Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2004 Mar;166(3):1517–1527. doi: 10.1534/genetics.166.3.1517

The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana.

Laura E Rose 1, Peter D Bittner-Eddy 1, Charles H Langley 1, Eric B Holub 1, Richard W Michelmore 1, Jim L Beynon 1
PMCID: PMC1470773  PMID: 15082565

Abstract

We have used the naturally occurring plant-parasite system of Arabidopsis thaliana and its common parasite Peronospora parasitica (downy mildew) to study the evolution of resistance specificity in the host population. DNA sequence of the resistance gene, RPP13, from 24 accessions, including 20 from the United Kingdom, revealed amino acid sequence diversity higher than that of any protein coding gene reported so far in A. thaliana. A significant excess of amino acid polymorphism segregating within this species is localized within the leucine-rich repeat (LRR) domain of RPP13. These results indicate that single alleles of the gene have not swept through the population, but instead, a diverse collection of alleles have been maintained. Transgenic complementation experiments demonstrate functional differences among alleles in their resistance to various pathogen isolates, suggesting that the extreme amino acid polymorphism in RPP13 is maintained through continual reciprocal selection between host and pathogen.

Full Text

The Full Text of this article is available as a PDF (316.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguadé M., Miyashita N., Langley C. H. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics. 1992 Nov;132(3):755–770. doi: 10.1093/genetics/132.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akashi H. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics. 1999 Jan;151(1):221–238. doi: 10.1093/genetics/151.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  4. Banerjee D., Zhang X., Bent A. F. The leucine-rich repeat domain can determine effective interaction between RPS2 and other host factors in arabidopsis RPS2-mediated disease resistance. Genetics. 2001 May;158(1):439–450. doi: 10.1093/genetics/158.1.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barrier Marianne, Bustamante Carlos D., Yu Jiaye, Purugganan Michael D. Selection on rapidly evolving proteins in the Arabidopsis genome. Genetics. 2003 Feb;163(2):723–733. doi: 10.1093/genetics/163.2.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bergelson J., Kreitman M., Stahl E. A., Tian D. Evolutionary dynamics of plant R-genes. Science. 2001 Jun 22;292(5525):2281–2285. doi: 10.1126/science.1061337. [DOI] [PubMed] [Google Scholar]
  7. Bittner-Eddy P. D., Beynon J. L. The Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid. Mol Plant Microbe Interact. 2001 Mar;14(3):416–421. doi: 10.1094/MPMI.2001.14.3.416. [DOI] [PubMed] [Google Scholar]
  8. Bittner-Eddy P. D., Crute I. R., Holub E. B., Beynon J. L. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 2000 Jan;21(2):177–188. doi: 10.1046/j.1365-313x.2000.00664.x. [DOI] [PubMed] [Google Scholar]
  9. Bittner-Eddy P., Can C., Gunn N., Pinel M., Tör M., Crute I., Holub E. B., Beynon J. Genetic and physical mapping of the RPP13 locus, in Arabidopsis, responsible for specific recognition of several Peronospora parasitica (downy mildew) isolates. Mol Plant Microbe Interact. 1999 Sep;12(9):792–802. doi: 10.1094/MPMI.1999.12.9.792. [DOI] [PubMed] [Google Scholar]
  10. Bryan G. T., Wu K. S., Farrall L., Jia Y., Hershey H. P., McAdams S. A., Faulk K. N., Donaldson G. K., Tarchini R., Valent B. tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell. 2000 Nov;12(11):2033–2046. doi: 10.1105/tpc.12.11.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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 U S A. 1999 Jan 5;96(1):302–306. doi: 10.1073/pnas.96.1.302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dodds P. N., Lawrence G. J., Ellis J. G. Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell. 2001 Jan;13(1):163–178. doi: 10.1105/tpc.13.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ellis J. G., Lawrence G. J., Luck J. E., Dodds P. N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell. 1999 Mar;11(3):495–506. doi: 10.1105/tpc.11.3.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grant M. R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R. W., Dangl J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. doi: 10.1126/science.7638602. [DOI] [PubMed] [Google Scholar]
  15. Grant M. R., McDowell J. M., Sharpe A. G., de Torres Zabala M., Lydiate D. J., Dangl J. L. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15843–15848. doi: 10.1073/pnas.95.26.15843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hanfstingl U., Berry A., Kellogg E. A., Costa J. T., 3rd, Rüdiger W., Ausubel F. M. Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection? Genetics. 1994 Nov;138(3):811–828. doi: 10.1093/genetics/138.3.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hauser M. T., Harr B., Schlötterer C. Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol Biol Evol. 2001 Sep;18(9):1754–1763. doi: 10.1093/oxfordjournals.molbev.a003963. [DOI] [PubMed] [Google Scholar]
