Journal of Genetics

, Volume 86, Issue 1, pp 27–35 | Cite as

Unique nucleotide polymorphism of ankyrin gene cluster in Arabidopsis

Research Article

Abstract

The ankyrin (ANK) gene cluster is a part of a multigene family encoding ANK transmembrane proteins in Arabidopsis thaliana, and plays an important role in protein-protein interactions and in signal pathways. In contrast to other regions of a genome, the ANK gene cluster exhibits an extremely high level of DNA polymorphism in an ∼5-kb region, without apparent decay. Phylogenetic analysis detects two clear, deeply differentiated haplotypes (dimorphism). The divergence between haplotypes of accession Col-0 and Ler-0 (Hap-C and Hap-L) is estimated to be 10.7%, approximately equal to the 10.5% average divergence between A. thaliana and A. lyrata. Sequence comparisons for the ANK gene cluster homologues in Col-0 indicate that the members evolve independently, and that the similarity among paralogues is lower than between alleles. Very little intralocus recombination or gene conversion is detected in ANK regions. All these characteristics of the ANK gene cluster are consistent with a tandem gene duplication and birth-and-death process. The possible mechanisms for and implications of this elevated nucleotide variation are also discussed, including the suggestion of balancing selection.

Keywords

ankyrin gene cluster divergence evolution gene duplication Arabidopsis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aguadé M. 2001 Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAH1 and F3H genes, in Arabidopsis thaliana. Mol. Biol. Evol. 18, 1–9.Google Scholar
  2. Becerra C., Jahrmann T., Puigdomènech P. and Vicient C. M. 2004 Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrintransmembrane proteins. Gene 340, 111–121.CrossRefPubMedGoogle Scholar
  3. Bergelson J., Stahl E., Dudek S. and Kreitman M. 1998 Genetic variation within and among populations of Arabidopsis thaliana. Genetics 148, 1311–1323.PubMedGoogle Scholar
  4. Britten R. J., Rowen L., Williams J. and Cameron R. A. 2003 Majority of divergence between closely related DNA samples is due to indels. Proc. Natl. Acad. Sci. USA 100, 4661–4665.CrossRefPubMedGoogle Scholar
  5. Clauss M. J. and Mitchell-Olds T. 2004 Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes. Genetics 166, 1419–1436.CrossRefPubMedGoogle Scholar
  6. Cork J. M. and Purugganan M. D. 2005 High-diversity genes in the Arabidopsis genome. Genetics 170, 1897–1911.CrossRefPubMedGoogle Scholar
  7. Gu X. and Nei M. 1999 Locus specificity of polymorphic alleles and evolution by a birth-and-death process in mammalian MHC genes. Mol. Biol. Evol. 16, 147–156.PubMedGoogle Scholar
  8. Hanfstingl U., Berry A., Kellogg E. A., Costa J. T. III, Rudiger W. and Ausubel F. M. 1994 Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection. Genetics 138, 811–828.PubMedGoogle Scholar
  9. Haubold B., Kroymann J., Ratzka A., Mitchell-Olds T. and Wiehe T. 2002 Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana. Genetics 161, 1269–1278.PubMedGoogle Scholar
  10. Hauser M. T., Harr B. and Schlotterer C. 2001 Trichome distribution in Abidopsis thaliana and its close relative A. lyrata: molecular analysis of the candidate gene GLABROUS1. Mol. Biol. Evol. 18, 1754–1763.PubMedGoogle Scholar
  11. Hurst L. D., Pál C. and Lercher M. J. 2004 The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 5, 299–310.CrossRefPubMedGoogle Scholar
  12. Innan H., Tajima F., Terauchi R. and Miyashita N. T. 1996 Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics 143, 1761–1770.PubMedGoogle Scholar
  13. Jander G., Norris S. R., Rounsley S. D., Bush D. F., Levin I. M. and Last R. L. 2002 Arabidopsis map-based cloning in the postgenome era. Plant Physiol. 129, 440–450.CrossRefPubMedGoogle Scholar
  14. Kawabe A. and Miyashita N. T. 1999 DNA variation in the basic chitinase locus (ChiB) region of the wild plant Arabidopsis thaliana. Genetics 153, 1445–1453.PubMedGoogle Scholar
  15. Kawabe A., Innan H., Terauchi R. and Miyashita N. T. 1997 Nucleotide polymorphism in the acidic chitinase locus (ChiA) region of the wild plant Arabidopsis thaliana. Mol. Biol. Evol. 14, 1303–1315.PubMedGoogle Scholar
  16. Koop B. F., Rowen L., Wang K., Kuo C. L., Seto D., Lenstra J. A. et al. 1994 The human T-cell receptor TCRAC/TCRDC (C alpha/C delta) region: organization, sequence, and evolution of 97.6 kb of DNA. Genomics 19, 478–493.CrossRefPubMedGoogle Scholar
  17. Krumlauf R. 1992 Evolution of the vertebrate Hox homeobox genes. BioEssays 14, 245–252.CrossRefPubMedGoogle Scholar
  18. Kuittinen H. and Aguadé M. 2000 Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana. Genetics 155, 863–872.PubMedGoogle Scholar
  19. Lercher M. J., Urrutia A. O. and Hurst L. D. 2002 Clustering of housekeeping genes provides a unified model of gene order in the human genome Nat. Genet. 31, 180–183.CrossRefPubMedGoogle Scholar
  20. Li J., Ji C., Zheng H., Fei X., Zheng M., Dai J., et al. 2005 Molecular cloning and characterization of a novel human gene containing four ankyrin repeat domains. Cell Mol. Biol. Lett. 10, 185–193.PubMedGoogle Scholar
  21. Martin D. I., Fiering S. and Groudine M. 1996 Regulation of beta-globin gene expression: straightening out the locus. Curr. Opin. Genet. Dev. 6, 488–495.CrossRefPubMedGoogle Scholar
  22. Michelmore R. W. and Meyers B. C. 1998 Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113–1130.PubMedGoogle Scholar
  23. Nei M. 1987 Molecular evolutionary genetics. Columbia University Press, New York.Google Scholar
  24. Nei M. and Hughes A. 1992 Balanced polymorphism and evolution by the birth and death process in the MHC loci. In Proceedings of the Eleventh Histocompatibility Workshop and Conference (ed. K. Tsuji, M. Aizawa and T. Suzuki), pp. 27–38. Oxford University Press, Oxford.Google Scholar
  25. Nei M. and Rooney A. P. 2005 Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39, 121–152.CrossRefPubMedGoogle Scholar
  26. Nei M., Gu X. and Sitnikova T. 1997 Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc. Natl. Acad. Sci. USA 94, 7799–7806.CrossRefPubMedGoogle Scholar
  27. Nei M., Rogozin I. B. and Piontkivska H. 2000 Purifying selection and birth-and-death evolution in the ubiquitin gene family. Proc. Natl. Acad. Sci. USA 97, 10866–10871.CrossRefPubMedGoogle Scholar
  28. Noel L., Moores T. L., van der Biezen E. A., Parniske M., Daniels M. J., Parker J. E. et al. 1999 Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11, 2099–2111.CrossRefPubMedGoogle Scholar
  29. Nordborg M., Hu T. T., Ishino Y., Jhaveri J., Toomajian C., Zheng H. et al. 2005 The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, 1–11.CrossRefGoogle Scholar
  30. Ota T. and Nei M. 1994 Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol. Biol. Evol. 11, 469–482.PubMedGoogle Scholar
  31. Parniske M., Hammond-Kosack K. E., Golstein C., Thomas C. M., Jones D. A. et al. 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.CrossRefPubMedGoogle Scholar
  32. Piontkivska H., Rooney A. P. and Nei M. 2002 Purifying selection and birth-and-death evolution in the histone H4 gene family. Mol. Biol. Evol. 19, 689–697.PubMedGoogle Scholar
  33. Purugganan M. D. and Suddith J. I. 1999 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.PubMedGoogle Scholar
  34. Richter T. E. and Ronald P. C. 2000 The evolution of disease resistance genes. Plant Mol. Biol. 42, 195–204.CrossRefPubMedGoogle Scholar
  35. Richter T. E., Prior T. J., Bennetzen J. L. and Hulbert S. H. 1995 New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141, 373–381.PubMedGoogle Scholar
  36. Ronald P. C. 1998 Resistance gene evolution. Curr. Opin. Plant Biol. 1, 294–298.CrossRefPubMedGoogle Scholar
  37. Rozas J., Sanchez-DelBarrio J. C., Messeguer X. and Rozas R. 2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefPubMedGoogle Scholar
  38. Saitou N. and Nei M. 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.PubMedGoogle Scholar
  39. Sedgwick S. G. and Smerdon S. J. 1999 The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem. Sci. 24, 311–316.CrossRefPubMedGoogle Scholar
  40. Song W. Y., Pi L. Y., Wang G. L., Gardner J., Holsten T. and Ronald P. C. 1997 Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9, 1279–1287.CrossRefPubMedGoogle Scholar
  41. Stahl E. A., Dwyer G., Mauricio R., Kreitman M. and Bergelson J. 1999 Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, 667–671.CrossRefPubMedGoogle Scholar
  42. Swofford D. L. 2000 PAUP*: phylogenetic analysis using parsimony. Sinauer, Sunderland.Google Scholar
  43. Tajima F. 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.PubMedGoogle Scholar
  44. Teeter K., Naeemuddin M., Gasperini R., Zimmerman E., White K. P., Hoskins R. et al. 2000 Haplotype dimorphism in a SNP collection from Drosophila melanogaster. J. Exp. Zool. 288, 63–75.CrossRefPubMedGoogle Scholar
  45. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F. and Higgens D. G. 1997 The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.CrossRefPubMedGoogle Scholar
  46. Tian D., Araki H., Stahl E., Bergelson J. and Kreitman M. 2002 Signature of balancing selection in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 11525–11530.CrossRefPubMedGoogle Scholar
  47. Wang S., Magoulas C. and Hickey D. 1999 Concerted evolution within a trypsin gene cluster in Drosophila. Mol. Biol. Evol. 16, 1117–1124.PubMedGoogle Scholar
  48. Watterson G. A. 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276.CrossRefPubMedGoogle Scholar
  49. Weiss A., Mcdonough D., Wertman B., Acakpo-satchivi L., Montgomery K., Kucherlapati R. et al. 1999 Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc. Natl. Acad. Sci. USA 96, 2958–2963.CrossRefPubMedGoogle Scholar
  50. Yoshida K., Kamiya T., Kawabe A. and Miyashita N. T. 2003 DNA polymorphism at the ACAULIS5 locus of the wild plant Arabidopsis thaliana. Genes Genet. Syst. 78, 11–21.CrossRefPubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2007

Authors and Affiliations

  1. 1.State Key Laboratory of Pharmaceutical Biotechnology, Department of BiologyNanjing UniversityNanjingChina
  2. 2.Center for Drug Discovery and Design, State Key Laboratory of Drug Research, Shanghai Institute of Materia MedicaChinese Academy of SciencesShanghaiChina

Personalised recommendations