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Induction and inhibition of cyclobutane pyrimidine dimer photolyase in etiolated cucumber (Cucumis sativus) cotyledons after ultraviolet irradiation depends on wavelength

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Abstract

Under polychromatic ultraviolet (UV) irradiation (maximum energy at 327 nm) the activity of DNA photolyase specific to cyclobutane pyrimidine dimers (CPDs), CPD photolyase, increased by an amount which depended on UV irradiance, and the level of CPD photolyase gene (CsPHR) transcripts temporarily increased before the activity reached a constant level. UV light (>320 nm) was more effective than visible light at increasing CPD photolyase activity. In contrast, monochromatic UV irradiation at wavelengths <300 nm increased the level of CsPHR transcripts similarly to irradiation at wavelengths >320 nm, but reduced CPD photolyase activity compared with the dark control. Exposure of a CPD photolyase solution to UV-C (254 nm) reduced enzyme activity and induced accumulation of H2O2. Addition of H2O2 to the enzyme solution also inactivated CPD photolyase activity. These results suggest the possibility that reactive oxygen species participate in the inactivation of CPD photolyase in cotyledons exposed to UV irradiation of <300 nm.

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Abbreviations

CPD:

Cyclobutane pyrimidine dimer

CTAB:

Hexadecyltrimethylammonium bromide

DTT:

Dithiothreitol

ELISA:

Enzyme-linked immunosorbent assay

PBS:

Phosphate-buffered saline

ROS:

Reactive oxygen species

RT-PCR:

Reverse transcription-polymerase chain reaction

References

  • A-H-Mackerness S, John CF, Jordan B, Thomas B (2001) Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 489:237–242

    Article  PubMed  CAS  Google Scholar 

  • Ahmad M, Jarillo JA, Klimczak LJ, Landry LG, Peng T, Last RL, Cashmore AR (1997) An enzyme similar to animal type II photolyases mediates photoreactivation in Arabidopsis. Plant Cell 9:199–207

    Article  PubMed  CAS  Google Scholar 

  • Blumthaler M, Ambach W (1990) Indication of increasing solar ultraviolet-B radiation flux in alpine regions. Science 248:206–208

    Article  PubMed  CAS  Google Scholar 

  • Britt AB (1996) DNA damage and repair in plants. Annu Rev Plant Physiol Plant Mol Biol 47:75–100

    Article  PubMed  CAS  Google Scholar 

  • Brosché M, Strid Å (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiol Plant 117:1–10

    Article  Google Scholar 

  • Buchholz G, Ehmann B, Wellmann E (1995) Ultraviolet light inhibition of phytochrome-induced flavonoid biosynthesis and DNA photolyase formation in mustard cotyledons (Sinapis alba L.). Plant Physiol 108:227–234

    PubMed  CAS  Google Scholar 

  • Dai Q, Yan B, Huang S, Liu X, Peng S, Miranda MLL, Chavez AQ, Vergara BS, Olszyk DM (1997) Response of oxidative stress defense systems in rice (Oryza sativa) leaves with supplemental UV-B radiation. Physiol Plant 101:301–308

    Article  CAS  Google Scholar 

  • Doyle JF, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133:1420–1428

    Article  PubMed  CAS  Google Scholar 

  • Gleason JF, Bhartia PK, Herman JR, McPerters R, Newman P, Stolarski RS, Flynn L, Labow G, Larko D, Seftor C, Wellemeyer C, Komhyr WD, Miller AJ, Planet W (1993) Record low global ozone in 1992. Science 260:523–526

    Article  CAS  PubMed  Google Scholar 

  • Hada M, Buchholz G, Hashimoto T, Nikaido O, Wellmann E (1999) Photoregulation of DNA photolyase in broom Sorghum seedlings. Photochem Photobiol 69:681–685

    Article  CAS  Google Scholar 

  • Hada M, Hino K, Buchholz G, Goss J, Wellmann E, Shin M (2000a) Assay of DNA photolyase activity in spinach leaves in relation to cell compartmentation—evidence for lack of DNA photolyase in chloroplasts. Biosci Biotechnol Biochem 64:1288–1291

    Article  CAS  Google Scholar 

  • Hada M, Iida Y, Takeuchi Y (2000b) Action spectra of DNA photolyases for photorepair of cyclobutane pyrimidine dimers in sorghum and cucumber. Plant Cell Physiol 41:644–648

    CAS  Google Scholar 

  • Hada M, Hino K, Takeuchi Y (2001) Development of UV defense mechanisms during growth of spinach seedlings. Plant Cell Physiol 42:784–787

    Article  PubMed  CAS  Google Scholar 

  • Hidema J, Kumagai T (1998) UVB-induced cyclobutyl pyrimidine dimer and photorepair with progress of growth and leaf age in rice. J Photochem Photobiol B 43:121–127

    Article  CAS  Google Scholar 

  • Ihara M, Yamamoto K, Ohnishi T (1987) Induction of phr gene expression by pyrimidine dimers in Escherichia coli. Photochem Photobiol 46:359–361

    PubMed  CAS  Google Scholar 

  • Langer B, Wellmann E (1990) Phytochrome induction of photoreactivating enzyme in Phaseolus vulgaris L. seedlings. Photochem Photobiol 52:861–863

    CAS  Google Scholar 

  • Mitani H, Shima A (1995) Induction of cyclobutane pyrimidine dimer photolyase in cultured fish cells by fluorescent light and oxygen stress. Photochem Photobiol 61:373–377

