Home LiteratureArticle Details
PMID: 15654111 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Genetics ·Vol. 169 ·No. 3 ·2005-03-00 ·Pages 1601-15

Schmid KJ, Ramos-Onsins S, Ringys-Beckstein H, Weisshaar B, Mitchell-Olds T

Abstract

The simultaneous analysis of multiple genomic loci is a powerful approach to studying the effects of population history and natural selection on patterns of genetic variation of a species. By surveying nucleotide sequence polymorphism at 334 randomly distributed genomic regions in 12 accessions of Arabidopsis thaliana, we examined whether a standard neutral model of nucleotide sequence polymorphism is consistent with observed data. The average nucleotide diversity was 0.0071 for total sites and 0.0083 for silent sites. Although levels of diversity are variable among loci, no correlation with local recombination rate was observed, but polymorphism levels were correlated for physically linked loci (<250 kb). We found that observed distributions of Tajima's D- and D/D(min)- and of Fu and Li's D-, D*- and F-, F*-statistics differed significantly from the expected distributions under a standard neutral model due to an excess of rare polymorphisms and high variances. Observed and expected distributions of Fay and Wu's H were not different, suggesting that demographic processes and not selection at multiple loci are responsible for the deviation from a neutral model. Maximum-likelihood comparisons of alternative demographic models like logistic population growth, glacial refugia, or past bottlenecks did not produce parameter estimates that were more consistent with observed patterns. However, exclusion of highly polymorphic "outlier loci" resulted in a fit to the logistic growth model. Various tests of neutrality revealed a set of candidate loci that may evolve under selection.

MeSH Terms
Arabidopsis/genetics Base Sequence DNA, Plant/chemistry,genetics Genetic Variation Genome, Plant Models, Genetic Molecular Sequence Data Polymorphism, Genetic Selection, Genetic
Chemicals
DNA, Plant
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Schmid Karl J
Department of Genetics and Evolution, Max-Planck Institute of Chemical Ecology, Jena, Germany. [email protected]
Ramos-Onsins Sebastian
Ringys-Beckstein Henriette
Weisshaar Bernd
Mitchell-Olds Thomas
References (71)
71 references, click to expand
  1. 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):811-28 PMID: 7851777
  2. Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling.
    Genetics. 1995 Aug;140(4):1421-30 PMID: 7498781
  3. Optimal sequencing strategies for surveying molecular genetic diversity.
    Genetics. 1996 Nov;144(3):1247-62 PMID: 8913765
  4. PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing.
    Nucleic Acids Res. 1997 Jul 15;25(14):2745-51 PMID: 9207020
  5. The coalescent process with selfing.
    Genetics. 1997 Jul;146(3):1185-95 PMID: 9215919
  6. DNA variation in the basic chitinase locus (ChiB) region of the wild plant Arabidopsis thaliana.
    Genetics. 1999 Nov;153(3):1445-53 PMID: 10545472
  7. Nonequilibrium migration in human history.
    Genetics. 1999 Dec;153(4):1863-71 PMID: 10581291
  8. Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima).
    Genetics. 1998 Nov;150(3):1239-44 PMID: 9799275
  9. DNA polymorphism in lycopersicon and crossing-over per physical length.
    Genetics. 1998 Dec;150(4):1585-93 PMID: 9832534
  10. Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):302-6 PMID: 9874813
  11. Molecular population genetics of floral homeotic loci. Departures from the equilibrium-neutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana.
    Genetics. 1999 Feb;151(2):839-48 PMID: 9927474
  12. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis.
    Bioinformatics. 1999 Feb;15(2):174-5 PMID: 10089204
  13. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482-7 PMID: 10200288
  14. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis.
    Nature. 1999 Aug 12;400(6745):667-71 PMID: 10458161
  15. Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana.
    Genetics. 2002 Jul;161(3):1269-78 PMID: 12136029
  16. Signature of balancing selection in Arabidopsis.
    Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11525-30 PMID: 12172007
  17. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana.
    Genetics. 2003 Feb;163(2):735-46 PMID: 12618410
  18. Molecular population genetics of the Arabidopsis CLAVATA2 region. The genomic scale of variation and selection in a selfing species.
    Genetics. 2003 Mar;163(3):1083-95 PMID: 12663546
  19. Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura.
    Genet Res. 2002 Dec;80(3):163-75 PMID: 12688655
  20. Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana.
    Genome Res. 2003 Jun;13(6A):1250-7 PMID: 12799357
  21. Effects of inbreeding on the genetic diversity of populations.
    Philos Trans R Soc Lond B Biol Sci. 2003 Jun 29;358(1434):1051-70 PMID: 12831472
  22. Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana.
    Genome Res. 2003 Aug;13(8):1897-903 PMID: 12902382
  23. The power and promise of population genomics: from genotyping to genome typing.
    Nat Rev Genet. 2003 Dec;4(12):981-94 PMID: 14631358
  24. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14587-92 PMID: 14506289
  25. Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome?
    Genome Res. 2003 Dec;13(12):2533-40 PMID: 14656961
  26. Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach.
    Genetics. 2003 Nov;165(3):1269-78 PMID: 14668381
  27. Metapopulation models for historical inference.
    Mol Ecol. 2004 Apr;13(4):865-75 PMID: 15012761
  28. Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata.
    Genetics. 2004 Jan;166(1):373-88 PMID: 15020431
  29. Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes.
    Genetics. 2004 Mar;166(3):1419-36 PMID: 15082560
  30. Comparative population genetics of the panicoid grasses: sequence polymorphism, linkage disequilibrium and selection in a diverse sample of sorghum bicolor.
    Genetics. 2004 May;167(1):471-83 PMID: 15166170
  31. Selection versus demography: a multilocus investigation of the domestication process in maize.
    Mol Biol Evol. 2004 Jul;21(7):1214-25 PMID: 15014173
  32. Population history and natural selection shape patterns of genetic variation in 132 genes.
    PLoS Biol. 2004 Oct;2(10):e286 PMID: 15361935
  33. The hitch-hiking effect of a favourable gene.
    Genet Res. 1974 Feb;23(1):23-35 PMID: 4407212
  34. On the number of segregating sites in genetical models without recombination.
    Theor Popul Biol. 1975 Apr;7(2):256-76 PMID: 1145509
  35. Evolutionary relationship of DNA sequences in finite populations.
    Genetics. 1983 Oct;105(2):437-60 PMID: 6628982
  36. Line-of-descent and genealogical processes, and their applications in population genetics models.
    Theor Popul Biol. 1984 Oct;26(2):119-64 PMID: 6505980
  37. A test of neutral molecular evolution based on nucleotide data.
    Genetics. 1987 May;116(1):153-9 PMID: 3110004
  38. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  39. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  40. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster.
    Nature. 1992 Apr 9;356(6369):519-20 PMID: 1560824
  41. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex.
    Genetics. 1993 Feb;133(2):375-87 PMID: 8436278
  42. Statistical tests of neutrality of mutations.
    Genetics. 1993 Mar;133(3):693-709 PMID: 8454210
  43. The effect of deleterious mutations on neutral molecular variation.
    Genetics. 1993 Aug;134(4):1289-303 PMID: 8375663
  44. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  45. Genetic definition and sequence analysis of Arabidopsis centromeres.
    Science. 1999 Dec 24;286(5449):2468-74 PMID: 10617454
  46. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization.
    Genetics. 2000 Feb;154(2):923-9 PMID: 10655241
  47. Detecting ancient admixture in humans using sequence polymorphism data.
    Genetics. 2000 Mar;154(3):1271-9 PMID: 10757768
  48. Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana.
    Genetics. 2000 Jun;155(2):863-72 PMID: 10835405
  49. Hitchhiking under positive Darwinian selection.
    Genetics. 2000 Jul;155(3):1405-13 PMID: 10880498
  50. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae).
    Mol Biol Evol. 2000 Oct;17(10):1483-98 PMID: 11018155
  51. The coalescent in an exponentially growing metapopulation and its application to Arabidopsis thaliana.
    Genetics. 2000 Aug;155(4):2015-9 PMID: 11032470
  52. An SNP map of the human genome generated by reduced representation shotgun sequencing.
    Nature. 2000 Sep 28;407(6803):513-6 PMID: 11029002
  53. DNA polymorphism at the cytosolic phosphoglucose isomerase (PgiC) locus of the wild plant Arabidopsis thaliana.
    Genetics. 2000 Nov;156(3):1339-47 PMID: 11063706
  54. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe.
    Mol Ecol. 2000 Dec;9(12):2109-18 PMID: 11123622
  55. Population genomics: genome-wide sampling of insect populations.
    Annu Rev Entomol. 2001;46:441-69 PMID: 11112176
  56. The coalescent in an island model of population subdivision with variation among demes.
    Theor Popul Biol. 2001 Mar;59(2):133-44 PMID: 11302758
  57. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.).