  18. Henikoff S., Comai L. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics. 1998 May;149(1):307–318. doi: 10.1093/genetics/149.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hudson R. R., Kaplan N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. doi: 10.1093/genetics/111.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hulbert S. H., Webb C. A., Smith S. M., Sun Q. Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol. 2001;39:285–312. doi: 10.1146/annurev.phyto.39.1.285. [DOI] [PubMed] [Google Scholar]
  21. Hwang C. F., Bhakta A. V., Truesdell G. M., Pudlo W. M., Williamson V. M. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell. 2000 Aug;12(8):1319–1329. doi: 10.1105/tpc.12.8.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Innan H., Tajima F., Terauchi R., Miyashita N. T. Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics. 1996 Aug;143(4):1761–1770. doi: 10.1093/genetics/143.4.1761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jia Y., McAdams S. A., Bryan G. T., Hershey H. P., Valent B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 2000 Aug 1;19(15):4004–4014. doi: 10.1093/emboj/19.15.4004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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. 1997 Dec;14(12):1303–1315. doi: 10.1093/oxfordjournals.molbev.a025740. [DOI] [PubMed] [Google Scholar]
  25. Kawabe A., Miyashita N. T. DNA variation in the basic chitinase locus (ChiB) region of the wild plant Arabidopsis thaliana. Genetics. 1999 Nov;153(3):1445–1453. doi: 10.1093/genetics/153.3.1445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kawabe A., Yamane K., Miyashita N. T. DNA polymorphism at the cytosolic phosphoglucose isomerase (PgiC) locus of the wild plant Arabidopsis thaliana. Genetics. 2000 Nov;156(3):1339–1347. doi: 10.1093/genetics/156.3.1339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kliebenstein D. J., Lambrix V. M., Reichelt M., Gershenzon J., Mitchell-Olds T. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell. 2001 Mar;13(3):681–693. doi: 10.1105/tpc.13.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Koch E., Slusarenko A. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell. 1990 May;2(5):437–445. doi: 10.1105/tpc.2.5.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kuittinen H., Aguadé M. Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana. Genetics. 2000 Jun;155(2):863–872. doi: 10.1093/genetics/155.2.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Luck J. E., Lawrence G. J., Dodds P. N., Shepherd K. W., Ellis J. G. Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell. 2000 Aug;12(8):1367–1377. doi: 10.1105/tpc.12.8.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mauricio Rodney, Stahl Eli A., Korves Tonia, Tian Dacheng, Kreitman Martin, Bergelson Joy. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics. 2003 Feb;163(2):735–746. doi: 10.1093/genetics/163.2.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  33. Michelmore R. W., Meyers B. C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998 Nov;8(11):1113–1130. doi: 10.1101/gr.8.11.1113. [DOI] [PubMed] [Google Scholar]
  34. Mondragón-Palomino Mariana, Meyers Blake C., Michelmore Richard W., Gaut Brandon S. Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res. 2002 Sep;12(9):1305–1315. doi: 10.1101/gr.159402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  36. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  37. Staskawicz B. J., Ausubel F. M., Baker B. J., Ellis J. G., Jones J. D. Molecular genetics of plant disease resistance. Science. 1995 May 5;268(5211):661–667. doi: 10.1126/science.7732374. [DOI] [PubMed] [Google Scholar]
  38. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tian Dacheng, Araki Hitoshi, Stahl Eli, Bergelson Joy, Kreitman Martin. Signature of balancing selection in Arabidopsis. Proc Natl Acad Sci U S A. 2002 Aug 9;99(17):11525–11530. doi: 10.1073/pnas.172203599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Van der Hoorn R. A., Roth R., De Wit P. J. Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein Avr4. Plant Cell. 2001 Feb;13(2):273–285. doi: 10.1105/tpc.13.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang G. L., Ruan D. L., Song W. Y., Sideris S., Chen L., Pi L. Y., Zhang S., Zhang Z., Fauquet C., Gaut B. S. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell. 1998 May;10(5):765–779. doi: 10.1105/tpc.10.5.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wulff B. B., Thomas C. M., Smoker M., Grant M., Jones J. D. Domain swapping and gene shuffling identify sequences required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins. Plant Cell. 2001 Feb;13(2):255–272. doi: 10.1105/tpc.13.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. van der Biezen E. A., Jones J. D. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol. 1998 Mar 26;8(7):R226–R227. doi: 10.1016/s0960-9822(98)70145-9. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES