Skip to main content
Genetics logoLink to Genetics
. 2003 Nov;165(3):1475–1488. doi: 10.1093/genetics/165.3.1475

An analysis of microsatellite loci in Arabidopsis thaliana: mutational dynamics and application.

V Vaughan Symonds 1, Alan M Lloyd 1
PMCID: PMC1462854  PMID: 14668396

Abstract

Microsatellite loci are among the most commonly used molecular markers. These loci typically exhibit variation for allele frequency distribution within a species. However, the factors contributing to this variation are not well understood. To expand on the current knowledge of microsatellite evolution, 20 microsatellite loci were examined for 126 accessions of the flowering plant, Arabidopsis thaliana. Substantial variability in mutation pattern among loci was found, most of which cannot be explained by the assumptions of the traditional stepwise mutation model or infinite alleles model. Here it is shown that the degree of locus diversity is strongly correlated with the number of contiguous repeats, more so than with the total number of repeats. These findings support a strong role for repeat disruptions in stabilizing microsatellite loci by reducing the substrate for polymerase slippage and recombination. Results of cluster analyses are also presented, demonstrating the potential of microsatellite loci for resolving relationships among accessions of A. thaliana.

Full Text

The Full Text of this article is available as a PDF (238.3 KB).

Selected References

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

  1. Alonso-Blanco C., Koornneef M. Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci. 2000 Jan;5(1):22–29. doi: 10.1016/s1360-1385(99)01510-1. [DOI] [PubMed] [Google Scholar]
  2. Bachtrog D., Agis M., Imhof M., Schlötterer C. Microsatellite variability differs between dinucleotide repeat motifs-evidence from Drosophila melanogaster. Mol Biol Evol. 2000 Sep;17(9):1277–1285. doi: 10.1093/oxfordjournals.molbev.a026411. [DOI] [PubMed] [Google Scholar]
  3. Balloux François, Lugon-Moulin Nicolas. The estimation of population differentiation with microsatellite markers. Mol Ecol. 2002 Feb;11(2):155–165. doi: 10.1046/j.0962-1083.2001.01436.x. [DOI] [PubMed] [Google Scholar]
  4. Barker G. C. Microsatellite DNA: a tool for population genetic analysis. Trans R Soc Trop Med Hyg. 2002 Apr;96 (Suppl 1):S21–S24. doi: 10.1016/s0035-9203(02)90047-7. [DOI] [PubMed] [Google Scholar]
  5. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  6. Bergelson J., Stahl E., Dudek S., Kreitman M. Genetic variation within and among populations of Arabidopsis thaliana. Genetics. 1998 Mar;148(3):1311–1323. doi: 10.1093/genetics/148.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Borevitz Justin O., Liang David, Plouffe David, Chang Hur-Song, Zhu Tong, Weigel Detlef, Berry Charles C., Winzeler Elizabeth, Chory Joanne. Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res. 2003 Mar;13(3):513–523. doi: 10.1101/gr.541303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boutin-Ganache I., Raposo M., Raymond M., Deschepper C. F. M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques. 2001 Jul;31(1):24-6, 28. [PubMed] [Google Scholar]
  9. Brohede Jesper, Primmer Craig R., Møller Anders, Ellegren Hans. Heterogeneity in the rate and pattern of germline mutation at individual microsatellite loci. Nucleic Acids Res. 2002 May 1;30(9):1997–2003. doi: 10.1093/nar/30.9.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Casacuberta E, Puigdomènech P, Monfort A. Distribution of microsatellites in relation to coding sequences within the Arabidopsis thaliana genome. Plant Sci. 2000 Aug 8;157(1):97–104. doi: 10.1016/s0168-9452(00)00271-5. [DOI] [PubMed] [Google Scholar]
  11. Chakraborty R., Kimmel M., Stivers D. N., Davison L. J., Deka R. Relative mutation rates at di-, tri-, and tetranucleotide microsatellite loci. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1041–1046. doi: 10.1073/pnas.94.3.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clauss M. J., Cobban H., Mitchell-Olds T. Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaeae). Mol Ecol. 2002 Mar;11(3):591–601. doi: 10.1046/j.0962-1083.2002.01465.x. [DOI] [PubMed] [Google Scholar]
