Physiological Damages and Biochemical Alleviation to Ozone Toxicity in Five Species of genus Acer

  • Han, Sim-Hee (Dept. of Forest Genetic Resources, Korea Forest Research Institute) ;
  • Kim, Du-Hyun (Dept. of Forest Genetic Resources, Korea Forest Research Institute) ;
  • Lee, Kab-Yeon (Dept. of Forest Genetic Resources, Korea Forest Research Institute) ;
  • Ku, Ja-Jung (Dept. of Forest Genetic Resources, Korea Forest Research Institute) ;
  • Kim, Pan-Gi (Dept. of Forest Resources and Environment, Sangju National University)
  • 투고 : 2007.07.04
  • 심사 : 2007.09.03
  • 발행 : 2007.10.31

초록

We investigated physiological damages and biochemical alleviation of five species of genus Acer under ozone fumigation in order to assess their tolerant ability against ozone toxicity. At the end of 150 ppb $O_3$ fumigation, photosynthetic characteristics were measured, and chlorophyll contents, malondialdehyde (MDA) and antioxidative enzyme activities were analyzed in the leaves of five maple trees (Acer buergerianum, A. ginnala, A. mono, A. palmatum, and A. palmatum var. sanguineum). The reduction of chlorophyll (chl) a in ozone-exposed plants was 16.8% (A. buergerianum) to 26.7% (A. ginnala) of control plants. For the content of chi b, A. ginnala and A. palmatum var. sanguineum represented the high reduction of 26.3% and 23.6%, respectively. The highest reduction on the chi a:b ratio was observed in the leaves of A. palmatum. The reduction of net photosynthesis in five species varied from 2.4% to 37.6%. Among five species, A. ginnala showed remarkable reduction (37.6%) for net photosynthesis in comparison with control. Carboxylation efficiency differed significantly (P < 0.05) among species and between control and ozone treatment. The reduction of carboxylation efficiency was the highest in the leaves of A. ginnala (44.7%). A. palmatum var. sanguineum showed the highest increase (41.7%) for MDA content. The highest increase of superoxide dismutase (SOD) activity represented in A. palmatum (26.1%) and the increase of ascorbate peroxidase (APX) activity ranged from 16.5% (A. ginnala) to 49.1% (A. palmatum var. sanguineum). A. mono showed the highest increase (376.6%) of glutathione reductase (GR) activity under ozone fumigation and A. buergerianum also represented high increase (42.3%) of GR activity. Catalse (CAT) activity increased in the leaves of A. ginnala, A. palmatun and A. palmatum var. sanguineum under ozone exposure, whereas A. buergerianum and A. mono decreased in comparison with control plants. In conclusion, physiological markers such as chlorophyll content and photosynthesis that responded sensitively to $O_3$ in maple trees were considered as the very important indicators in order to evaluate the tolerance against $O_3$ stress, and parameters were closely related with each other. Among anti oxidative enzymes, SOD and APX might be contributed to alleviate to $O_3$ toxicity through the increase of activity in all maple trees. Therefore, these compounds can be used as a biochemical maker to assess the stress tolerance to $O_3$.

