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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References
Puchta, H., Swoboda, P. & Hohn, B. Induction of homologous DNA recombination in whole plants. Plant J. 7, 203–210 (1995)
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)
Ries, G. et al. Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101 (2000)
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)
Walbot, V. Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol. Gen. Genet. 234, 353–360 (1992)
Walbot, V. UV-B damage amplified by transposons in maize. Nature 397, 398–399 (1999)
Kumar, A. & Bennetzen, J. L. Plant retrotransposons. Annu. Rev. Genet. 33, 479–532 (1999)
Dellaporta, S. et al. Endogenous transposable elements associated with virus infection in maize. Cold Spring Harbor Symp. Quant. Biol. 49, 321–328 (1984)
Johns, M. A., Mottinger, J. & Freeling, M. A low copy number, copia-like transposon in maize. EMBO J. 4, 1093–1102 (1985)
Brakke, M. Mutations, the aberrant ratio phenomenon, and virus infection of maize. Annu. Rev. Phytopathol. 22, 77–94 (1984)
Lucht, J. M. et al. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genet. 30, 311–314 (2002)
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)
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)
Burk, L. G. & Menser, H. A. A dominant aurea mutation in tobacco. Tob. Sci. 8, 101–104 (1964)
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)
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)
Dempsey, D. A., Shah, J. & Klessig, D. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18, 547–575 (1999)
Dong, X. Genetic dissection of systemic acquired resistance. Curr. Opin. Plant Biol. 4, 309–314 (2001)
Pearce, G., Strydom, D., Johnson, S. & Ryan, C. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895–897 (1991)
Waterhouse, P., Wang, M.-B. & Finnegan, J. Role of short RNAs in gene silencing. Trends Plant Sci. 6, 297–301 (2001)
Karpinski, S. et al. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657 (1999)
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)
Gorbunova, V. et al. A new hyperrecombinogenic mutant of Nicotiana tabacum. Plant J. 24, 601–611 (2000)
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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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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DOI: https://doi.org/10.1038/nature01683
