Skip to main content
Log in

Unique pattern of R-gene variation within populations in Arabidopsis

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

An understanding of the variation pattern in disease resistance (R) genes is essential for its use in breeding programs aimed at neutralizing the threat of pathogens. Although the variation between populations is well known, there is little research about R-gene variation patterns within populations. Here, we investigate the polymorphism at three R-gene loci of 39 individual plants from nine populations of Arabidopsis thaliana. Our data suggest that alleles of each locus from individuals within a local population were either nearly identical, or highly diverse as ones between populations. The vast majority (92.5%) of within-population variation was shared globally, with high levels of allelic diversity (up to 11.7%) and abundant diverse-alleles. This unique pattern of within-population variation at R-loci suggests that individual plants within a population had the great potential to maintain a high level of globally-shared polymorphisms, and that the diversifying selection was the major force maintaining such polymorphisms. Consequently, the shared-polymorphism became recyclable for new R-genes, as the corresponding avirulence re-emerges in pathogen populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, Beynon JL (2004) Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306:1957–1960

    Article  PubMed  CAS  Google Scholar 

  • Bakker EG, Stahl EA, Toomajian C, Nordborg M, Kreitman M, Bergelson J (2006) Distribution of genetic variation within and among local populations of Arabidopsis thaliana over its species range. Mol Ecol 15:1405–1418

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285

    Article  PubMed  CAS  Google Scholar 

  • Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF (2000) Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663–676

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  PubMed  CAS  Google Scholar 

  • Datta A, Hendrix M, Lipsitch M, Jinks-Robertson S (1997) Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc Natl Acad Sci USA 94:9757–9762

    Article  PubMed  CAS  Google Scholar 

  • de Wit PJ, Brandwagt BF, van den Burg HA, Cai X, van der Hoorn RA, de Jong CF, van Klooster J, de Kock MJ, Kruijt M, Lindhout WH, Luderer R, Takken FL, Westerink N, Vervoort JJ, Joosten MH (2002) The molecular basis of co-evolution between Cladosporium fulvum and tomato. Antonie Van Leewenhoek 81:409–412

    Article  Google Scholar 

  • Ding J, Cheng H, Jin X, Araki H, Yang Y, Tian D (2006) Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis. Genetica (in press). doi:101007/s10709–006–0002–9

  • Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11:495–506

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112

    Article  PubMed  CAS  Google Scholar 

  • Holub EB (2001) Arms race is an ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR (1987) Estimating the recombination parameter of a finite population model without selection. Genet Res 50:245–250

    Article  PubMed  CAS  Google Scholar 

  • Jia Y, Bryan GT, Farrall L, Valent B (2003) Natural variation at the Pi-ta rice blast resistance locus. Phytopathology 93:1452–1459

    Article  CAS  PubMed  Google Scholar 

  • Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular evolutionary genetics Analysis and sequence alignment. Briefings in Bioinformatics 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  PubMed  CAS  Google Scholar 

  • Mauricio R, Stahl EA, Korves T, Tian D, Kreitman M, Bergelson J (2003) Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163:735–746

    PubMed  CAS  Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379

    Article  PubMed  CAS  Google Scholar 

  • McDowell JM, Woffenden BJ (2003) Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol 21:178–183

    Article  PubMed  CAS  Google Scholar 

  • McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, Holub EB, Dangl JL (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10:1861–1874

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  PubMed  CAS  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    PubMed  CAS  Google Scholar 

  • Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441:947–952

    Article  PubMed  CAS  Google Scholar 

  • Moffat AS (2001) Finding new ways to fight plant diseases. Science 292:2270–2273

    Article  PubMed  CAS  Google Scholar 

  • Noel L, Moores TL, van Der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant cell 11:2099–2112

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Donnelly P (1997) The coalescent process with selfing. Genetics 146:1185–1195

    PubMed  CAS  Google Scholar 

  • Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196

    Article  PubMed  CAS  Google Scholar 

  • Pan Q, Liu YS, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    PubMed  CAS  Google Scholar 

  • Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JD (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821–832

    Article  PubMed  CAS  Google Scholar 

  • Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, Beynon JL (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517–1527

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Shen J, Araki H, Chen L, Chen JQ, Tian D (2006) Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172:1243–1250

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP; Sukamto (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 32:655–667

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D (2006) Genome-wide investigation on the genetic variation of rice disease resistance genes. Plant Mol Biol 62:181–193

    Article  PubMed  CAS  Google Scholar 

  • Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 271:402–415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Joy Bergelson for providing DNA of A. thaliana accessions and A. lyrata. This study was supported by NSFC (30570987 and 30470122) and Pre-program for NBRPC (2005CCA02100) to D. T. or J. Q. C.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jian-Qun Chen or Dacheng Tian.

Additional information

Communicated by S. Hohmann.

Nucleotide sequence data reported are available in the GenBank databases under the accession numbers EF368054-EF368158.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ding, J., Zhang, W., Jing, Z. et al. Unique pattern of R-gene variation within populations in Arabidopsis. Mol Genet Genomics 277, 619–629 (2007). https://doi.org/10.1007/s00438-007-0213-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-007-0213-5

Keywords

Navigation