키워드

참고문헌

  1. Agrawal, M., Krizek, D.T., Agrawal, S.B., Kramer, G.F., Lee, E.H., Mirecki, R.M. and Rowland, R.A. 1993. Influence of inverse day/night temperature on ozone sensitivity and selected morphological and physiological responses of cucumber. Journal of the American Society for Horticultural Science 118: 649-654
  2. Amthor, J.S. 1988. Growth and maintenance respiration in leaves of bean (Phaseolus vulgaris L.) exposed to ozone in open-top chambers in the field. New Phytologist 110: 319-325 https://doi.org/10.1111/j.1469-8137.1988.tb00268.x
  3. Anderson, P.D., Palmer, B., Houpis, J.L.J., Smith, M.K. and Pushnik, J.C. 2003. Chloroplastic responses of ponderosa pine (Pinus ponderosa) seedlings to ozone exposure. Environment International 29: 407-413 https://doi.org/10.1016/S0160-4120(02)00177-0
  4. Apel, K. and Hirt, H. 2004. Reactive oxygen species: oxidative stress and signal transduction. Annu. Rev. Plant Biol. 55: 373-399 https://doi.org/10.1146/annurev.arplant.55.031903.141701
  5. Asada, K. 1997. The role of ascorbate peroxidase and monodehydroascorbate reductase in $H_2O_2$ scavenging in plants. pp. 715-735. In: Scandalios, J.G. (Eds.) Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Cold Spring Harbor Lab, Plainview, New York
  6. Asada, K. and Takahashi, M. 1987. Production and scavenging of active oxygen in photosynthesis. pp. 227-287. In: Kyle, D.J., Osmond, C.B. and Arntzen, C.J. (Eds.) Photoinhibition: Topics in Photosynthesis, IX. Elsevier, Amsterdam
  7. Barness. J.D., Velissariou, D., Davison, A.W. and Holevas, C.D. 1990. Comparative ozone sensitivity of old and modem Greek cultivars of spring wheat. New Phytologist 116: 707-714 https://doi.org/10.1111/j.1469-8137.1990.tb00557.x
  8. Beauchamp, C. and Fridovichi, I. 1971. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44: 276-297 https://doi.org/10.1016/0003-2697(71)90370-8
  9. Bowler, C., Montagu, M.C. and Inz, D. 1992. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43: 83-116 https://doi.org/10.1146/annurev.pp.43.060192.000503
  10. Brunschon-Harti, S., Fangmeier, A. and Jager, H.J. 1995. Effects of ethylenediurea and ozone on the antioxidative systems in beans (Phaseolus vulgaris L.). Environmental Pollution 90: 95-103 https://doi.org/10.1016/0269-7491(94)00084-Q
  11. Carlberg, I. and Mannervik B. 1985. Glutathione reductase. Methods in Enzymology 113: 485-490
  12. Carnahan, J.E., Jenner, E.L. and Wat, E.K.W. 1978. Prevention of ozone injury to plants by a new protectant chemical. Phytopathology 68: 1225-1229 https://doi.org/10.1094/Phyto-68-1225
  13. Conklin, P.L. and Barth, C. 2004. Ascorbic acid, a familiar small molecule inter-wined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environment 27: 959- 970 https://doi.org/10.1111/j.1365-3040.2004.01203.x
  14. Della Torre, G., Ferranti, F., Lupattelli, M., Pocceschi, N., Figoli, A., Nali, C. and Lorenzini, G. 1998. Effects of ozone on morpho-anatomy and physiology of Hedera helix. Chemosphere 36: 651-656 https://doi.org/10.1016/S0045-6535(97)10102-3
  15. Dhindsa, R.S., Plumb-Dhindsa, P. and Thorpe, T.A. 1981. Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32: 93-101 https://doi.org/10.1093/jxb/32.1.93
  16. Dizengremel, P. 2001. Effects of ozone on the carbon metabolism of forest trees. Plant Physiology and Biochemistry 39: 729-742 https://doi.org/10.1016/S0981-9428(01)01291-8
  17. Elstner, E.F., Wagner, G.A. and Schutz, W. 1988. Activated oxygen in green plants in relation to stress situations. pp. 159-187. In: Randall, D.D., Blevins, D.G., Campbell, W.H. (Eds.), Current Topics Plant Biochemistry and Physiology, Vol. 7. Columbia Press, University of Missouri
  18. Farquhar, G.D., Caemmerer, von S. and Berry, J.A. 1980. A biochemical model of photosynthetic $CO_2$ assimilation in leaves of $C_3$ species. Planta. 149: 78-90 https://doi.org/10.1007/BF00386231
  19. Fiscus, E.L., Booker, F.L. and Burkey, K.O. 2005. Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant Cell Environ. 28: 997-1011 https://doi.org/10.1111/j.1365-3040.2005.01349.x
