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Elevated UV-B radiation reduces genome stability in plants

Abstract

Long-term depletion of the stratospheric ozone layer contributes to an increase in terrestrial solar ultraviolet-B radiation1,2,3. This has deleterious effects on living organisms, such as DNA damage4,5. When exposed to elevated ultraviolet-B radiation (UV-B; 280–315 nm), plants display a wide variety of physiological and morphological responses characterized as acclimation and adaptation6. Here we show, using special sun simulators, that elevated solar UV-B doses increase the frequency of somatic homologous DNA rearrangements in Arabidopsis and tobacco plants. Increases in recombination are accompanied by a strong induction of photolyase and Rad51 gene expression. These genes are putatively involved in major DNA repair pathways, photoreactivation and recombination repair7,8. In mutant Arabidopsis plants that are deficient in photoreactivating ultraviolet-induced cyclobutane pyrimidine dimers, recombination under elevated UV-B regimes greatly exceeds wild-type levels. Our results show that homologous recombination repair pathways might be involved in eliminating UV-B-induced DNA lesions in plants. Thus, increases in terrestrial solar UV-B radiation as forecasted for the early 21st century may affect genome stability in plants.

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Figure 1: Transgenic Arabidopsis thaliana plants (line A11) grown under different daily UV-B doses.
Figure 2: UV-B acclimation responses in Arabidopsis thaliana line A651 grown under different daily UV-B doses.

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References

  1. Kerr, J. & McElroy, C. Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262, 1032–1034 (1993).

    Article  ADS  CAS  Google Scholar 

  2. Madronich, S., McKenzie, R. L., Björn, L. O. & Caldwell, M. M. Changes in biologically active ultraviolet radiation reaching the earth's surface. J. Photochem. Photobiol. B 46, 5–19 (1998).

    Article  CAS  Google Scholar 

  3. McKenzie, R., Connor, B. & Bodeker, G. Increased summertime UV radiation in New Zealand in response to ozone loss. Science 285, 1709 –1711 (1999).

    Article  CAS  Google Scholar 

  4. Rozema, J., van de Staaij, J., Björn, L. O. & Caldwell, M. M. UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol. Evol. 12, 22–28 (1997).

    Article  CAS  Google Scholar 

  5. Rousseaux, M. C. et al. Ozone depletion and UVB radiation: Impact on plant DNA damage in southern South America. Proc. Natl Acad. Sci. USA 96, 15310–15315 (1999).

    Article  ADS  CAS  Google Scholar 

  6. Jansen, M. A. K., Gaba, V. & Greenberg, B. M. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3, 131–135 (1998).

    Article  Google Scholar 

  7. Britt, A. B. Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 4, 20–24 ( 1999).

    Article  CAS  Google Scholar 

  8. Vispe, S., Cazaux, C., Lesca, C. & Defais, M. Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res. 26, 2859–2864 (1998).

    Article  CAS  Google Scholar 

  9. Tevini, M. in UV-B Radiation and Ozone Depletion: Effects on Humans, Animals and Plants, Microorganisms and Materials (ed. Tevini, M.) 125– 153 (CRC Press, Boca Raton: Lewis Publishers, USA, 1993).

    Google Scholar 

  10. Puchta, H. & Hohn, B. From centiMorgans to base pairs: homologous recombination in plants. Trends Plant Sci. 1, 340–348 (1996).

    Article  Google Scholar 

  11. Caldwell, M. M., Flint, S. & Searles, P. S. Spectral balance and UV-B sensitivity of soybean: a field experiment. Plant Cell Environ. 17, 267–276 (1994).

    Article  Google Scholar 

  12. Döhring, T., Köfferlein, M., Thiel, S. & Seidlitz, H. K. Spectral shaping of artificial UV-B irradiation for vegetation stress research. J. Plant Physiol. 148, 115– 119 (1996).

    Article  Google Scholar 

  13. Caldwell, M. M. in Photophysiology Vol. 6 (ed. Giese, A. C.) 131 –177 (Academic, New York, 1971).

    Book  Google Scholar 

  14. Swoboda, P., Gal, S., Hohn, B. & Puchta, H. Intrachromosomal homologous recombination in whole plants. EMBO J. 13 , 484–489 (1994).

