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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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The Activities of Antioxidant Enzymes in Response to Oxidative Stresses and Hormones in Paraquat-tolerant Rehmannia glutinosa Plants

  • Choi, Dong-Geun (Department of Horticulture, Jeollabuk-do Agricultural Research and Extension Services) ;
  • Yoo, Nam-Hee (Institute of Agricultural Science and Technology, Chonbuk National University) ;
  • Yu, Chang-Yeon (Division of Applied Plant Sciences, Kangwon Natl University) ;
  • De Los Reyes, Benildo (Department of Biological Sciences, Univ. of Maine) ;
  • Yun, Song-Joong (Institute of Agricultural Science and Technology, Chonbuk National University)
  • Published : 2004.09.30
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Abstract

All members of R. glutinosa show the unique characteristic of intrinsic tolerance to paraquat (PQ). Antioxidant enzymes have been proposed to be the primary mechanism of PQ resistance in several plant species. Therefore, the antioxidant enzyme systems of R. glutinosa were evaluated by comparatively analyzing cellular antioxidant enzyme levels, and their responses of oxidative stresses and hormones. The levels of ascorbate peroxidase (APX), glutathione reductase (GR), non-specific peroxidase (POX), and superoxide dismutase (SOD) were 7.3-, 4.9-, 2.7- and 1.6-fold higher in PQ-tolerant R. glutinosa than in PQ-susceptible soybeans. However, the activity of catalase (CAT) was about 12-fold higher in the soybeans. The activities of antioxidant enzymes reduced after PQ treatment in the two species, with the exception of POX and SOD in R. glutinosa, which increased by about 40%. Interestingly, the activities of APX, SOD and POX in R. glutinosa, relative to those in soybeans, were further increased by 49, 67 and 93% after PQ treatment. The considerably higher intrinsic levels, and increases in the relative activities of antioxidant enzymes in R. glutinosa under oxidative stress support the possible role of these enzymes in the PQ tolerance of R. glutinosa. However, the relatively lower levels of SOD versus PQ tolerance, and the mixed responses of antioxidant enzymes to stresses and hormones, suggest a possible alternative mechanism(s) for PQ tolerance in R. glutinosa.

