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Pathogen-induced systemic plant signal triggers DNA rearrangements

Nature volume 423, pages 760–762 (2003)Cite this article

Abstract

Plant genome stability is known to be affected by various abiotic environmental conditions1,2,3,4,5,6,7, but little is known about the effect of pathogens. For example, exposure of maize plants to barley stripe mosaic virus seems to activate transposable elements8,9 and to cause mutations in the non-infected progeny of infected plants10. The induction by barley stripe mosaic virus of an inherited effect may mean that the virus has a non-cell-autonomous influence on genome stability. Infection with Peronospora parasitica results in an increase in the frequency of somatic recombination in Arabidopsis thaliana11; however, it is unclear whether effects on recombination require the presence of the pathogen or represent a systemic plant response. It is also not clear whether the changes in the frequency of somatic recombination can be inherited. Here we report a threefold increase in homologous recombination frequency in both infected and non-infected tissue of tobacco plants infected with either tobacco mosaic virus12 or oilseed rape mosaic virus13. These results indicate the existence of a systemic recombination signal that also results in an increased frequency of meiotic and/or inherited late somatic recombination.

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Figure 1: The presence of TMV is not required for the increase in recombination frequency.
Figure 2: Grafting experiments.

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References

  1. Puchta, H., Swoboda, P. & Hohn, B. Induction of homologous DNA recombination in whole plants. Plant J. 7, 203–210 (1995)

    Article  CAS  Google Scholar 

  2. Kovalchuk, I., Kovalchuk, O., Arkhipov, A. & Hohn, B. Transgenic plants are sensitive bioindicators of nuclear pollution caused by the Chernobyl accident. Nature Biotechnol. 16, 1054–1057 (1998)

    Article  CAS  Google Scholar 

  3. Ries, G. et al. Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101 (2000)

    Article  ADS  CAS  Google Scholar 

  4. Ries, G., Buchholz, G., Frohnmeyer, H. & Hohn, B. UV-damage-mediated induction of homologous recombination in Arabidopsis is dependent on photosynthetically active radiation. Proc. Natl Acad. Sci. USA 97, 13425–13429 (2000)

    Article  ADS  CAS  Google Scholar 

  5. Walbot, V. Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol. Gen. Genet. 234, 353–360 (1992)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  7. Kumar, A. & Bennetzen, J. L. Plant retrotransposons. Annu. Rev. Genet. 33, 479–532 (1999)

    Article  CAS  Google Scholar 

  8. Dellaporta, S. et al. Endogenous transposable elements associated with virus infection in maize. Cold Spring Harbor Symp. Quant. Biol. 49, 321–328 (1984)

    Article  CAS  Google Scholar 

  9. Johns, M. A., Mottinger, J. & Freeling, M. A low copy number, copia-like transposon in maize. EMBO J. 4, 1093–1102 (1985)

    Article  CAS  Google Scholar 

  10. Brakke, M. Mutations, the aberrant ratio phenomenon, and virus infection of maize. Annu. Rev. Phytopathol. 22, 77–94 (1984)

    Article  Google Scholar 

  11. Lucht, J. M. et al. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genet. 30, 311–314 (2002)

    Article  Google Scholar 

  12. Harrison, B. D. & Wilson, T. M. A. Milestones in the research on tobacco mosaic virus. Phil. Trans. R. Soc. Lond. B 354, 521–529 (1999)

    Article  CAS  Google Scholar 

  13. Aguilar, I., Sanchez, F., Martin, A., Martinez-Herrera, D. & Ponz, F. Nucleotide sequence of Chinese rape mosaic virus (oilseed rape mosaic virus), a crucifer tobamovirus infecting Arabidopsis thaliana. Plant Mol. Biol. 30, 191–197 (1996)

    Article  CAS  Google Scholar 

  14. Burk, L. G. & Menser, H. A. A dominant aurea mutation in tobacco. Tob. Sci. 8, 101–104 (1964)

    Google Scholar 

  15. Shalev, G., Sitrit, Y., Avivi-Ragolski, N., Lichtenstein, C. & Levy, A. A. Stimulation of homologous recombination in plants by expression of the bacterial resolvase RuvC. Proc. Natl Acad. Sci. USA 96, 7398–7402 (1999)

    Article  ADS  CAS  Google Scholar 

  16. Boyko, V., Ferralli, J., Ashby, J., Schellenbaum, P. & Heinlein, M. Function of microtubules in intercellular transport of plant virus RNA. Nature Cell Biol. 2, 826–832 (2000)

    Article  CAS  Google Scholar 

  17. Dempsey, D. A., Shah, J. & Klessig, D. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18, 547–575 (1999)

    Article  CAS  Google Scholar 

  18. Dong, X. Genetic dissection of systemic acquired resistance. Curr. Opin. Plant Biol. 4, 309–314 (2001)

    Article  CAS  Google Scholar 

  19. Pearce, G., Strydom, D., Johnson, S. & Ryan, C. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895–897 (1991)

    Article  ADS  CAS  Google Scholar 

  20. Waterhouse, P., Wang, M.-B. & Finnegan, J. Role of short RNAs in gene silencing. Trends Plant Sci. 6, 297–301 (2001)

    Article  CAS  Google Scholar 

  21. Karpinski, S. et al. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657 (1999)

    Article  ADS  CAS  Google Scholar 

  22. Whitham, S. et al. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78, 1101–1115 (1994)

    Article  CAS  Google Scholar 

  23. Gorbunova, V. et al. A new hyperrecombinogenic mutant of Nicotiana tabacum. Plant J. 24, 601–611 (2000)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank S. van Eeden for technical assistance and H. Rothnie, K. Smith and E. Schultz for comments on the manuscript. The Novartis Research Foundation and Alberta Ingenuity Grant are acknowledged for financial support.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, T1K 3M4, Canada

    Igor Kovalchuk, Olga Kovalchuk & Jody Filkowski

  2. Friedrich Miescher-Institut for Biomedical Research, PO Box 2543, CH-4002, Basel, Switzerland

    Véronique Kalck, Vitaly Boyko, Manfred Heinlein & Barbara Hohn

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  1. Igor Kovalchuk
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  2. Olga Kovalchuk
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Correspondence to Igor Kovalchuk.

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Kovalchuk, I., Kovalchuk, O., Kalck, V. et al. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423, 760–762 (2003). https://doi.org/10.1038/nature01683

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