Simulating ozone detoxification in the leaf apoplast through the direct reaction with ascorbate

Planta

Volumn 210, Issue 3, 2000, Pages 454-467

  Plöchl, Matthias ^a   Lyons, Tom ^b   Ollerenshaw, John ^b   Barnes, Jeremy ^b  

^a LEIBNIZ INSTITUTE FOR AGRICULTURAL ENGINEERING AND BIOECONOMY ATB   (Germany)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Ascorbic acid; Compartmentation (ascorbate); Computer model; Detoxification (ozone); Leaf apoplast; Ozone

Indexed keywords

APOPLAST; ASCORBIC ACID; CELL MEMBRANE; CELL WALL; CYTOSOL; DETOXIFICATION; MATHEMATICAL MODEL; MEMBRANE PERMEABILITY; OZONE; PH; REACTION ANALYSIS; REACTION MECHANISM; SIMULATION; SIMULATION MODEL;

EID: 17544402043     PISSN: 00320935     EISSN: None     Source Type: Journal    
DOI: 10.1007/PL00008153     Document Type: Article

References (118)

1. Asard H, Horemans N, Caubergs RJ (1995) Involvement of ascorbic acid and a b-type cytochrome in plant plasma membrane redox reactions. Protoplasma 184: 36-41
2. Banerjee S, Yalkowsky SH, Valvani SC (1980) Water solubility and octanol/water partition coefficients of organics. Limitations of the solubility-partition coefficient correlation. Environ Sci Technol 14: 1227-1229
3. Barnes JD, Balaguer L, Manrique E, Davison AW (1999a) Resistance to air pollutants: from cell to community. In: Valladres F, Pugnaire FI (eds) Handbook of functional ecology. Dekker, New York, pp 735-770
4. Barnes JD, Bender J, Lyons T, Borland AM (1999b) Natural and man-made selection for air pollution resistance. J Exp Bot 50: 1423-1435
5. Bennett JP, Rassat P, Berrang P, Karnosky DF (1992) Relationships between leaf anatomy and ozone sensitivity of Fraxinus pennsylvanica Marsh and Prunus serotina Ehrh. Environ Exp Bot 32: 33-41
6. Bérczi, A, Møller IM (1998) NADH-monodehydroascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membranes. Plant Physiol 116: 1029-1036
7. Bors W, Langebartels C, Michel C, Sandermann H (1989) Polyamines as protectants against ozone damage. Phytochemistry 28: 1589-1595
8. Briner E, Perrottet E (1939) Determination of the solubility of ozone in water and aqueous sodium chloride solution; calculation of the solubility of atmospheric ozone in water. Helv Chim Acta 22: 397-404 [in French]
9. Castillo FJ, Greppin H (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure. Environ Exp Bot 28: 231-238
10. 2+. Plant Physiol 74: 846-851
11. Chameides WL (1989) The chemistry of ozone deposition to plant leaves: role of ascorbic acid. Environ Sci Technol 23: 595 600
12. Chameides WL, Kasibhatla PS, Yienger J, Levy H (1994) Growth of continental-scale metro-agro-plexes, regional ozone pollution, and world food production. Science 264: 74-77
13. Chappelka AH, Chevone BI (1992) Tree responses to ozone. In: Lefohn AS (ed) Surface-level ozone exposures and their effects on vegetation. Lewis Publishers, Chelsea, pp 271-324
14. Chiou CT, Freed VH, Schmedding DW, Kohnert RL (1977) Partition coefficient and bioaccumulation of selected organic chemicals. Environ Sci Technol 11: 475-478
15. Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93: 9970-9974
16. Cross CE, Motchnik PA, Bruener BA. Jones DA, Kaur H, Ames BN, Halliwell B (1992) Oxidative damage to plasma constituents by ozone. FEBS Lett 298: 269-272
17. Cross CE, van der Vliet A, Louie S, Thiele JJ, Halliwell B (1998) Oxidative stress and antioxidants at biosurfaces: plants, skin, and respiratory tract surfaces. Environ Health Perspect 106: 1241-1251
18. Dack MRJ (1976) Solvent structure. III. The dependence of partial molal volumes on internal pressure and solvent compressibility. Aust J Chem 29: 779-786
19. Davison AW, Barnes JD (1998) Effects of ozone on wild plants. New Phytol 139: 135-151
20. Deutsch JC (1998a) Ascorbic acid oxidation by hydrogen peroxide. Anal Biochem 255: 1-7
21. Deutsch JC (1998b) Oxygen-accepting antioxidants which arise during ascorbate oxidation. Anal Biochem 265: 238-245
22. Dietz K-J (1997) Functions and responses of the leaf apoplast under stress. Prog Bot 58: 221-254
23. Eckey-Kaltenbach H, Heller W, Sonnenbichler J, Zetl I, Schäfer W, Ernst D, Sandermann H (1993) Oxidative stress and plant secondary metabolism: 6′-O-malonylapin in parsley. Phytochemistry 34: 687-691
24. Eckey-Kaltenbach H, Ernst D, Heller W, Sandermann H (1994) Biochemical plant response to ozone. IV. Cross-induction of defensive pathways in parsley (Petroselinum crispum L.) plants. Plant Physiol 104: 67-74
25. Evans LS, Ting IP (1974) Ozone sensitivity of leaves: relationship to leaf water content, gas transfer resistance, and anatomical characteristics. Am J Bot 61: 592-597
26. 2 studies. J Exp Bot 48: 307-313
27. Foyer CH, Halliwell B (1976) Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133: 21-25
28. Foyer CH, Lelandais M (1996) A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. J Plant Physiol 148: 391-398
29. Foyer CH, Mullineaux PM (1998) The presence of dehydroascorbate and dehydroascorbate reductase in plant tissues. FEBS Lett 425: 528-529
30. Freebairn HT (1960) The prevention of air pollution damage to plants by the use of vitamin C sprays. J Air Pollut Control Assoc 10: 314-317
31. Freebairn HT, Taylor OC (1960) Prevention of plant damage from air-borne oxidizing agents. Proc Am Soc Hort Sci 76: 693-699
32. Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J 332: 507-515
33. Fuhrer J, Skarby L, Ashmore MR (1997) Critical levels for ozone effects on vegetation in Europe. Environ Pollut 97: 91-106
34. Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature and stomatal diffusion resistance. Meded Landbowhogesch Wageningen 13: 1-68
35. Giamalva DH, Church DF, Pryor WA (1985) A comparison of the rates of ozonation of biological antioxidants and oleate and linoleate esters. Biochem Biophys Res Commun 133: 773-779
36. Gimmler HB, Heilmann B, Demmig B, Hartung W (1981) The permeability coefficients of the plasmalemma and the chloroplast envelope of spinach mesophyll cells for phytohormones. Z Naturforsch 36C: 672-678
37. Günthardt-Goerg MS, McQuattie CJ, Scheidegger C, Rhiner C, Matyssek R (1997) Ozone-induced cytochemical and ultrastructural changes in leaf mesophyll cell walls. Can J Forest Res 27: 453-463
38. Hartung W, Radin JW, Hendrix DL (1988) Abscisic acid movement into the apoplastic solution of water-stressed cotton leaves. Plant Physiol 86: 908-913
39. Harris MJ, Bailey-Serres, JN (1994) Ozone effects on gene expression and molecular approaches to breeding for air pollution resistance. In: Basra AS (ed) Stress-induced gene expression in plants. Harwood Academic Publ. Singapore, pp 185-207
40. Heath RL (1980) Initial events in injury to plants by air pollutants. Annu Rev Plant Physiol 31: 395-431
41. Heath RL (1987) The biochemistry of ozone attack on the plasma membranes of plant cells. Rec Adv Phytochem 21: 29-54
42. Heath RL (1988) Biochemical mechanisms of pollutant stress. In: Heck WW, Taylor OC, Tingey DT (eds) Assessment of crop loss from air pollutants. Elsevier, New York, pp 259-286
43. Heck WW, Adams RM, Cure WW, Heagle AS, Heggestad HE, Kohut RJ, Kress LW, Rawlings JO, Taylor OC (1983) A reassessment of crop loss from ozone. Environ Sci Technol 12: 572A-581A
44. Hoffmann B, Plänker R, Mengal K (1992) Measurements of pH in the apoplast of sunflower leaves by means of fluorescence. Physiol Plant 84: 146-153
45. Horemans N, Asard H, Caubergs RJ (1996) Transport of ascorbate into plasma membrane vesicles of Phaseolus vulgaris L. Protoplasma 194: 177-185
46. Horemans N, Asard H, Caubergs RJ (1997) The ascorbate carrier of higher plant plasma membranes preferentially translocates the fully oxidized (dehydroascorbate) molecule. Plant Physiol 114: 1247-1253