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References

  1. Allen, R. D., Webb, R. P. and Schake, S. A. (1997) Use of transgenic plants to study antioxidant defense. Free Rad. Biol. Med. 23, 473-479. https://doi.org/10.1016/S0891-5849(97)00107-X
  2. Aono, M., Saji, H., Sakamoto, A., Tanaka, K., Kondo, N. and Tanaka, K. (1995) Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase. Plant Cell Physiol. 36, 1687-1691.
  3. Asada, K. and Takahashi, M. (1987) Production and scavenging of active oxygen in photosynthesis; in Photoinhibition, Kyle, D. J., Osmond, C. B. and Arntzen, C. J. (eds.), pp. 227-287, Elsevier, Amsterdam, Netherlands.
  4. Baek, S. H., Kwon, I. S., Park T. I., Yun, S. J., Kim, J. K. and Choi, K. G. (2000) Activities and isozyme profiles of antioxidant enzymes in intercellular compartment of overwintering barley leaves. J. Biochem. Mol. Biol. 33, 385-390.
  5. Beers, R. F. and Sizer, I. W. (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133-140.
  6. Bradford, M. M. (1979) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
  7. Chance, B. and Maehly, A. C. (1955) Assay of catalase and peroxidase. Methods Enzymol. 2, 764-775. https://doi.org/10.1016/S0076-6879(55)02300-8
  8. Chun, J. C., Kim, J. C., Hwang, I. T. and Kim, S. E. (2002) Acteoside from Rehmannia glutinosa nullifies paraquat activity in Cucumis sativus. Pestic. Biochem. Physiol. 72, 153-159. https://doi.org/10.1016/S0048-3575(02)00008-1
  9. Chun, J. C., Ma, S. Y., Kim, S. E. and Lee, H. J. (1997) Physiological responses of Rehmannia glutinosa to paraquat and its tolerance mechanisms. Pestic. Biochem. Physiol. 59, 51-63. https://doi.org/10.1006/pest.1997.2307
  10. Chung, I. M., Park, M. R., Chun, J. C. and Yun, S. J. (2003) Resveratrol accumulation and resveratrol synthase gene expression in response to abiotic stresses and hormones in peanut plants. Plant Sci. 164, 103-109. https://doi.org/10.1016/S0168-9452(02)00341-2
  11. Dixon, D., Cummins, I., Cole, D. J. and Edwards, R. (1998) Glutathione-mediated detoxification systems in plants. Curr. Opin. Plant Biol. 1, 258-266. https://doi.org/10.1016/S1369-5266(98)80114-3
  12. Donahue, J. L., Okpodu, C. M., Cramer, C. L., Grabau, E. A. and Alscher, R. G. (1997) Response of antioxidants to paraquat in pea leaves. Relationships to resistance. Plant Physiol. 113, 249-257.
  13. Fodor, J., Gullner, G., Adam, A. L., Barna, B., Komives, T. and Kiraly, Z. (1997) Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Role in systemic acquired resistance. Plant Physiol. 114, 1443-1451.
  14. Foyer, C., Descourvieres, P, and Kunert, K. J. (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ. 17, 507-523. https://doi.org/10.1111/j.1365-3040.1994.tb00146.x
  15. Fuerst, E. P. and Vaughn, K. C. (1990) Mechanisms of paraquat resistance. Weed Technol. 4, 150-156.
  16. Ganesan, V. and Thomas, G. (2001) Salicylic acid response in rice: influence of salicylic acid on $H_2O_2$ accumulation and oxidative stress. Plant Sci. 160, 1095-1106. https://doi.org/10.1016/S0168-9452(01)00327-2
  17. Gao, J. J., Igalashi, K. and Nukina, M. (1999) Radical scavenging activity of phenylpropanoid glycosides in Caryopteris incana. Biosci. Biotech. Biochem. 63, 983-988. https://doi.org/10.1271/bbb.63.983
  18. Hart, J. J. and DiTomaso, M. (1994) Sequestration and oxygen radical detoxification as mechanisms of paraquat resistance. Weed Sci. 42, 277-284.
  19. Hodges, D. M. and Forney, C. F. (2000) The effects of ethylene, depressed oxygen and elevated carbon dioxide on antioxidant profiles of senescing spinach leaves. J. Exp. Bot. 51, 645-655. https://doi.org/10.1093/jexbot/51.344.645
  20. Kim, J. S. and Chun, J. C. (1992) Resistance of the medicinal plant jiwhang (Rehmannia glutinosa) to paraquat. Korean J. Weed Sci. 12, 374-378.
  21. Kurepa, J., Herouart, D., Van Montagu, M. and Inze, 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. https://doi.org/10.1093/oxfordjournals.pcp.a029190
  22. Lasat, M. M., DiTomaso, J. M., Hart, J. J. and Kochian, L. V. (1997) Evidence for vacuolar sequestration of paraquat in roots of a paraquat-resistant Hordeum glaucum biotype. Physiol. Plant. 99, 255-262. https://doi.org/10.1111/j.1399-3054.1997.tb05410.x
  23. Lee, H. Y., Eum, W. S., Kim, D. W., Lee, B. R., Yoon, C. S., Jang, S. H., Choi, H. S., Choi, S. H., Baek, N.-I., Kang, J. H., Kang, T.-C., Won, M. H., Cho, S.-W., Lee, K. S., Park, J., and Choi, S. Y. (2003) Isolation and Identification of an Antioxidant Enzyme Catalase Stimulatory Compound from Garnoderma lucidum. J. Biochem. Mol. Biol. 36, 450-455. https://doi.org/10.5483/BMBRep.2003.36.5.450
  24. Liu, M. J., Li, K. X., Guo, H. Z., Lee, K. M., Qin, L. and Chan, K. M. (2003) The effects of verbascoside on plasma lipid peroxidation level and erythrocyte membrane fluidity during immobilization in rabbits: a time course study. Life Sci. 73, 883-892. https://doi.org/10.1016/S0024-3205(03)00354-0
  25. Mano, J., Ohno, C., Domae, Y. and Asada, K. (2001) Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ESR. Biochem. Biophys. Acta. 1504, 275-287. https://doi.org/10.1016/S0005-2728(00)00256-5