    PubMed  CAS  Google Scholar 

  • Mitani H, Uchida N, Shima A (1996) Induction of cyclobutane pyrimidine dimer photolyase in cultured cells by UVA and blue light. Photochem Photobiol 64:943–948

    PubMed  CAS  Google Scholar 

  • Mitchell DL (1988) The relative cytotoxicity of (6–4)photoproducts and cyclobutane dimers in mammalian cells. Photochem Photobiol 48:51–57

    Article  PubMed  CAS  Google Scholar 

  • Molina MJ, Rowland FS (1974) Stratospheric sink for chlorofluoromethanes: chlorine atom-catalysed destruction of ozone. Nature 249:810–812

    Article  CAS  Google Scholar 

  • Pang Q, Hays JB (1991) UV-B inducible and temperature-sensitive photoreactivation of cyclobutane pyrimidine dimers in Arabidopsis thaliana. Plant Physiol 95:536–543

    Article  PubMed  CAS  Google Scholar 

  • Quaite FE, Takayanagi S, Ruffini J, Sutherland JC, Sutherland BM (1994) DNA damage levels determine cyclobutyl pyrimidine dimer repair mechanisms in alfalfa seedlings. Plant Cell 6:1635–1641

    Article  PubMed  CAS  Google Scholar 

  • Ries G, Heller W, Puchta H, Sandermann H, Seidlitz HK, Hohn B (2000) Elevated UV-B radiation reduces genome stability in plants. Nature 406:98–101

    Article  PubMed  CAS  Google Scholar 

  • Sancar A (1994a) Mechanisms of DNA excision repair. Science 266:1954–1956

    Article  CAS  Google Scholar 

  • Sancar A (1994b) Structure and function of DNA photolyase. Biochemistry 33:2–9

    Article  CAS  Google Scholar 

  • Setlow RB (1974) The wavelengths in sunlight effective in producing skin cancer: A theoretical analysis. Proc Nat Acad Sci USA 71:3363–3366

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Nakajima N, Saji H, Kondo N (2002) Diurnal changes of cucumber CPD photolyase gene (CsPHR) expression and its physiological role in growth under UV-B irradiation. Plant Cell Physiol 43:342–349

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Murakami M, Nakajima N, Kondo N, Nikaido O (1996) Induction and repair of damage to DNA in cucumber cotyledons irradiated with UV-B. Plant Cell Physiol 37:181–187

    CAS  Google Scholar 

  • Takeuchi Y, Iida Y, Nakajima N, Nikaido O (2000) Formation of DNA lesions in cucumber cotyledons exposed to solar UV radiation. Environ Sci 13:351–355

    CAS  Google Scholar 

  • Taylor RM, Nikaido O, Jordan BR, Rosamond J, Bray CM, Tobin AK (1996) Ultraviolet-B-induced DNA lesions and their removal in wheat (Triticum aestivum L.) leaves. Plant Cell Environ 19:171–181

    Article  CAS  Google Scholar 

  • Taylor RM, Tobin AK, Bray CM (1997) DNA damage and repair in plants. In: Lumsden PJ (ed) Plants and UV-B: responses to environmental change. Cambridge University Press, Cambridge, pp. 53–76

    Google Scholar 

  • Todo T (1999) Functional diversity of the DNA photolyase/blue light receptor family. Mut Res 434:89–97

    CAS  Google Scholar 

  • Warm E, Laties GG (1982) Quantification of hydrogen peroxide in plant extracts by the chemiluminescence reaction with luminol. Phytochemistry 21:827–831

    Article  CAS  Google Scholar 

  • Watanabe K, Yamada N, Takeuchi Y (2006) Oxidative DNA damage in cucumber cotyledons irradiated with ultraviolet light. J Plant Res 119:239–246

    Article  PubMed  CAS  Google Scholar 

  • Watanabe M, Furuya M, Miyoshi Y, Inoue Y, Iwahashi I, Matsumoto K (1982) Design and performance of the Okazaki Large Spectrograph for photobiological research. Photochem Photobiol 36:491–498

    CAS  Google Scholar 

  • Waterworth WM, Jiang Q, West CE, Nikaido M, Bray CM (2002) Characterization of Arabidopsis photolyase enzymes and analysis of their role in protection from ultraviolet-B radiation. J Exp Bot 53:1005–1015

    Article  PubMed  CAS  Google Scholar 

  • Yasui A, Eker APM, Yasuhira S, Yajima H, Kobayashi T, Takao M, Oikawa A (1994) A new class of DNA photolyases present in various organisms including aplacental animals. EMBO J 13:6143–6151

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Irradiation with monochromatic UV light was performed under the Cooperative Research Program of the National Institute for Basic Biology for the Okazaki large spectrograph. We thank Dr M. Watanabe and Mr S. Higashi of the Large Spectrograph Laboratory at the National Institute for Basic Biology for assistance with UV irradiation. This work was supported in part by Grants-in-Aid from the Japan Society for the Promotion of Science (Research for the Future Program, JSPS-RFTF96L00602) and from the Global Environment Research Fund of the Environment Agency of Japan.

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Correspondence to Yuichi Takeuchi.

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Takeuchi, Y., Inoue, T., Takemura, K. et al. Induction and inhibition of cyclobutane pyrimidine dimer photolyase in etiolated cucumber (Cucumis sativus) cotyledons after ultraviolet irradiation depends on wavelength. J Plant Res 120, 365–374 (2007). https://doi.org/10.1007/s10265-006-0065-9

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