Differential Expression of Three Catalase Genes in Hot Pepper (Capsicum annuum L.)

  • Lee, Sang Ho (School of Biological Sciences, Chungnam National University) ;
  • An, Chung Sun (School of Biological Sciences, Seoul National University)
  • Received : 2005.05.26
  • Accepted : 2005.06.09
  • Published : 2005.10.31

Abstract

Three different catalase cDNA clones (CaCat1, CaCat2, and CaCat3) were isolated from hot pepper (Capsicum annuum L.), and their expression patterns were analyzed at the levels of mRNA and enzyme activity. Northern hybridization showed that the three catalase genes were differentially expressed in various organs, and that expression of CaCat1 and CaCat2 was regulated differently by the circadian rhythm. In situ hybridization revealed different spatial distributions of CaCat1 and CaCat2 transcripts in leaf and stem. In response to wounding and paraquat treatment, CaCat1 mRNA increased at 4-12 h in both paraquat-treated and systemic leaves. In contrast, wounding had no significant effect on expression of the catalase genes. The increase of catalase activity in the paraquat-treated and systemic leaves paralleled that of CaCat1 mRNA, but did not match that of CaCat1 mRNA in paraquat-treated stems. Our results suggest that CaCat1 may play a role in responses to environmental stresses.

Keywords

Acknowledgement

Supported by : Korean Foundation of Science and Technology

References

  1. Acevedo, A. and Scandalios, J. G. (1991) Catalase and superoxide dismutase gene expression and distribution during stem development in maize. Dev. Genet. 12, 423-430 https://doi.org/10.1002/dvg.1020120607
  2. Anderson, M. D., Prasad, T. K., and Stewart, C. R. (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol. 109, 1247-1257
  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
  4. Bailly, C., Leymarie, J., Lehner, A., Rousseau, S., Come, D., et al. (2004) Catalase activity and expression in developing sunflower seeds as related to drying. J. Exp. Bot. 55. 475-483 https://doi.org/10.1093/jxb/erh050
  5. Bethke, P. C. and Jones, R. L. (2001) Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 25, 19-29 https://doi.org/10.1046/j.1365-313x.2001.00930.x
  6. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantity of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  7. Brisson, L. F., Zelitch, I., and Havir, E. A. (1998) Manipulation of catalase levels produces altered photosynthesis in transgenic tobacco plants. Plant Physiol. 116, 259-269 https://doi.org/10.1104/pp.116.1.259
  8. Chen, Z., Iyer, S., Caplan, A., Klessig, D. F., and Fan, B. (1997) Differential accumulation of salicylic acid and salicylic acidsensitive catalase in different rice tissues. Plant Physiol. 114, 193-201
  9. Cox, K. H. and Goldberg, R. B. (1988) Analysis of plant gene expression; in Plant Molecular Biology: A Practical Approach, Shaw C. H. (ed.), pp. 1-35. IRL Press, Oxford
  10. Dat, J., Vandenbeele, S., Vranova, E., Van Montagu, M., Inze, D., et al. (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol. Life Sci. 57, 779-795 https://doi.org/10.1007/s000180050041
  11. Drory, A. and Woodson, W. R. (1992) Molecular cloning and nucleotide sequence of a cDNA encoding catalase from tomato. Plant Physiol. 100, 1605-1606 https://doi.org/10.1104/pp.100.3.1605
  12. Durner, J. and Klessig, D. F. (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J. Biol. Chem. 271, 28492-28501 https://doi.org/10.1074/jbc.271.45.28492
  13. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., et al. (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15, 1212-1226 https://doi.org/10.1105/tpc.009464
  14. Esaka, M., Yamada, N., Kitabayashi, M., Setoguchi, Y., Tsugeki, R., et al. (1997) cDNA cloning and differential gene expression of three catalases in pumpkin. Plant Mol. Biol. 33, 141-155 https://doi.org/10.1023/A:1005742916292
  15. Frugoli, J. A., Zhong, H. H., Nuccio, M. L., Mccourt, P., Mcpeek, M. A., et al. (1996) Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 112, 327-336 https://doi.org/10.1104/pp.112.1.327
  16. Gould, S. F., Keller, G.-A., Schneider, M., Howell, S. H., Garrard, L. J., et al. (1990) Peroxisomal protein import is conserved between yeast, plants, insects and mammals. EMBO J. 9, 85-90
  17. Grant, J. J. and Loake, G. J. (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124, 21-29 https://doi.org/10.1104/pp.124.1.21
  18. Guan, L. M., Zhao, J., and Scandalios, J. G. (2000) Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: $H_2O_2$ is the likely intermediary signaling molecule for the response. Plant J. 22, 87-95 https://doi.org/10.1046/j.1365-313x.2000.00723.x
  19. Halliwell, B. (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplast. Chem. Phys. Lipids 44, 327-340 https://doi.org/10.1016/0009-3084(87)90056-9
  20. Halliwell, B. and Gutteridge, J. M. C. (1999) Oxidative stress: adaptation, damage, repair and death; in Free Radicals in Biology and Medicine, Halliwell, B. (ed.), pp. 246?350, Oxford University Press, Oxford
  21. Harmer, S. L., Hogenesch, J. B., Straume, M., Chang, H., Han, B., et al. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113 https://doi.org/10.1126/science.290.5499.2110
  22. Iwamoto, M., Higo, H., and Higo, K. (2000) Differential diurnal expression of rice catalase genes: the 5-flanking region of CatA is not sufficient for circadian control. Plant Sci. 151, 39-46 https://doi.org/10.1016/S0168-9452(99)00194-6
  23. Jung, M. Y., Bock, J. Y., Baik, S. O., Lee, J. H., and Lee, T. K. (1999) Effects of roasting on pyrazine contents and oxidative stability of red pepper seed oil prior to its extraction. J. Agric. Food Chem. 47, 1700-1704 https://doi.org/10.1021/jf981028l
  24. Kreps, J. A., Wu, Y., Chang, H., Zhu, T., Wang, X., et al. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129-2141 https://doi.org/10.1104/pp.008532
  25. Kwon, S. I. and An, C. S. (2001) Molecular cloning, characterization and expression analysis of a catalase cDNA from hot pepper (Capsicum annuum L.). Plant Sci. 160, 961-969 https://doi.org/10.1016/S0168-9452(01)00332-6
  26. Mackhann, H. I. and Hirsch, A. M. (1993) In situ localization of specific mRNAs in plant tissues; in Methods in Plant Molecular Biology and Biotechnology, Glick, B. R. and Thompson, J. E. (eds.), pp. 179-205, CRC Press, Boca Raton
  27. Mcclung, C. R. (1997) Regulation of catalases in Arabidopsis. Free Radic. Biol. Med. 23, 489-496 https://doi.org/10.1016/S0891-5849(97)00109-3
  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. Mullineaux, P. and Karpinski, S. (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr. Opin. Plant Biol. 5, 43-48 https://doi.org/10.1016/S1369-5266(01)00226-6
  30. Ni, W. and Trelease, R. N. (1991) Post-transcriptional regulation of catalase isozyme expression in cotton seeds. Plant Cell 3, 737-744 https://doi.org/10.1105/tpc.3.7.737
  31. Orendi, G., Zimmermann, P., Baar, C., and Zentgraf, U. (2001) Loss of stress-induced expression of catalase3 during leaf senescence in Arabidopsis thaliana is restricted to oxidative stress. Plant Sci. 161, 301-314 https://doi.org/10.1016/S0168-9452(01)00409-5
  32. Orozco-Cardenas, M. and Ryan, C. A. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96, 6553-6557
  33. Prasad, T. K., Anderson, M. D., and Stewart, C. R. (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol. 105, 619-627
  34. Rao, M. V., Paliyath, G., and Ormrod, D. P. (1996) Ultraviolet- B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol. 110, 125-136 https://doi.org/10.1104/pp.110.1.125
  35. Scandalios, J. G., Guan, L., and Polidoros, A. N. (1997) Catalases in plants; in Oxidative Stress and the Molecular Biology of Antioxidant Defenses, Sacandalios, J. G. (ed.), pp. 343-406, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
  36. Taylor, N. L., Day, D. A., and Millar, A. H. (2002) Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J. Biol. Chem. 277, 42663-42668 https://doi.org/10.1074/jbc.M204761200
  37. Willekens, H., Langebartels, C., Tire, C., Van Montagu, M., Inze, D., et al. (1994a) Differential expression of catalase genes in Nicotiana plumbaginifolia (L.). Proc. Natl. Acad. Sci. USA 91, 10450-10454
  38. Willekens, H., Van Camp, W., Van Montagu, M., Inze, D., Langebartels, C., et al. (1994b) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol. 106, 1007-1014
  39. Willekens, H., Villarroel, R., Van Montagu, M., Inze, D., and Van Camp, W. (1994c) Molecular identification of catalases from Nicotiana plumbaginifolia (L.). FEBS Lett. 352, 79-83 https://doi.org/10.1016/0014-5793(94)00923-6
  40. Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., et al. (1997) Catalase is a sink for $H_2O_2$ and is indispensable for stress defence in C3 plants. EMBO J. 16, 4806-4816 https://doi.org/10.1093/emboj/16.16.4806
  41. Yi, S., Yu, S., and Choi, D. (1999) Molecular cloning of a catalase cDNA from Nicotiana glutinosa L. and its repression by tobacco mosaic virus infection. Mol. Cells 9, 320-325
  42. Yi, S., Yu, S., and Choi, D. (2003) Involvement of hydrogen peroxide in repression of catalase in TMV-infected resistang tobacco. Mol. Cells 15, 364-369
  43. Zhong, H. H. and McClung, C. R. (1996) The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol. Gen. Genet. 251, 196-203
  44. Zhong, H. H., Young, J. C., Pease, E. A., Hangarter, R. P., and McClung, C. R. (1994) Interactions between light and the circadian clock in the regulation of CAT2 expression in Arabidopsis. Plant Physiol. 104, 889-898