47. Horemans N, Asard H, Caubergs RJ (1998) Carrier mediated uptake of dehydroascorbate into plant plasma membrane vesicles shows trans-stimulation. FEBS Lett 421: 41-44
48. Izuta T (1998) Ecophysiological responses of Japanese forest tree species to ozone, simulated acid rain and soil acidification. J Plant Res 111: 471-480
49. Jakob A, Heber U (1998) Apoplastic ascorbate does not prevent the oxidation of fluorescent amphiphilic dyes by ambient and elevated concentrations of ozone in leaves. Plant Cell Physiol 39: 313-322
50. Jorgensen SE (1990) Estimation of physical-chemical parameters in ecotoxicology. In: Jorgensen SE (ed) Modelling in ecotoxicology, developments in environmental modelling 16. Elsevier, Amsterdam, pp 51-68
51. Kangasjärvi J, Talvinen J, Utriainen M, Karjalainen R (1994) Plant defence systems induced by ozone. Plant Cell Environ 17: 783-794
52. Kanofsky JR, Sima PD (1995a) Singlet oxygen generation from the reaction of ozone with plant leaves. J Biol Chem 270: 7850-7852
53. Kanofsky JR, Sima PD (1995b) Reactive absorption of ozone by aqueous biomolecule solutions: implications for the role of sulfhydryl compounds as targets for ozone. Arch Biochem Biophys 316: 52-62
54. Kelly FJ, Mudway I, Krishna MT, Holgate ST (1995) The free radical basis of air pollution: focus on ozone. Respir Med 89: 647-656
55. Kerstiens G, Lendzian KJ (1989) Interactions between ozone and plant cuticles. I. Ozone deposition and permeability. New Phytol 112: 13-19
56. Kollist H, Moldau H, Mortensen L, Rasmussen SK, Jorgensen LB (1996) Ascorbate levels and ozone decay in the cell walls of barley and wheat seedlings. In: Obinger C, Burner U, Ebermann R, Penel C, Greppin H (eds) Plant peroxidases: biochemistry and physiology. Proceedings IV Internatl Symp 1996. Rochat-Bauman, Geneva, pp 358-362
57. Laisk A, Kull O, Moldau H (1989) Ozone concentration in leaf intercellular air spaces is close to zero. Plant Physiol 90: 1163-1167
58. Langebartels C, Kerner K, Leonardi S, Schraudner M, Trost M, Heller W, Sandermann H (1991) Biochemical plant responses to ozone. I. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiol 95: 882-889
59. Lee EH (1991) Plant resistance mechanisms to air pollutants: rhythms in ascorbic acid production during growth under ozone stress. Chronobiol Int 8: 93-102
60. 3-resistant cultivars by high-performance liquid chromotography. Environ Exp Bot 24: 331-341
61. Liso R, De Gara L, Tommasi F, Arigoni O (1985) Ascorbic acid requirement for increased peroxidase activity in potato tuber slice aging. FEBS Lett 187: 141-145
62. Loewus FA (1980) L-ascorbic acid: metabolism, biosynthesis, function. In: Preiss J (ed) The biochemistry of plants, vol 3. Academic Press, New York, pp 77-99
63. Loewus FA (1988) Ascorbic acid and its metabolic products. In: Preiss J (ed)The biochemistry of plants, vol 14. Academic Press, New York, pp 85-107
64. Luwe M (1996) Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentrations in the air. Plant Cell Environ 19: 321-328
65. Luwe M, Heber U (1995) Ozone detoxification in theapoplasm and symplasm of spinach, bean and beech leaves at ambient and elevated concentrations of ozone in the air. Planta 197: 448-455
66. Luwe MWF, Takahama U, Heber U (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves. Plant Physiol 101: 969-976
67. Lyons T. Plöchl M, Turcsányi E, Barnes J (1999a) Extracellular antioxidants: a protective screen against ozone? In: Agrawal S, Agrawal M (eds) Environmental pollution and plant responses. CRC Press Lewis Publishers, Boca Raton, pp 183-201
68. Lyons T, Ollerenshaw JH, Barnes JD (1999b) Impacts of ozone on Plantago major: apoplastic and symplastic antioxidant status. New Phytol 141: 253-263
69. Mächler F, Wasescha MR, Krieg F, Oertli JJ (1995) Damage by ozone and protection by ascorbic acid in barley leaves. J Plant Physiol 147: 469-473
70. Mansfield TA, Freer-Smith PH (1984) The role of stomata in resistance mechanisms. In: Koziol MJ, Whatley FJ (eds) Gaseous air pollutants and plant metabolism. Butterworths, London, pp 131-146
