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.

Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis

Nature volume 400, pages 667–671 (1999)Cite this article

Abstract

The co-evolutionary ‘arms race’1 is a widely accepted model for the evolution of host–pathogen interactions. This model predicts that variation for disease resistance will be transient, and that host populations generally will be monomorphic at disease-resistance (R -gene) loci. However, plant populations show considerable polymorphism at R -gene loci involved in pathogen recognition2. Here we have tested the arms-race model in Arabidopsis thaliana by analysing sequences flanking Rpm1, a gene conferring the ability to recognize Pseudomonas pathogens carrying AvrRpm1 orAvrB (ref. 3). We reject the arms-race hypothesis: resistance andsusceptibility alleles at this locus have co-existed for millions of years. To account for the age of alleles and the relative levels ofpolymorphism within allelic classes, we use coalescence theory to model the long-term accumulation of nucleotide polymorphism in the context of the short-term ecological dynamics of disease resistance. This analysis supports a ‘trench warfare’ hypothesis, inwhich advances and retreats of resistance-allele frequency maintain variation for disease resistance as a dynamic polymorphism4,5.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Figure 1: Genealogy of the Rpm1 junction region.
Figure 2: Sliding window analysis.
Figure 3: Model for an Athaliana–Pseudomonas interaction.
Figure 4: Resistance-allele frequency distributions.

References

  1. Dawkins, R. & Krebs, J. R. Arms race between and within species. Proc. R. Soc. Lond. B 205, 489–511 (1979).

    Article  ADS  CAS  Google Scholar 

  2. Kunkel, B. Auseful weed put to work: genetic analysis of disease resistance loci in Arabidopsis thaliana. Trends Genet. 12, 63–69 (1996).

    Article  CAS  Google Scholar 

  3. Grant, M. R.et al. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269, 843–846 (1995).

    Article  ADS  CAS  Google Scholar 

  4. Jayakar, S. D. Amathematical model for interaction of gene frequencies in a parasite and its host. Theor. Popul. Biol. 1, 140–164 (1970).

    Article  CAS  Google Scholar 

  5. Hamilton, W. D. in Population Biology of Infectious Diseases (eds Anderson, R. M. & May, R. M.) 269–296 (Springer, Berlin, 1982).

    Book  Google Scholar 

  6. Grant, M. R.et al. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc. Natl Acad. Sci. USA 95, 15843–15848 (1998).

    Article  ADS  CAS  Google Scholar 

  7. O'Kane, S. L. & Al-Shehbaz, I. Asynopsis of Arabidopsis (Brassicaceae). Novon 7, 323–327 (1997).

    Article  Google Scholar 

  8. Whalen, M. C., Innes, R. W., Bent, A. F. & Staskawicz, B. J. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3, 49–59 (1991).

    Article  CAS  Google Scholar 

  9. May, R. M. in Ecology and Genetics of Host-Parasite Interactions (eds Rollinson, D. & Anderson, R. M.) 243–262 (Academic, New York, 1985).

    Google Scholar 

  10. Maynard Smith, J. & Haigh, J. The hitchhiking effect of a favourable gene. Genet. Res. 23, 23–25 (1974).

    Article  Google Scholar 

  11. May, R. M. & Anderson, R. M. Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. Lond. B 219, 281–313 (1983).

    Article  ADS  CAS  Google Scholar 

  12. Hamilton, W. D., Axelrod, R. & Tanese, R. Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl Acad. Sci. USA 87, 3566–3573 (1990).

    Article  ADS  CAS  Google Scholar 

  13. Hudson, R. R. & Kaplan, N. L. The coalescent process in models with selection and recombination. Genetics 120, 831–840 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).

    Book  Google Scholar 

  15. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. McDonald, J. H. Improved tests for heterogenity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol. Biol. Evol. 15, 377–384 (1998).

    Article  CAS  Google Scholar 

  17. Innan, H., Tajima, F., Terauchi, R. & Miyashita, N. T. Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics 143, 1761–1770 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Kawabe, A., Innan, H., Terauchi, R. & Miyashita, N. T. Nucleotide polymorphism in the acidic chitinase locus (ChiA) region of the wild plant Arabidopsis thaliana. Mol. Biol. Evol. 14, 1303–1315 (1997).

