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Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana

Nature volume 423, pages 74–77 (2003)Cite this article

Abstract

Resistance genes (R-genes) act as an immune system in plants by recognizing pathogens and inducing defensive pathways. Many R-gene loci are present in plant genomes, presumably reflecting the need to maintain a large repertoire of resistance alleles. These loci also often segregate for resistance and susceptibility alleles that natural selection has maintained as polymorphisms within a species for millions of years1,2,3,4,5. Given the obvious advantage to an individual of being disease resistant, what prevents these resistance alleles from being driven to fixation by natural selection? A cost of resistance6 is one potential explanation; most models require a lower fitness of resistant individuals in the absence of pathogens for long-term persistence of susceptibility alleles7. Here we test for the presence of a cost of resistance at the RPM1 locus of Arabidopsis thaliana. Results of a field experiment comparing the fitness of isogenic strains that differ in the presence or absence of RPM1 and its natural promoter reveal a large cost of RPM1, providing the first evidence that costs contribute to the maintenance of an ancient R-gene polymorphism.

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Figure 1: RPM1 expression.
Figure 2: Total seed numbers.

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References

  1. Grant, M. R. et al. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc. Natl Acad. Sci. USA 87, 15843–15848 (1998)

    Article  ADS  Google Scholar 

  2. 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 

  3. Stahl, E. A., Dwyer, G., Mauricio, R., Kreitman, M. & Bergelson, J. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, 667–671 (1999)

    Article  ADS  CAS  Google Scholar 

  4. Tian, D., Araki, H., Stahl, E., Bergelson, J. & Kreitman, M. Signature of balancing selection in Arabidopsis. Proc. Natl Acad. Sci. USA 99, 11525–11530 (2002)

    Article  ADS  CAS  Google Scholar 

  5. Mauricio, R., Korves, T., Stahl, E. A., Kreitman, M. & Bergelson, J. Natural selection for polymorphism in the disease resistance gene RPS2 of Arabidopsis. Genetics 163, 735–746 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Simms, E. L. & Rausher, M. D. Costs and benefits of plant resistance to herbivory. Am. Nat. 130, 570–581 (1987)

    Article  Google Scholar 

  7. Bergelson, J., Dwyer, G. & Emerson, J. J. Models and data on plant–enemy coevolution. Annu. Rev. Genet. 35, 469–499 (2001)

    Article  CAS  Google Scholar 

  8. Boyes, D. C., Nam, J. & Dangl, J. L. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl Acad. Sci. USA 95, 15849–15854 (1998)

    Article  ADS  CAS  Google Scholar 

  9. Bisgrove, S. R., Simonich, M. T., Smith, N. M., Sattler, A. & Innes, R. W. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6, 927–933 (1994)

    Article  CAS  Google Scholar 

  10. 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 

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

    Article  Google Scholar 

  12. Ow, D. W. & Medberry, S. L. Genome manipulation through site-specific recombination. Crit. Rev. Plant Sci. 14, 239–261 (1995)

    Article  CAS  Google Scholar 

  13. Howe, C. Gene Cloning and Manipulation (Cambridge Univ. Press, Cambridge, 1995)

    Google Scholar 

  14. 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 

  15. Mackey, D., Holt, B. F., Wiig, A. & Dangl, J. L. RIN4 interacts with Pseudomonas syringae Type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754 (2002)

    Article  CAS  Google Scholar 

  16. Jorgensen, J. H. & Jensen, H. P. Effect of ‘unnecessary’ powdery mildew resistance genes on agronomic properties of spring barley. Norsk Landbruksforsking. Suppl. 9, 125–130 (1990)

    Google Scholar 

  17. Brown, J. K. M. Yield penalties of disease resistance in crops. Curr. Opin. Plant Biol. 5, 1–6 (2002)

    Article  Google Scholar 

  18. Rausher, M. D. Co-evolution and plant resistance to natural enemies. Nature 411, 857–864 (2001)

    Article  ADS  CAS  Google Scholar 

  19. Stuiver, M. H. & Custers, J. H. H. V. Engineering disease resistance in plants. Nature 411, 865–868 (2001)

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  21. Wang, Z.-W., Yamanouchi, U., Katayose, Y., Sasaki, T. & Yano, M. Expression of the Pib rice-blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Mol. Biol. 47, 653–661 (2001)

    Article  CAS  Google Scholar 

  22. Oldroyd, G. E. D. & Staskawicz, B. J. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA 95, 10300–10305 (1998)

    Article  ADS  CAS  Google Scholar 

  23. Tang, X. et al. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11, 15–29 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Mindrinos, M., Katagiri, F., Yu, G. & Ausubel, F. M. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78, 1089–1099 (1994)

    Article  CAS  Google Scholar 

  25. Tao, Y., Yuan, F., Leister, R. T., Ausubel, F. M. & Katagiri, F. Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell 12, 2541–2554 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Holt, B. J. et al. An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev. Cell 2, 807–817 (2002)

    Article  Google Scholar 

  27. van der Biezen, E. A. & Jones, J. D. G. Plant disease resistance proteins and the gene for gene concept. Trends Biochem. Sci. 23, 454–456 (1998)

    Article  CAS  Google Scholar 

  28. Dangl, J. L. & Jones, J. D. G. Plant pathogens and integrated defence responses to infection. Nature 411, 826–832 (2001)

    Article  ADS  CAS  Google Scholar 

  29. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R. & Dangl, J. L. Arabidopsis RIN4 is a target of the Type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389 (2003)

    Article  CAS  Google Scholar 

  30. Gillespie, J. H. Natural selection for resistance to epidemics. Ecology 56, 493–495 (1975)

    Article  Google Scholar 

  31. Jakob, K. et al. Pseudomonas viridiflava and P. syringae—natural pathogens of Arabidopsis thaliana. Mol. Plant–Microbe Interact. 15, 1195–1203 (2002)

    Article  CAS  Google Scholar 

  32. Heid, C. A., Stevens, J., Livak, K. J. & Williams, P. M. Real time quantitative PCR. Genome Res. 6, 986–994 (1996)

    Article  CAS  Google Scholar 

  33. Klement, Z. Rapid detection of the pathogenicity of phytopathogenic Pseudomonads. Nature 199, 299–300 (1963)

    Article  ADS  CAS  Google Scholar 

  34. Moore, E. R. B. et al. The determination and comparison of the 16S rRNA gene sequences of species of the genus Pseudomonas (sensu stricto) and estimation of the natural intrageneric relationships. Syst. Appl. Microbiol. 19, 478–492 (1996)

    Article  CAS  Google Scholar 

  35. Dewdney, J. et al. Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 24, 205–218 (2000)

    Article  CAS  Google Scholar 

  36. Traw, M. B., Kim, J., Enright, S., Cipollini, D. F. & Bergelson, J. Negative cross-talk between the salicylate and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Mol. Ecol. 12, 1125–1135 (2003)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Dangl for feedback, and members of the Department of Ecology and Evolution for assistance in the field. This research was supported by NIH grants to J.B.

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Authors and Affiliations

  1. Department of Ecology and Evolution, University of Chicago, 1101 E. 57th Street, Illinois, 60637, Chicago, USA

    D. Tian, M. B. Traw, M. Kreitman & J. Bergelson

  2. Department of Biology, Nanjing University, 22 Han Kou Road, 210093, Nanjing, People's Republic of China

    J. Q. Chen

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  1. D. Tian
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Correspondence to J. Bergelson.

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Tian, D., Traw, M., Chen, J. et al. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74–77 (2003). https://doi.org/10.1038/nature01588

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