  13. Cornuet J. M., Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996 Dec;144(4):2001–2014. doi: 10.1093/genetics/144.4.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cunniff C. Molecular mechanisms in neurologic disorders. Semin Pediatr Neurol. 2001 Sep;8(3):128–134. doi: 10.1053/spen.2001/26446. [DOI] [PubMed] [Google Scholar]
  15. Driscoll Carlos A., Menotti-Raymond Marilyn, Nelson George, Goldstein David, O'Brien Stephen J. Genomic microsatellites as evolutionary chronometers: a test in wild cats. Genome Res. 2002 Mar;12(3):414–423. doi: 10.1101/gr.185702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eckert Kristin A., Mowery Andrew, Hile Suzanne E. Misalignment-mediated DNA polymerase beta mutations: comparison of microsatellite and frame-shift error rates using a forward mutation assay. Biochemistry. 2002 Aug 20;41(33):10490–10498. doi: 10.1021/bi025918c. [DOI] [PubMed] [Google Scholar]
  17. Ellegren H. Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet. 2000 Dec;16(12):551–558. doi: 10.1016/s0168-9525(00)02139-9. [DOI] [PubMed] [Google Scholar]
  18. Estoup Arnaud, Jarne Philippe, Cornuet Jean-Marie. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol. 2002 Sep;11(9):1591–1604. doi: 10.1046/j.1365-294x.2002.01576.x. [DOI] [PubMed] [Google Scholar]
  19. Gill P., Jeffreys A. J., Werrett D. J. Forensic application of DNA 'fingerprints'. Nature. 1985 Dec 12;318(6046):577–579. doi: 10.1038/318577a0. [DOI] [PubMed] [Google Scholar]
  20. Grimaldi M. C., Crouau-Roy B. Microsatellite allelic homoplasy due to variable flanking sequences. J Mol Evol. 1997 Mar;44(3):336–340. doi: 10.1007/pl00006151. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Hile S. E., Yan G., Eckert K. A. Somatic mutation rates and specificities at TC/AG and GT/CA microsatellite sequences in nontumorigenic human lymphoblastoid cells. Cancer Res. 2000 Mar 15;60(6):1698–1703. [PubMed] [Google Scholar]
  23. Innan H., Terauchi R., Miyashita N. T. Microsatellite polymorphism in natural populations of the wild plant Arabidopsis thaliana. Genetics. 1997 Aug;146(4):1441–1452. doi: 10.1093/genetics/146.4.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Katti M. V., Ranjekar P. K., Gupta V. S. Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol. 2001 Jul;18(7):1161–1167. doi: 10.1093/oxfordjournals.molbev.a003903. [DOI] [PubMed] [Google Scholar]
  25. Litt M., Luty J. A. A hypervariable microsatellite revealed by in vitro amplification of a dinucleotide repeat within the cardiac muscle actin gene. Am J Hum Genet. 1989 Mar;44(3):397–401. [PMC free article] [PubMed] [Google Scholar]
  26. Lukowitz W., Gillmor C. S., Scheible W. R. Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 2000 Jul;123(3):795–805. doi: 10.1104/pp.123.3.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Matsuoka Y., Mitchell S. E., Kresovich S., Goodman M., Doebley J. Microsatellites in Zea - variability, patterns of mutations, and use for evolutionary studies. Theor Appl Genet. 2002 Feb;104(2-3):436–450. doi: 10.1007/s001220100694. [DOI] [PubMed] [Google Scholar]
  28. McCouch S. R., Chen X., Panaud O., Temnykh S., Xu Y., Cho Y. G., Huang N., Ishii T., Blair M. Microsatellite marker development, mapping and applications in rice genetics and breeding. Plant Mol Biol. 1997 Sep;35(1-2):89–99. [PubMed] [Google Scholar]
  29. Moriguchi Y., Iwata H., Ujino-Ihara T., Yoshimura K., Taira H., Tsumura Y. Development and characterization of microsatellite markers for Cryptomeria japonica D.Don. Theor Appl Genet. 2002 Nov 15;106(4):751–758. doi: 10.1007/s00122-002-1149-0. [DOI] [PubMed] [Google Scholar]
  30. Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3321–3323. doi: 10.1073/pnas.70.12.3321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Noor M. A., Kliman R. M., Machado C. A. Evolutionary history of microsatellites in the obscura group of Drosophila. Mol Biol Evol. 2001 Apr;18(4):551–556. doi: 10.1093/oxfordjournals.molbev.a003834. [DOI] [PubMed] [Google Scholar]