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9161-6 PMID: 11470895
  58. 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):1754-63 PMID: 11504855
  59. The centromere1 (CEN1) region of Arabidopsis thaliana: architecture and functional impact of chromatin.
    Plant J. 2001 Aug;27(4):285-96 PMID: 11532174
  60. Gene genealogies in a metapopulation.
    Genetics. 2001 Oct;159(2):893-905 PMID: 11606561
  61. The extent of linkage disequilibrium in Arabidopsis thaliana.
    Nat Genet. 2002 Feb;30(2):190-3 PMID: 11780140
  62. Linkage disequilibrium: what history has to tell us.
    Trends Genet. 2002 Feb;18(2):83-90 PMID: 11818140
  63. Generating samples under a Wright-Fisher neutral model of genetic variation.
    Bioinformatics. 2002 Feb;18(2):337-8 PMID: 11847089
  64. The cost of inbreeding in Arabidopsis.
    Nature. 2002 Apr 4;416(6880):531-4 PMID: 11932744
  65. Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway.
    Genetics. 2002 Apr;160(4):1641-50 PMID: 11973317
  66. Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana.
    Genetics. 2002 May;161(1):289-98 PMID: 12019242
  67. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection.
    Genetics. 1997 Oct;147(2):915-25 PMID: 9335623
  68. Nucleotide polymorphism in the acidic chitinase locus (ChiA) region of the wild plant Arabidopsis thaliana.
    Mol Biol Evol. 1997 Dec;14(12):1303-15 PMID: 9402740
  69. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species.
    Genetics. 1998 Jan;148(1):423-34 PMID: 9475752
  70. Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: nonneutral evolution and naturally occurring variation in floral homeotic function.
    Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8130-4 PMID: 9653152
  71. Promiscuity in transgenic plants.
    Nature. 1998 Sep 3;395(6697):25 PMID: 9738493
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2005-03-00
Epub
2005-00-16
Pages
1601-15
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1449538
Subset
IM
Databases
GENBANK
CW672529, CW672530, CW672531, CW672532, CW672533, CW672534, CW672535, CW672536, CW672537, CW672538, CW672539, CW672540, CW672541, CW672542, CW672543, CW672544, CW672545, CW672546, CW672547, CW672548, CW672549, CW672550, CW672551, CW672552, CW672553, CW672554, CW672555, CW672556, CW672557, CW672558, CW672559, CW672560, CW672561, CW672562, CW672563, CW672564, CW672565, CW672566, CW672567, CW672568, CW672569, CW672570, CW672571, CW672572, CW672573, CW672574, CW672575, CW672576, CW672577, CW672578, CW672579, CW672580, CW672581, CW672582, CW672583, CW672584, CW672585, CW672586, CW672587, CW672588, CW672589, CW672590, CW672591, CW672592, CW672593, CW672594, CW672595, CW672596, CW672597, CW672598, CW672599, CW672600, CW672601, CW672602, CW672603, CW672604, CW672605, CW672606, CW672607, CW672608, CW672609, CW672610, CW672611, CW672612, CW672613, CW672614, CW672615, CW672616, CW672617, CW672618, CW672619, CW672620, CW672621, CW672622, CW672623, CW672624, CW672625, CW672626, CW672627, CW672628, CW672629, CW672630, CW672631, CW672632, CW672633, CW672634, CW672635, CW672636, CW672637, CW672638, CW672639, CW672640, CW672641, CW672642, CW672643, CW672644, CW672645, CW672646, CW672647, CW672648, CW672649, CW672650, CW672651, CW672652, CW672653, CW672654, CW672655, CW672656, CW672657, CW672658, CW672659, CW672660, CW672661, CW672662, CW672663, CW672664, CW672665, CW672666, CW672667, CW672668, CW672669, CW672670, CW672671, CW672672, CW672673, CW672674, CW672675, CW672676, CW672677, CW672678, CW672679, CW672680, CW672681, CW672682, CW672683, CW672684, CW672685, CW672686, CW672687, CW672688, CW672689, CW672690, CW672691, CW672692, CW672693, CW672694, CW672695, CW672696, CW672697, CW672698, CW672699, CW672700, CW672701, CW672702, CW672703, CW672704, CW672705, CW672706, CW672707, CW672708, CW672709, CW672710, CW672711, CW672712, CW672713, CW672714, CW672715, CW672716, CW672717, CW672718, CW672719, CW672720, CW672721
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]