A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism

Genetics

Volumn 169, Issue 3, 2005, Pages 1601-1615

  Schmid, Karl J ^a   Ramos Onsins, Sebastian ^a   Ringys Beckstein, Henriette ^a   Weisshaar, Bernd ^b,c   Mitchell Olds, Thomas ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; CODON; CONTROLLED STUDY; DNA POLYMORPHISM; DNA SEQUENCE; GENE LOCUS; GENETIC VARIABILITY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PLANT GENETICS; PRIORITY JOURNAL; REVIEW;

ARABIDOPSIS; BASE SEQUENCE; DNA, PLANT; GENOME, PLANT; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; SELECTION (GENETICS); VARIATION (GENETICS);

EID: 17444402038     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.033795     Document Type: Review

References (84)

1. ABBOTT, R. J., and M. F. GOMES, 1989 Population genetic structure and outcrossing rate of Arabidopsis thaliana. Heredity 42: 411-418.
2. AKEY, J., M. EBERLE, M. RIEDER, C. CARLSON, M. SHRIVER et al., 2004 Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2: e286.
3. ALTSHULER, D., V. POLLARA, C. C. W. VAN ETTEN, J. BALDWIN, L. LINTON et al., 2000 SNP map of the human genome generated by reduced representation sequencing. Nature 407: 513-516.
4. BEGUN, D., and C. AQUADRO, 1992 Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356: 519-520.
5. BERGELSON, J., C. PURRINGTON and G. WICHMANN, 1998 Promiscuity in transgenic plants. Nature 395: 25.
6. BLACK, W., C. BAER, M. ANTOLIND and N. DUTEAU, 2001 Population genomics: genome-wide sampling of insect populations. Annu. Rev. Entomol. 46: 441-469.
7. BUSTAMANTE, C., R. NIELSEN, S. SAWYER, K. OLSEN, M. PURUGGANAN et al., 2002 The cost of inbreeding in Arabidopsis. Nature 416: 531-534.
8. CAICEDO, A. L., B. A. SCHAAL and B. N. KUNKEL, 1998 Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 302-306.
9. CHARLESWORTH, B., M. MORGAN and D. CHARLESWORTH, 1993 The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.
10. CHARLESWORTH, D., 2003 Effects of inbreeding on the genetic diversity of populations. Philos. Trans. R. Soc. Lond. B 358: 1051-1070.
11. CLAUSS, M., and T. MITCHELL-OLDS, 2004 Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes. Genetics 166: 1419-1436.
12. COPENHAVER, G., K. NICKEL, T. KUROMORI, M. BENITO, S. KAUL et al., 1999 Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286: 2468-2474.
13. DURET, L., and D. MOUCHIROUD, 1999 Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 4482-4487.
14. DVORAK, J., M. LUO and Z. YANG, 1998 Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148: 423-434.
15. FAY, J. C., and C.-I WU, 2000 Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
16. FU, Y.-X., 1997 Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
17. FU, Y.-X., and W.-H. LI, 1993 Statistical tests of neutrality of mutations. Genetics 133: 693-709.
18. GLINKA, S., L. OMETTO, S. MOUSSET, W. STEPHAN and D. DE LORENZO, 2003 Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics 165: 1269-1278.
19. HAGENBLAD, J., and M. NORDBORG, 2002 Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana. Genetics 161: 289-298.
20. HAMBLIN, M., S. MITCHELL, G. WHITE, J. ALLEGO, R. KUKATLA et al., 2004 Comparative population genetics of the Panicoid grasses: sequence polymorphism, linkage disequilibrium and selection in a diverse sample of Sorghum bicolor. Genetics 167: 471-483.
21. HANFSTINGL, U., A. BERRY, E. E. KELLOG, J. T. COSTA, III, W. RÜDIGER et al., 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.
22. HASTINGS, W., 1970 Monte Carlo sampling methods using Markov chains and their applications. Biometrika 57: 57-109.
23. HAUBOLD, B., J. KROYMANN, A. RATZKA, T. MITCHELL-OLDS and T. WIEHE, 2002 Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana. Genetics 161: 1269-1278.
24. HAUPT, W., T. FISCHER, S. WINDERL, P. FRANSZ and R. TORRES-RUIZ, 2001 The CENTROMERE1 (CEN1) region of Arabidopsis thaliana: architecture and functional impact of chromatin. Plant J. 27: 285-296.
25. HAUSER, M.-T., B. HARR and C. SCHLÖTTERER, 2001 Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol. Biol. Evol. 18: 1754-1763.
26. HEDRICK, P., and L. HOLDEN, 1979 Hitch-hiking: an alternative to coadaptation for the barley and slender wild oat examples. Heredity 43: 79-86.
27. HUDSON, R., 1993 The how and why of generating gene genealogies, pp. 23-36 in Mechanisms of Molecular Evolution, edited by N. TAKAHATA and A. CLARK. Sinauer Associates, Sunderland, MA.
28. HUDSON, R., 2000 Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338.
29. HUDSON, R. R., 1990 Gene genealogies and the coalescent process, pp. 1-44 in Oxford Surveys in Evolutionary Biology, Vol. 7, edited by D. FUTUYMA and J. ANTONOVICS. Oxford University Press, London/New York/Oxford.
30. HUDSON, R. R., M. KREITMAN and M. AGUADÉ, 1987 A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153-159.
31. INNAN, H., and W. STEPHAN, 2000 The coalescent in an exponentially growing metapopulation and its application to Arabidopsis thaliana. Genetics 155: 2015-2019.
32. JUKES, T., and C. CANTOR, 1969 Evolution of protein molecules, pp. 21-132 in Mammalian Protein Metabolism, edited by H. MUNRO. Academic Press, New York.
33. KAWABE, A., and N. MIYASHITA, 1999 DNA variation in the basic chitinase locus (ChiB) region of the wild plant Arabidopsis thaliana. Genetics 153: 1445-1453.
34. KAWABE, A., H. INNANA, R. TERAUCHI and N. T. MIYASHITA, 1997 Nucleotide polymorphism in the acidic chitinase locus (ChiA) region of the wild plant Arabidopsis thaliana. Mol. Biol. Evol 14: 1303-1315.
35. KAWABE, A., K. YAMANE and N. MIYASHITA, 2000 DNA polymorphism at the cytosolic phosphoglucose isomerase (PgiC) locus of the wild plant Arabidopsis thaliana. Genetics 156: 1339-1347.
36. KLIMAN, R., and J. HEY, 1993 DNA sequence variation at the period locus within and among species of the Drosophila melanogaster species complex. Genetics 133: 375-387.
37. KOCH, M., B. HAUBOLD and T. MITCHELL-OLDS, 2000 Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis and related genera (Brassicaeae). Mol. Biol. Evol. 17: 1483-1498.
38. KOENKER, R., and K. HALLOCK, 2001 Quantile regression. J. Econ. Perspect. 15: 143-156.
39. KRAFT, T., T. SALL, I. MAGNUSSON-RADING, N. NILSSON and C. HALLDEN, 1998 Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics 150: 1239-1244.
40. KROYMANN, J., S. DONNERHACKE, D. SCHNABELRAUCH and T. MITCHELL-OLDS, 2003 Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc. Natl. Acad. Sci. USA 100: 14587-14592.
41. KUHNER, M., J. YAMATO and J. FELSENSTEIN, 1995 Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. Genetics 140: 1421-1430.
42. KUITTINEN, H., and M. AGUADÉ, 2000 Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana. Genetics 155: 863-872.
43. LUIKART, G., P. ENGLAND, D. TALLMON, S. JORDAN and P. TABERLET, 2003 The power and promise of population genomics: from genotyping to genome typing. Nat. Rev. Genet. 4: 981-994.
44. MAURICIO, R., E. STAHL, T. KORVES, D. TIAN, M. KREITMAN et al., 2003 Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163: 735-746.
45. MAYNARD SMITH, J., and J. HAIGH, 1974 The hitch-hiking effect of a favorable gene. Genet. Res. 23: 23-35.
46. MCDONALD, J., and M. KREITMAN, 1991 Adaptive evolution at the Adh locus in Drosophila. Nature 351: 652-654.
47. METROPOLIS, N., A. ROSENBEUTH, M. ROSENBLUTH, A. TELLER and E. TELLER, 1953 Equations of state calculations by fast computing machines. J. Chem. Phys. 21: 1087-1091.
48. MITCHELL-OLDS, T., 2001 Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16: 693-700.
49. NEI, M., 1987 Molecular Evolutionary Genetics. Columbia University Press, New York.
50. NICKERSON, D., V. O. TOBE and S. L. TAYLOR, 1997 PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Genome Res. 25: 2745-2751.
51. NORDBORG, M., 2000 Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154: 923-929.
52. NORDBORG, M., and P. DONNEELY, 1997 The coalescent process with selfing. Genetics 146: 1185-1195.
53. NORDBORG, M., and S. TAVARÉ, 2002 Linkage disequilibrium: what history has to tell us. Trends Genet. 18: 83-90.