  32. Noël L., Moores T. L., van Der Biezen E. A., Parniske M., Daniels M. J., Parker J. E., Jones J. D. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell. 1999 Nov;11(11):2099–2112. [PMC free article] [PubMed] [Google Scholar]
  33. Ranum Laura P. W., Day John W. Dominantly inherited, non-coding microsatellite expansion disorders. Curr Opin Genet Dev. 2002 Jun;12(3):266–271. doi: 10.1016/s0959-437x(02)00297-6. [DOI] [PubMed] [Google Scholar]
  34. Richard G. F., Pâques F. Mini- and microsatellite expansions: the recombination connection. EMBO Rep. 2000 Aug;1(2):122–126. doi: 10.1093/embo-reports/kvd031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rolfsmeier M. L., Lahue R. S. Stabilizing effects of interruptions on trinucleotide repeat expansions in Saccharomyces cerevisiae. Mol Cell Biol. 2000 Jan;20(1):173–180. doi: 10.1128/mcb.20.1.173-180.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rubinsztein D. C., Amos B., Cooper G. Microsatellite and trinucleotide-repeat evolution: evidence for mutational bias and different rates of evolution in different lineages. Philos Trans R Soc Lond B Biol Sci. 1999 Jun 29;354(1386):1095–1099. doi: 10.1098/rstb.1999.0465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sakamoto T., Okamoto N. [Microsatellite linkage map of rainbow trout and its application for QTL analysis]. Tanpakushitsu Kakusan Koso. 2000 Dec;45(17 Suppl):2872–2879. [PubMed] [Google Scholar]
  38. Schug M. D., Wetterstrand K. A., Gaudette M. S., Lim R. H., Hutter C. M., Aquadro C. F. The distribution and frequency of microsatellite loci in Drosophila melanogaster. Mol Ecol. 1998 Jan;7(1):57–70. doi: 10.1046/j.1365-294x.1998.00304.x. [DOI] [PubMed] [Google Scholar]
  39. Sharbel T. F., Haubold B., Mitchell-Olds T. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol Ecol. 2000 Dec;9(12):2109–2118. doi: 10.1046/j.1365-294x.2000.01122.x. [DOI] [PubMed] [Google Scholar]
  40. Shriver M. D., Jin L., Chakraborty R., Boerwinkle E. VNTR allele frequency distributions under the stepwise mutation model: a computer simulation approach. Genetics. 1993 Jul;134(3):983–993. doi: 10.1093/genetics/134.3.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sia E. A., Kokoska R. J., Dominska M., Greenwell P., Petes T. D. Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes. Mol Cell Biol. 1997 May;17(5):2851–2858. doi: 10.1128/mcb.17.5.2851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thuillet Anne-Céline, Bru David, David Jacques, Roumet Pierre, Santoni Sylvain, Sourdille Pierre, Bataillon Thomas. Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp durum desf. Mol Biol Evol. 2002 Jan;19(1):122–125. doi: 10.1093/oxfordjournals.molbev.a003977. [DOI] [PubMed] [Google Scholar]
  43. Vigouroux Yves, Jaqueth Jennifer S., Matsuoka Yoshihiro, Smith Oscar S., Beavis William D., Smith J. Stephen C., Doebley John. Rate and pattern of mutation at microsatellite loci in maize. Mol Biol Evol. 2002 Aug;19(8):1251–1260. doi: 10.1093/oxfordjournals.molbev.a004186. [DOI] [PubMed] [Google Scholar]
  44. Vision T. J., Brown D. G., Tanksley S. D. The origins of genomic duplications in Arabidopsis. Science. 2000 Dec 15;290(5499):2114–2117. doi: 10.1126/science.290.5499.2114. [DOI] [PubMed] [Google Scholar]
  45. Wierdl M., Dominska M., Petes T. D. Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics. 1997 Jul;146(3):769–779. doi: 10.1093/genetics/146.3.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zane L., Bargelloni L., Patarnello T. Strategies for microsatellite isolation: a review. Mol Ecol. 2002 Jan;11(1):1–16. doi: 10.1046/j.0962-1083.2001.01418.x. [DOI] [PubMed] [Google Scholar]
  47. van Treuren R., Kuittinen H., Kärkkäinen K., Baena-Gonzalez E., Savolainen O. Evolution of microsatellites in Arabis petraea and Arabis lyrata, outcrossing relatives of Arabidopsis thaliana. Mol Biol Evol. 1997 Mar;14(3):220–229. doi: 10.1093/oxfordjournals.molbev.a025758. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES