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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.

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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.

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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M. Grant and J. McDowell provided unpublished sequences, and R. Hudson provided computer code.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.

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  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

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  1. Eli A. Stahl
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Correspondence to Joy Bergelson.

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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

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