54. NORDBORG, M., J. BOREVITZ, J. BERGELSON, C. BERRY, J. CHORY et al., 2002 The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 30: 190-193.
55. OLSEN, K., A. WOMACK, A. GARRETT, J. SUDDITH and M. PURUGGANAN, 2002 Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway. Genetics 160: 1641-1650.
56. PLUZHNIKOV, A., and P. DONNELLY, 1996 Optimal sequencing strategies for surveying molecular genetic diversity. Genetics 144: 1247-1262.
57. PURUGGANAN, M., and J. SUDDITH, 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.
58. PURUGGANAN, M. D., and J. I. SUDDITH, 1998 Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: non-neutral evolution and naturally occurring variation in floral homeotic function. Proc. Natl. Acad. Sci. USA 95: 8130-8134.
59. RAMOS-ONSINS, S., B. STRANGER, T. MITCHELL-OLDS and M. AGUADÉ, 2004 Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166: 372-388.
60. ROZAS, J., and R. ROZAS, 1999 DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
61. SCHAEFFER, S., 2002 Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura. Genet. Res. 80: 163-175.
62. SCHARF, F., F. JUANES and M. SUTHERLAND, 1998 Inferring ecological relationships from the edges of scatter diagrams: comparison of regression techniques. Ecology 79: 448-460.
63. SCHMID, K., T. ROSLEFF-SÖRENSEN, R. STRACKE, O. TÖRJEK, T. ALTMANN et al., 2003 Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res. 13: 1250-1257.
64. SHARBEL, T., B. HAUBOLD and T. MITCHELL-OLDS, 2000 Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol. Ecol. 9: 2109-2118.
65. SHEPARD, K., and M. PURUGGANAN, 2003 Molecular population genetics of the Arabidopsis CLAVATA2 region: the genomic scale of variation and selection in a selfing species. Genetics 163: 1083-1095.
66. SOKAL, R. R., and F. J. ROHLF, 1995 Biometry. Sinauer Associates, Sunderland, MA.
67. STAHL, E., G. DWYER, R. MAURICIO, M. KREITMAN and J. BERGELSON, 1999 Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667-671.
68. STEPHAN, W., and C. LANGLEY, 1998 DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics 150: 1585-1593.
69. TAJIMA, F., 1983 Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437-460.
70. TAJIMA, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
71. TAVARÉ, S., 1984 Line-of-descent and genealogical processes, and their applications in population genetics models. Theor. Popul. Biol. 26: 119-164.
72. TENAILLON, M., M. SAWKINS, A. LONG, R. GAUT, J. DOEBLEY et al., 2001 Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L). Proc. Natl. Acad. Sci. USA 98: 9161-9166.
73. TENAILLON, M., J. U'REN, O. TENAILLON and B. GAUTH, 2004 Selection versus demography: a multilocus investigation of the domestication process in maize. Mol. Biol. Evol. 21: 1214-1225.
74. THOMPSON, J. D., D. G. HIGGINS and T. J. GIBSON, 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.
75. TIAN, D., H. ARAKI, E. STAHL, J. BERGELSON and M. KREITMAN, 2002 Signature of balancing selection in Arabidopsis. Proc. Natl. Acad. Sci. USA 99: 11525-11530.
76. WAKELEY, J., 1999 Non-equilibrium migration in human history. Genetics 153: 1863-1871.
77. WAKELEY, J., 2001 The coalescent in an island model of population subdivision with variation among demes. Theor. Popul. Biol. 59: 133-144.
78. WAKELEY, J., 2004 Metapopulation models for historical inference. Mol. Ecol. 13: 865-875.
79. WAKELEY, J., and N. ALIACAR, 2001 Gene genealogies in a metapopulation. Genetics 159: 893-905.
80. WALL, J., 1999 Recombination and the power of statistical tests of neutrality. Genet. Res. 74: 65-79.
81. WALL, J., 2000 Detecting ancient admixture in humans using sequence polymorphism data. Genetics 154: 1271-1279.
82. WATTERSON, G. A., 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7: 256-276.
83. WRIGHT, S., N. AGRAWAL and T. BUREAU, 2003 Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res. 13: 1897-1903.
84. ZHANG, L., and B. GAUT, 2003 Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Mol. Biol. Evol. 13: 2533-2540.