  20. Fossati, P., Prencipe, L. and Berti, G. 1980. Use of 3,5-dichloro-2-hydroxy benzenesulfonic acid /4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. The Clinical Chemistry Methodology 26: 227-231
  21. Foyer, C.H., Lelandais, M. and Kunert,. K.J. 1994. Photooxidative stress in plants. Physiologia Plantamm 92: 696-717 https://doi.org/10.1111/j.1399-3054.1994.tb03042.x
  22. Guidi, L., Nali, C. Lorenzini, G. and Soldatini, G.F. 1998. Photosynthetic response to ozone of two poplar clones showing different sensitivity. Chemosphere 36: 657-662 https://doi.org/10.1016/S0045-6535(97)10103-5
  23. Guidi, L.. Bongi, G., Ciompi, S. and Soldatini, G.F. 1999. In Vida faba leaves photoinhibition from ozone fumigation in light precedes a decrease in quantum yield of functional PSII centres. Journal of Plant Physiology 154: 167-172 https://doi.org/10.1016/S0176-1617(99)80205-3
  24. Han, S.H., Lee, J.C. Lee, W.Y., Park, Y. and Oh, C.Y. 2006a. Antioxidant characteristics in the leaves of 14 coniferous trees under field conditions. Journal of Korean Forest Society 95: 209-215
  25. Han, S.H., Lee, J.C., Oh, C.Y. and Kim, P.G 2006b. Antioxidant characteristics and phytoremediation potential of 27 texa of roadside trees at industrial complex area. Korean Journal of Agricultural and Forest Meteorology 8: 159-168
  26. Heath, R.L. and Parker, L. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125: 189-198 https://doi.org/10.1016/0003-9861(68)90654-1
  27. Heggestad, H.E. 1991. Origin of Bel-W3 Bel-C and Bel-B tobacco varieties and their use as indicators of ozone. Environmental Pollution 74: 246-291
  28. Hill, A.C. and Littlefield, N. 1969. Ozone. Effect on apparent photosynthesis rate of transpiration and stomatal closure in plants. Environmental Science and Technology 3: 52-55 https://doi.org/10.1021/es60024a002
  29. Iglesias, J.D., Calatayud, ., Barreno, E., Primo-Millo, E. and Talon, M. 2006. Responses of citrus plants to ozone: Leaf biochemistry, antioxidant mechanisms and lipid peroxidation. Plant Physiology and Biochemistry 44: 125-131 https://doi.org/10.1016/j.plaphy.2006.03.007
  30. Kendrick Jr., J.B., Darley, E.F. and Middleton, J.T. 1962. Chemotherapy for oxidant and ozone induced plant damage. Water Air Soil Pollution 6: 391-402
  31. Kim, P.G. and Lee, E.J. 2001. Ecophysiology of photosynthesis 1: Effects of light intensity and intercellular $CO_2$ pressure on photosynthesis. Korean Journal of Agricultural and Forest Meteorology. 3: 126-133
  32. Knudson, L.L., Tibbitts, T.W. and Edwards, G.E. 1977. Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiology 60: 606-608 https://doi.org/10.1104/pp.60.4.606
  33. Lee, E.H., Jersey, J.A., Gifford, C. and Bennett, J.H. 1984. Differential ozone tolerance in soybean and snap beans: analysis of ascorbic acid in $O_3$-susceptible and $O_3$-resistant cultivars by high performance liquid chromatography. Environmental and Experimental Botany 24: 331-341 https://doi.org/10.1016/0098-8472(84)90030-3
  34. Lee, J.C., Han, S.H., Kim, P.G, Jang, S.S. and Woo, S.Y. 2003. Growth, physiological responses and ozone uptake of five Betula species exposed to ozone. Korean Journal of Ecology. 26: 165-172 https://doi.org/10.5141/JEFB.2003.26.4.165
  35. Lee, J.C., Oh, C.Y., Han, S.H. and Kim, J.S. 2006. Difference in growth, SOD activity and MDA content between ozone tolerant and sensitive families of open-pollinated Pinus densiflora. Journal of Korean Forest Society 95: 323-327
  36. Lehnherr, B., Grandjean, A., Machler, F. and Fuhrer, J. 1987. The effect of ozone in ambient air on ribulose-bisphosphate carboxylase/oxygenase activity decreases photosynthesis and grain yield in wheat. Journal of Plant Physiology 130: 189-200 https://doi.org/10.1016/S0176-1617(87)80223-7
  37. Lichtenthaler, H.K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382 https://doi.org/10.1016/0076-6879(87)48036-1