71. Menser HA (1964) Responses of plants to air pollutants. III. A relation between ascorbic acid levels and ozone susceptibility of light-preconditioned tobacco plants. Plant Physiol 39: 564-567
72. 2 exchange in plants under ozone stress. Russ J Plant Physiol 40: 532-538
73. Moldau H (1998) Hierarchy of ozone scavenging reaction in the plant cell wall. Physiol Plant 104: 617-622
74. Moldau H, Bichele I, Hüve K (1998) Dark-induced ascorbate deficiency in leaf cell walls increases plasmalemma injury under ozone. Planta 207: 60-66
75. Moldau H, Padu E, Bichele I (1997) Quantification of ozone decay and requirement for ascorbate in Phaseolus vulgaris L. mesophyll cell walls. Phyton 37: 175-180
76. Morell S, Follmann H, De Tullio M, Häberlein I (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Lett 414: 567-570
77. Morell S, Follmann H, De Tullio M, Haberlein I (1998) Dehydroascorbate reduction: the phantom remaining. FEBS Lett 425: 530-531
78. Mudway IS, Kelly FJ (1998) Modeling the interaction of ozone with pulmonary epithelial lining fluid antioxidants. Toxicol Appl Pharmacol 148: 91-100
79. Mühling KH, Plieth C, Hansen U-P, Sattelmacher B (1995) Apoplastic pH of intact leaves of Vicia faba as influenced by light. J Exp Bot 46: 377-382
80. Musselman RC, Massman WJ (1999) Ozone flux to vegetation and its relationship to plant response and ambient air quality standards. Atmos Environ 33: 65-73
81. Navas P, Villalba JM, Córdoba F (1994) Ascorbate function at the plasma membrane. Biochim Biophys Acta 1197: 1-13
82. Nobel PS (1991) Physicochemical and environmental plant physiology. Academic Press, San Diego
83. Noctor G, Foyer CH (1998) Ascorbate and gluathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279
84. O'Dell RA, Taheri M, Kabel RL (1977) A model for uptake of pollutants by vegetation. J Air Pollut Control Assoc 27: 1104-1109
85. 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: 790-799
86. Pääkkönen E, Holopainen T, Kärenlampi L (1995) Ageing-related anatomical and ultrastructural changes in leaves of birch (Betula pendula Roth.) clones affected by low ozone exposures. Annal Bot 75: 285-294
87. Pfanz H (1987) Uptake and distribution and sulphur dioxide in plant cells and organelles. Effects on metabolism. PhD thesis, Universität Würzburg [in German]
88. Pfanz H, Oppmann B (1991) The possible role of apoplastic peroxidases in detoxifying the air pollutant sulphur dioxide. In: Lobarzewski J, Greppin H, Penel C, Gaspar T (eds) Biochemical, molecular and physiological aspects of plant peroxidases. University Marie Curie-Sklodowska and University of Geneva, Lublin and Geneva, pp 401-417
89. Plöchl M (1992) The importance of apoplastic ascorbic acid in the scavenging of ozone and nitrogen dioxide in plant leaves: the dynamic modelling of the involvement of metabolic process in the leaf system. PhD thesis, Johann Wolfgang Goethe-University, Frankfurt, Germany [in German]
90. Polle A, Chakrabarti K, Schurmann 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
91. Polle A, Wieser G, Havranek WM (1995) Quantification of ozone influx and apoplastic ascorbate content in needles of Norway spruce trees (Picea abies L., Karst.) at high altitude. Plant Cell Environ 18: 681-688
92. Ranieri A, D'Urso G, Nali C, Lorenzini G, Soldatini GF (1996) Ozone stimulates apoplastic antioxidant systems in pumpkin leaves. Physiol Plant 97: 381-387
93. Rautenkranz AAF, Li L, Mächler F, Martinoia E, Oertli JJ (1994) Transport of ascorbic and dehydroascorbic acids across protoplast and vacuole membranes isolated from barley (Hordeum vulgare L. cv Gerbel) leaves. Plant Physiol 106: 187-193
94. Robinson MF, Heath J, Mansfield TA (1998) Disturbances in stomatal behaviour caused by air pollutants. J Exp Bot 49: 461-469