    Article  CAS  Google Scholar 

  19. Purugganan, M. D. & Suddith, J. I. Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: nonneutral evolution and naturally occurring variation in floral homeotic function. Proc. Natl Acad. Sci. USA 95, 8130–8134 (1998).

    Article  ADS  CAS  Google Scholar 

  20. Purugganan, M. D. & Suddith, J. I. Molecular population genetics of floral homeotic loci: departures from the equilibrium-neutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana. Genetics 151, 839–848 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Wolfe, K. H., Sharp, P. M. & Li, W.-H. Rates of synonymous substitution in plant nuclear genes. J. Mol. Evol. 29, 208–211 (1989).

    Article  ADS  CAS  Google Scholar 

  22. Nei, M. & Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418–426 (1986).

    CAS  PubMed  Google Scholar 

  23. Redei, G. P. Arabidopsis as a genetic tool. Annu. Rev. Genet. 9, 111–127 (1986).

    Article  Google Scholar 

  24. Bergelson, J. & Purrington, C. Surveying patterns in the cost of resistance in plants. Am. Nat. 148, 536–558 (1996).

    Article  Google Scholar 

  25. Hirano, S. S. & Upper, C. D. Population biology and epidemiology of Pseudomonas syringae. Annu. Rev. Phytopath. 28, 155–177 (1990).

    Article  Google Scholar 

  26. Judson, O. Preserving genes: a model of the maintenance of genetic variation in a metapopulation under frequency-dependent selection. Genet. Res. Camb. 65, 175–191 (1995).

    Article  ADS  Google Scholar 

  27. Caicedo, A. L., Schaal, B. A. & Kunkel, B. N. Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 96, 302–306 (1999).

    Article  ADS  CAS  Google Scholar 

  28. Bergelson, J., Stahl, E., Dudek, S. & Kreitman, M. Genetic variation within and among populations of Arabidopsis thaliana. Genetics 148, 1311–1323 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Rozas, J. & Rozas, R. DnaSP version 2.0: A novel software package for extensive molecular population genetics analysis. Comput. Appl. Biosci. 13, 307–311 (1997).

    CAS  PubMed  Google Scholar 

  30. Hudson, R. R. in Oxford Surveys in Evolutionary Biology Vol. 7 (eds Futuyama, D. & Antonovics, J.) 1–44 (Oxford Univ. Press, Oxford, 1990).

    Google Scholar 

Download references

Acknowledgements

M. Grant and J. McDowell provided unpublished sequences, and R. Hudson provided computer code. The Nottingham and Ohio State University Arabidopsis stock centres provided seeds. We thank R. Hudson, H. Innan, A. Kawabe, C. Langley, Y. Satta and N. Takahata for helpful discussions, and J. Dangl, P. Kareiva, S. Levin and J. McDowell for commenting on earlier versions of the manuscript. G.D. was supported by a Dropkin fellowship and R.M. was supported by an NSF/Sloan Fellowship in Molecular Evolution. This work was supported by an NSF Presidential Award and Packard Fellowship to J.B., an NIH grant to M.K., an NIH grant to J.B. and M.K. and a University of Chicago Hinds Fund grant to E.A.S.

Author information

Authors and Affiliations

  1. Committee on Genetics, Department of Ecology and Evolution, University of Chicago, Chicago, 60637, Illinois, USA

    Eli A. Stahl, Martin Kreitman & Joy Bergelson

  2. Department of Ecology and Evolution, University of Chicago, Chicago, 60637, Illinois, USA

    Greg Dwyer, Rodney Mauricio, Martin Kreitman & Joy Bergelson

Authors
  1. Eli A. Stahl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Greg Dwyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodney Mauricio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin Kreitman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joy Bergelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joy Bergelson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stahl, E., Dwyer, G., Mauricio, R. et al. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, 667–671 (1999). https://doi.org/10.1038/23260

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/23260

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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