  38. Ltz, C., Anegg, S., Gerant, D., Alaoui-Sosse, B., Gerard, J, and Dizengremel, P. 2000. Beech trees exposed to high $CO_2$ and to simulated summer ozone levels: effects on photosynthesis, chloroplast components and leaf enzyme activity. Physiologia Plantarum 109: 252-259 https://doi.org/10.1034/j.1399-3054.2000.100305.x
  39. Lyons, T, Plchi, M. Turcsanyi, E. and Barnes, J.D. 1999. Extracellular antioxidants: a protective screen against ozone? pp. 183-201. In: Agrawal, S.B. and Agrawal, M. (Eds.) Environmental Pollution and Plant Responses CRC/ Lewis Publishers, Boca Raton
  40. Manning, W.J., Feder, W.A. and Vardaro, P.M. 1974. Suppression of oxidant injury by benomyl: effects on yields of bean cultivars in the field. Journal of Environmental Quality 3: 1-3 https://doi.org/10.2134/jeq1974.00472425000300010001x
  41. Matyssek, R. and Innes, J.L. 1999. Ozone- a risk factor for forest trees and forests in Europe? Water Air Soil Pollution 116: 199-226 https://doi.org/10.1023/A:1005267214560
  42. Matyssek, R. and Sandermann, H. 2003. Impact of ozone on trees: an ecophysiological perspective. Prog. Botany 64: 349-404
  43. Mehlhorn, H., O'Shea, J.M. and Wellburn, A.R. 1990. Electron spin resonance evidence for deformation of free radicals in plants exposed to ozone. Physiologia Plantarum 79: 377-383 https://doi.org/10.1111/j.1399-3054.1990.tb06756.x
  44. Mikkelsen, T.N., Didell, B. and Ltz, C. 1995. Changes in pigment concentration and composition in Norway spruce induced by long-term exposure to low levels of zone. Environmental Pollution 87: 197-205 https://doi.org/10.1016/0269-7491(94)P2607-B
  45. Ministry of Environment. 2005. Annual Report of Air Quality in Korea 2004. 145p
  46. Moldau, H., Sober, J. and Sober, A. 1993. Impact of acute exposure on $CO_2$ uptake by two cultivars of Phaseolus vulgaris L. Photosynthetica 28: 133-141
  47. Nakano, Y., and Asada, K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology 22: 867-880
  48. Ormrod D.P., Black, V.J. and Unsworth, M.H. 1981. Depression of net photosynthesis in Vida faba L. exposed to sulphur dioxide and ozone. Nature (London) 291: 585-586 https://doi.org/10.1038/291585a0
  49. Ormrod, D.P. and Beckerson, D.W. 1986. Po1yamines. Horticultural Science 21: 1070-1071
  50. Pell, E.J. and Pearson, N.S. 1983. Ozone-induced reduction in quantity of ribulose-1,5-bisphosphate carboxylase in alfalfa foliage. Plant Physiology 73: 185-187 https://doi.org/10.1104/pp.73.1.185
  51. Pleijel, H., Norberg, P.A., Selldn, G. and Skrby, L. 1999. Tropospheric ozone decreases biomass production in radish plants (Raphanus sativus) grown in rural south-west Sweden. Environmental Pollution 106: 143-147 https://doi.org/10.1016/S0269-7491(99)00057-3
  52. Pleijel, H., Skrby, L., Ojanper, K. and Selldn, G. 1994. Exposure of oats, Avena sativa L. to filtered and unfiltered air in open-top chambers: effects on grain yield and quality. Environ Pollution 86: 129-134 https://doi.org/10.1016/0269-7491(94)90183-X
  53. Posthumus, A.C. 1991. Effects of air pollution on plants and vegetations. pp. 191-198. In: Rozema, J. and Verkleij, J.A.C. (Eds.), Ecological Responses to Environmental Stresses. Kluwer Academic Publishers, Netherlands
  54. Prince, A., Lucas, P.W. and Lea, P.J. 1990. Age dependent damage and glutathione metabolism in ozone fumigated barley: a leaf section approach. Journal of Experimental Botany 41: 1309-1317 https://doi.org/10.1093/jxb/41.10.1309
  55. Pye, J.M. 1988. Impact of ozone on tree growth and yield of trees: a review. Journal of Environmental Quality 17: 347-391 https://doi.org/10.2134/jeq1988.00472425001700030003x
  56. Ranieri, A., D'Urso, G., Nali, C., Lorenzini, G. and Soldatini, G.F. 1996. Ozone stimulates apoplastic antioxidant systems in pumpkin leaves. Physiologia Plantarum 97: 381-387 https://doi.org/10.1034/j.1399-3054.1996.970224.x
  57. Reich P.B. 1987. Quantifying plant response to ozone: a unifying theory. Tree Physiology 3: 63-91 https://doi.org/10.1093/treephys/3.1.63
