planta 103: 155–163CrossRefGoogle Scholar
  137. Ziegler I (1973) Effect of sulphite on phosphoenolpyruvate carboxylase and malate formation in extracts of Zea mays. Phytochemistry 12: 1027–1030CrossRefGoogle Scholar
  138. Ziegler I (1974) Malate dehydrogenase in Zea mays: properties and inhibition by sulfite. Biochim Biophys Acta 364: 28–37PubMedGoogle Scholar

Copyright information

© Springer -Verlag Tokyo 2002

Authors and Affiliations

  • Noriaki Kondo
    • 1
  1. 1.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoBunkyo-ku, TokyoJapan

Personalised recommendations