95. Runeckles VC (1992) Uptake of ozone by vegetation. In: Lefohn AS (ed) Surface-level ozone exposures and their effects on vegetation. Lewis Publishers, Chelsea, pp 157-188
96. Runeckles VC, Chevone BI (1992) Crop responses to ozone. In: Lefohn AS (ed) Surface-level ozone exposures and their effects on vegetation. Lewis Publishers, Chelsea, pp 189-270
97. Sandermann H, Wellburn AR, Heath RL (1997) Forest decline and ozone: a comparison of controlled chamber and field experiments (Ecological studies 127). Springer, Berlin
98. Schraudner M, Langebartels C, Sandermann H (1997) Changes in the biochemical status of plant cells induced by the environmental pollutant ozone. Physiol Plant 100: 274-280
99. Seel F (1965) Acid-and base-reactions with water. Analytical Chemistry. Verlag Chemie, Weinheim, pp 37-49, 108-126
100. Shamin M, Khoo SB (1979) Some physical properties of aqueous L-ascorbic acid solutions. Aust J Chem 32: 2293-2295
101. Slobodin JM, Basova AK, Helms EE (1946) Ascorbic acid: methods of generation and properties. I. Solubility of ascorbic acid and of intermediates of synthesis. Z Prikladnoj Chimii 19: 170-171 [in Russ]
102. Slovik S, Baier M, Hartung W (1992) Compartmental distribution and redistribution of acid in intact leaves. I. Mathematical formulation. Planta 187: 14-25
103. Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78: 661-669
104. Streller S, Wingsle G (1994) Pinus sylvestris L, needles contain extracellular CuZn superoxide dismutase. Planta 192: 195-201
105. Stockwell WR, Kramm G, Scheel H-E, Mohnen VA, Seiler W (1997) Ozone formation, destruction and exposure in Europe and the United States. In: Sandermann H, Wellburn AR, Heath RL (eds) Forest decline and ozone: a comparison of controlled chamber and field experiments (Ecological studies 127). Springer, Berlin, PP 1-38
106. Takahama U, Oniki T (1992) Regulation of peroxidase-dependant oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol 33: 379-387
107. Takahama U, Oniki T (1994) The association of ascorbate and ascorbate oxidase in the apoplast with IAA-enhanced elongation of epicotyls from Vigna angularis. Plant Cell Physiol 35: 257-266
108. Taylor GE, Tingey DT, Ratsch HC (1982) Ozone flux in Glycine max (L.) Merr.: sites of regulation and relationship to leaf injury. Oecologia 53: 179-186
109. Turcsányi E, Cardoso-Vilhena J, Daymond J, Gillespie C, Balaguer L, Ollerenshaw JH, Barnes JD (1999a) Impacts of troposphenc ozone: past, present and likely future. In: Singh SN (ed) Climate change and plants. Springer, in press
110. Turcsányi E, Lyons T, Plöchl M, Barnes J (1999b) Does ascorbate in the mesophyll cell walls form the first line of defence against ozone? I. Testing the concept using broad bean (Vicia faba L.). J Exp Bot, in press
111. Turrell FM (1942) A quantitative morphological analysis of large and small leaves of alfalfa, with special reference to internal surface. Am J Bot 22: 400-415
112. 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
113. Vanacker H, Harbinson J, Ruisch J, Carver TLW, Foyer CH (1998b) Antioxidant defences of the apoplast. Protoplasma 205: 129-140
114. Van der Vliet A, O'Neill CA, Eiserich JP, Cross CE (1995) Oxidative damage to extracellular fluids by ozone and possible protective effects of thiols. Arch Biochem Biophys 321: 43-50
115. Wang D, Hinckley TM, Cumming AB, Braatne J (1995) A comparison of measured and modeled ozone uptake into plant leaves. Environ Poll 89: 247-254
116. Wellburn AR (1990) Why are atmospheric oxides of nitrogen usually phytotoxic and not alternative fertilizers? New Phytol 115: 395-402
117. Wiese CB, Pell EJ (1997) Influence of ozone on transgenic tobacco plants expressing reduced quantities of Rubisco. Plant Cell Environ 20: 1283-1291
118. Winkler BS, Orseili SM, Rex TS (1994) The redox couple between glutathione and ascorbic acid: a chemical and physiological perspective. Free Rad Biol Med 17: 333-349