  58. Reich, P.B. 1983. Effects of low concentrations of 03 on net photosynthesis, dark respiration, and chlorophyll contents in aging hybrid poplar leaves. Plant Physiology 73: 291-296 https://doi.org/10.1104/pp.73.2.291
  59. Reich, P.B. and Amundson, R.G. 1985. Ambient levels of ozone reduce net photosynthesis in tree and crop species. Science 230: 566-570 https://doi.org/10.1126/science.230.4725.566
  60. Robinson, D.C. and Wellburn, A.R. 1991. Seasonal changes in the pigments of Norway spruce, Picea abies Karst, and the influence of summer ozone exposure. Trans L. New Phytologist 119: 251-259 https://doi.org/10.1111/j.1469-8137.1991.tb01028.x
  61. Saitanis, C.J., Riga-Karandinos, A.N. and Karandinos, M.G. 2001. Effects of ozone on chlorophyll and quantum yield of tobacco (Nicotiana tabacum L.) varieties. Chemosphere 42: 945-953 https://doi.org/10.1016/S0045-6535(00)00158-2
  62. Sakaki, T., Kondo, N. and Sugahara, K. 1983. Breakdown of photosynthetic pigments and lipids in spinach leaves with ozone fumigation: role of active oxygens. Physiologia Plantarum 59: 28-34 https://doi.org/10.1111/j.1399-3054.1983.tb06566.x
  63. Sasek, T.W. and Richardson, C.J. 1989. Effects of chronic doses of ozone on loblolly pine: Photosynthetic characteristics in the third growing season. Forest Science 3: 745-755
  64. Schraudner, M., Langebartels, C. and Sandermann, Jr. H. 1997. Changes in the biochemical status of plant cells induced by the environmental pollutant ozone. Physiologia Plantarum 100: 274-280 https://doi.org/10.1111/j.1399-3054.1997.tb04783.x
  65. Skrby, L., Troeng, E. and Bostrm, C.A. 1987. Ozone uptake and effects on transpiration, net photosynthesis, and dark respiration in Scots pine. Forest Science 33: 801-808
  66. Soldatini, G.F., Nali, C., Guidi, L. and Lorenzini, G. 1998. Photosynthesis of Hedera canariensis var azorica variegated leaves as affected by ozone. Photosynthetica 35: 248-253
  67. Tanaka, K., Otsubo, T. and Kondo, N. 1982. Participation of hydrogen peroxide in the inactivation of Calvin-cycle SH enzymes in $SO_2$-fumigated spinach leaves. Plant Cell and Physiology 23: 1009-1018
  68. Tanaka, K., Suda, Y., Kondo, N. and Sugahara, K. 1985. $O_3$ tolerance and the ascorbate-dependent $H_2O_2$ decomposing system in chloroplasts. Plant Cell and Physiology 26: 1425-1431
  69. Warren, C.R., Lw, M., Matyssek, R. and Tausz, M. 2007. Internal conductance to $CO_2$ transfer of adult Fagus sylvatica: variation between sun and shade leaves and due to free-air ozone fumigation. Environmental and Experimental Botany 59: 130-138 https://doi.org/10.1016/j.envexpbot.2005.11.004
  70. Weber, H., Chetelat, A., Reymond, P. and Farme, E.E. 2004. Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J. 37: 877-888 https://doi.org/10.1111/j.1365-313X.2003.02013.x
  71. Welfare, K., Flowers, T.J., Taylor, G. and Yeo, A.R. 1996. Additive and antagonistic effects of ozone and salinity on the growth, ion contents and gas exchange of five varieties of rice Oryza sativa L. Environmental Pollution 92: 257-266 https://doi.org/10.1016/0269-7491(96)00003-6
  72. Winston, G.W. 1990. Physiochemical basis for free radical formation in cells: production and defense. pp. 5886. In: Alscher, R.G. and Cumming, J.R. (Eds.) Stress response in Plants: Adaptation and Acclimation mechanisms. Wiley Liss, New York
  73. Wolf, S.P., Gamer, A. and Dean, R.T. 1986. Free radical, lipids and protein degradation. Biochemical Science 11: 27-31 https://doi.org/10.1016/0968-0004(86)90228-8
  74. Xu, Z.Z. and Zhou, G.S. 2005. Effects of water stress on photosynthesis and nitrogen metabolism in vegetative and reproductive shoots of Leymus chinensis. Photosynthetica 43: 29-35
  75. Yoshida, M., Nouchi, Y. and Toyama, S. 1994. Studies on the role of active oxygen in ozone in injury to plant cells. I. Generation of active oxygen in rice protoplast exposed to ozone. Plant Science 95: 197-205 https://doi.org/10.1016/0168-9452(94)90093-0