  26. Matters, G. L. and Scandalios, J.G. (1986) Effect of the free radical-generating herbicide paraquat on the expression of the superoxide dismutase (Sod) genes in maize. Biochim. Biophys. Acta. 3, 29-38.
  27. Melhorn, H. (1990) Ethylene-promoted ascorbate peroxidase activity protects plants against hydrogen peroxide, ozone and paraquat. Plant Cell Environ. 13, 971-976. https://doi.org/10.1111/j.1365-3040.1990.tb01988.x
  28. Mittler, R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410. https://doi.org/10.1016/S1360-1385(02)02312-9
  29. Miyagawa, Y., Tamoi, M. and 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. https://doi.org/10.1093/pcp/41.3.311
  30. Nakano, Y. and Asada, K. (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22, 867-880.
  31. Norman, M. A., Fuerst, E. P., Smeda, R. J. and Vaughn, K. C. (1993) Evaluation of paraquat resistance mechanisms in Conyza. Pestic. Biochem. Physiol. 46, 236-249. https://doi.org/10.1006/pest.1993.1055
  32. Nebot, C., Moutet, M., Huet, P., Xu, J. Z., Yadan, J. C. and Chaudiere, J. (1993) Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Anal. Biochem. 214, 442-452. https://doi.org/10.1006/abio.1993.1521
  33. Oberley, L. W. and Spitz, D. R. (1984) Assay of superoxide dismutase activity in tumor tissue. Methods Enzymol. 105, 457-464. https://doi.org/10.1016/S0076-6879(84)05064-3
  34. O'Kane, D., Gill, V., Boyd, P. and Burdon, R. (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198, 371-377. https://doi.org/10.1007/BF00620053
  35. Okuda, T., Matsuda, Y., Sugawara, M. and Sagisaka, S. (1992) Metabolic response to treatment with cold, paraquat, or 3-amino-1,2,4-triazole in leaves of winter wheat. Biosci. Biotechnol. Biochem. 56, 1911-1915. https://doi.org/10.1271/bbb.56.1911
  36. Preston, C. (1994) Resistance to photosystem I disrupting herbicides; in Herbicide Resistance in Plants: Biology and Biochemistry, Powles, S. B. and Holtum, J. A. M. (eds.), pp. 61-82, Lewis Publishers, Boca Raton, USA.
  37. Rao, M. V., Paliyath, G., Ormrod, D. P., Murr, D. P. and Watkins, C. B. (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and $H_2O_2$-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires $H_2O_2$. Plant Physiol. 115, 137-149. https://doi.org/10.1104/pp.115.1.137
  38. Rice-Evans, C. A., Miller, N. J. and Paganga, G. (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci. 2, 152-159. https://doi.org/10.1016/S1360-1385(97)01018-2
  39. Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J. E., Rodermel, S., Inze, D. and Mittler, R. (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 32, 329-342. https://doi.org/10.1046/j.1365-313X.2002.01427.x
  40. Soar, C. J., Karotam, J., Preston, C. and Powles, S. B. (2003) Reduced paraquat translocation in paraquat resistant Arctotheca calendula (L.) Levyns is a consequence of the primary resistance mechanism, not the cause. Pestic. Biochem. Physiol. 76, 91-98. https://doi.org/10.1016/S0048-3575(03)00069-5
  41. Summer-Matter, K., Sticher, L. and Metraux, J. P. (1995) Systemic response in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv syringae. Plant Physiol. 108, 1379-1385.
  42. Sylvestre, I., Droillard, M. J., Bureau, J. M. and Paulin, A. (1989) Effects of the ethylene rise on the peroxidation of membrane lipids during the senescence of cut carnations. Plant Physiol. Biochem. 27, 407-413.
  43. Tsang, E. W., Bowler, C., Herouart, D., Van Camp, W., Villarroel, R., Genetello C., Van Montagu, M. and Inze, D. (1991) Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3, 783-792. https://doi.org/10.1105/tpc.3.8.783
  44. Van Breusegem, F,. Slooten, L., Stassart, J. M., Moens, T., Botterman, J., Van Montagu, M. and Inze, D. (1999) Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol. 40, 515-523. https://doi.org/10.1093/oxfordjournals.pcp.a029572
  45. Vartak, V. and Bhargava, S. (1999) Photosynthetic performance and antioxidant metabolism in a paraquat-resistant mutant of Chlamydomonas reinhardtii L. Pestic. Biochem. Physiol. 64, 9-15. https://doi.org/10.1006/pest.1999.2405
  46. Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., Van Montagu, M. and Van Camp, W. (1997) Catalase is a sink for $H_2O_2$ and is indispensable for stress defense in C-3 plants. EMBO J. 16, 4806-4816. https://doi.org/10.1093/emboj/16.16.4806
  47. Ye, B. and Gressel, J. (1994) Constitutive variation of ascorbate peroxidase activity during development parallels that of superoxide dismutase and glutathione reductase in paraquatresistant Conyza. Plant Sci. 102, 147-151. https://doi.org/10.1016/0168-9452(94)90032-9
  48. Ye, B. and Gressel, J. (2000) Transient, oxidant-induced antioxidant transcript and enzyme levels correlate with greater oxidant-resistance in paraquat-resistant Conyza bonariensis. Planta 211, 50-61. https://doi.org/10.1007/s004250000257
  49. Yun, Y. S. and Lee, Y. N. (2003) Production of superoxide dismutase by Deinococcus radiophilous. J. Biochem. Mol. Biol. 36, 282-287. https://doi.org/10.5483/BMBRep.2003.36.3.282

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