    Article  CAS  Google Scholar 

  15. Puchta, H., Swoboda, P., Gal, S., Blot, M. & Hohn, B. Somatic intrachromosomal homologous recombination events in populations of plant siblings. Plant Mol. Biol. 28, 281 –292 (1995).

    Article  CAS  Google Scholar 

  16. Tovar, J. & Lichtenstein, C. Somatic and meiotic chromosomal recombination between inverted duplications in transgenic tobacco plants. Plant Cell 4, 319–332 (1992).

    Article  CAS  Google Scholar 

  17. Gale, J. M. & Smerdon, M. J. UV induced (6-4) photoproducts are distributed differently than cyclobutane dimers in nucleosomes. Photochem. Photobiol. 51, 411–417 (1990).

    Article  CAS  Google Scholar 

  18. Suter, B., Livingstone-Zatchej, M. & Thomas, F. Chromatin structure modulates DNA repair by photolyase in vivo. EMBO J. 16, 2150–2160 (1997).

    Article  CAS  Google Scholar 

  19. Landry, L. G. et al. An Arabidopsis photolyase mutant is hypersensitive to ultraviolet-B radiation. Proc. Natl Acad. Sci. USA 94, 328–332 (1997).

    Article  ADS  CAS  Google Scholar 

  20. Mount, D. W. Reprogramming transcription. Nature 383, 763–764 (1996).

    Article  ADS  CAS  Google Scholar 

  21. Stapleton, A. E. & Walbot, V. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiol. 105, 881–889 (1994).

    Article  CAS  Google Scholar 

  22. Landry, L. G., Chapple, C. C. & Last, R. L. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol. 109, 1159–1166 ( 1995).

    Article  CAS  Google Scholar 

  23. Shinohara, A., Ogawa, H. & Ogawa, T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457–470 (1992).

    Article  CAS  Google Scholar 

  24. Doutriaux, M. P., Couteau, F., Bergounioux, C. & White, C. Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol. Gen. Genet. 257, 283– 291 (1998).

    Article  CAS  Google Scholar 

  25. Walbot, V. On the life strategies of plants and animals. Trends Genet. 1, 165–169 (1985).

    Article  Google Scholar 

  26. Jackson, J. F. DNA repair in pollen. A review. Mutat. Res. 181, 17–29 (1987).

    Article  CAS  Google Scholar 

  27. Walbot, V. UV-B damage amplified by transposons in maize. Nature 397, 398–399 (1999).

    Article  ADS  CAS  Google Scholar 

  28. Quaite, F. E., Sutherland, B. M. & Sutherland, J. C. Action spectrum for DNA damage in alfalfa lowers predicted impact of ozone depletion. Nature 358, 576–578 (1992).

    Article  ADS  CAS  Google Scholar 

  29. Stapleton, A. E., Mori, T. & Walbot, V. A simple and sensitive antibody-based method to measure UV-induced DNA damage in Zea mays. Plant Mol. Biol. Reporter 11, 230–236 ( 1993).

    Article  CAS  Google Scholar 

  30. Turunen, M. et al. The effects of UV-B exclusion on the soluble phenolics of young Scots pine seedlings in the Subarctic. Environ. Pollut. 106, 219–228 (1999).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank C. Langebartels, T. Boller, J. Lucht, G. Buchholz, H. Frohnmeyer, P. Crouzet, P. Pelczar, C. Körner and A. Kuttenberger for discussions and comments. We also thank S. Stich, V. Gloeckler and C. Ramos for assistance. The photolyase mutant line (uvr2-1) was obtained from the Arabidopsis Biological Resource Center, Ohio, USA. This work was supported by a fellowship from the Foundation of the Chemical Industry of Basel to G.R. and Novartis Research Foundation.

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Correspondence to Gerhard Ries.

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Ries, G., Heller, W., Puchta, H. et al. Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101 (2000). https://doi.org/10.1038/35017595

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