Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Pathogen stress increases somatic recombination frequency in Arabidopsis

Nature Genetics volume 30, pages 311–314 (2002)Cite this article

Abstract

Evolution is based on genetic variability and subsequent phenotypic selection. Mechanisms that modulate the rate of mutation according to environmental cues, and thus control the balance between genetic stability and flexibility, might provide a distinct evolutionary advantage1,2,3,4. Stress-induced mutations stimulated by unfavorable environments, and possible mechanisms for their induction, have been described for several organisms2,3,4, but research in this area has mainly focused on microorganisms. We have analyzed the influence of adverse environmental conditions on the genetic stability of the higher plant Arabidopsis thaliana. Here we show that a biotic stress factor—attack by the oomycete pathogen Peronospora parasitica—can stimulate somatic recombination in Arabidopsis. The same effect was observed when plant pathogen-defense mechanisms were activated by the chemicals 2,6-dichloroisonicotinic acid (INA) or benzothiadiazole (BTH), or by a mutation (cim3). Together with previous studies of recombination induced by abiotic factors, these findings suggest that increased somatic recombination is a general stress response in plants. The increased genetic flexibility might facilitate evolutionary adaptation of plant populations to stressful environments.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Detection of somatic recombination events in Arabidopsis thaliana.
Figure 2: Induction of somatic recombination in Arabidopsis by P. parasitica infection.
Figure 3: Induction of plant pathogen-defense response and somatic recombination by salicylic-acid analogs.
Figure 4: Induction of plant pathogen-defense response and somatic recombination by the cim3 mutation.

Similar content being viewed by others

References

  1. McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984).

    Article  CAS  Google Scholar 

  2. Radman, M., Matic, I. & Taddei, F. Evolution of evolvability. Ann. NY Acad. Sci. 870, 146–155 (1999).

    Article  CAS  Google Scholar 

  3. Caporale, L.H. Mutation is modulated: implications for evolution. Bioessays 22, 388–395 (2000).

    Article  CAS  Google Scholar 

  4. Rosenberg, S.M. Evolving responsively: adaptive mutation. Nature Rev. Genet. 2, 504–515 (2001).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  6. Walbot, V. Sources and consequences of phenotypic and genotypic plasticity in flowering plants. Trends Plant Sci. 1, 27–32 (1996).

    Article  Google Scholar 

  7. Lebel, E.G., Masson, J., Bogucki, A. & Paszkowski, J. Stress-induced intrachromosomal recombination in plant somatic cells. Proc. Natl Acad. Sci. USA 90, 422–426 (1993).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Kovalchuk, I., Kovalchuk, O., Arkhipov, A. & Hohn, B. Transgenic plants are sensitive bioindicators of nuclear pollution caused by the Chernobyl accident. Nature Biotechnol. 16, 1054–1059 (1998).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. 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 

  13. Mauch-Mani, B. & Slusarenko, A.J. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8, 203–212 (1996).

    Article  CAS  Google Scholar 

  14. Heath, M.C. Hypersensitive response-related death. Plant Mol. Biol. 44, 321–333 (2000).

    Article  CAS  Google Scholar 

  15. Uknes, S. et al. Acquired resistance in Arabidopsis. Plant Cell 4, 645–656 (1992).

    Article  CAS  Google Scholar 

  16. Ryals, J.A. et al. Systemic acquired resistance. Plant Cell 8, 1809–1819 (1996).

    Article  CAS  Google Scholar 

  17. McDowell, J.M. & Dangl, J.L. Signal transduction in the plant immune response. Trends Biochem. Sci. 25, 79–82 (2000).

    Article  CAS  Google Scholar 

  18. Yang, Y., Shah, J. & Klessig, D.F. Signal perception and transduction in plant defense responses. Genes Dev. 11, 1621–1639 (1997).

    Article  CAS  Google Scholar 

  19. Lawton, K.A. et al. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10, 71–82 (1996).

    Article  CAS  Google Scholar 

  20. Weymann, K. et al. Suppression and restoration of lesion formation in Arabidopsis lsd mutants. Plant Cell 7, 2013–2022 (1995).

    Article  CAS  Google Scholar 

  21. Alvarez, M.E. et al. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784 (1998).

    Article  CAS  Google Scholar 

  22. Mittler, R. & Lam, E. Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol. Biol. 34, 209–221 (1997).

    Article  CAS  Google Scholar 

  23. Gallego, M.E. et al. Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. Plant J. 25, 31–41 (2001).

    Article  CAS  Google Scholar 

  24. Saxe, D., Datta, A. & Jinks-Robertson, S. Stimulation of mitotic recombination events by high levels of RNA polymerase II transcription in yeast. Mol. Cell. Biol. 20, 5404–5414 (2000).

    Article  CAS  Google Scholar 

  25. Maleck, K. et al. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet. 26, 403–410 (2000).

    Article  CAS  Google Scholar 

  26. Young, N.D. The genetic architecture of resistance. Curr. Opin. Plant Biol. 3, 285–290 (2000).

    Article  CAS  Google Scholar 

  27. Ellis, J., Dodds, P. & Pryor, T. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3, 278–284 (2000).

    Article  CAS  Google Scholar 

  28. Parniske, M. et al. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91, 821–832 (1997).

    Article  CAS  Google Scholar 

  29. Richter, T.E. & Ronald, P.C. The evolution of disease resistance genes. Plant Mol. Biol. 42, 195–204 (2000).

    Article  CAS  Google Scholar 

  30. Tinland, B., Hohn, B. & Puchta, H. Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus. Proc. Natl Acad. Sci. USA 91, 8000–8004 (1994).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Ramos for technical assistance, I. Kovalchuk and J. Molinier for critical comments on the manuscript, and D. Brubacher for help with data analysis. BTH was a gift from H. Kessmann, and K. Lawton supplied PR-1 antiserum. This work was supported by the NOVARTIS Research Foundation, by a grant from the European Union/Swiss Federal Office for Education and Science (to B.H.), a grant from the Swiss National Science Foundation (to J.P.M.) and an EMBO long-term fellowship (to J.M.L.).

Author information

Author notes

  1. Jan M. Lucht

    Present address: Freiburg University, Plant Biotechnology, Sonnenstrasse 5, D-79104, Freiburg, Germany

  2. Brigitte Mauch-Mani

    Present address: Institut de Botanique, Université de Neuchâtel, Switzerland

Authors and Affiliations

  1. Friedrich Miescher Institute, PO Box 2543, Basel, CH-4002, Switzerland

    Jan M. Lucht & Barbara Hohn

  2. Department of Biology, University of Fribourg, Fribourg, CH-1700, Switzerland

    Brigitte Mauch-Mani & Jean-Pierre Metraux

  3. Syngenta, PO Box 12257, Research Triangle Park, 27709, North Carolina, USA

    Henry-York Steiner

  4. Paradigm Genetics, PO Box 14528, Research Triangle Park, 27709, North Carolina, USA

    John Ryals

Authors
  1. Jan M. Lucht
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brigitte Mauch-Mani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Henry-York Steiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean-Pierre Metraux
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John Ryals
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Barbara Hohn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jan M. Lucht.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lucht, J., Mauch-Mani, B., Steiner, HY. et al. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat Genet 30, 311–314 (2002). https://doi.org/10.1038/ng846

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng846

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing