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. 2004 May;167(1):471–483. doi: 10.1534/genetics.167.1.471

Comparative population genetics of the panicoid grasses: sequence polymorphism, linkage disequilibrium and selection in a diverse sample of sorghum bicolor.

Martha T Hamblin 1, Sharon E Mitchell 1, Gemma M White 1, Javier Gallego 1, Rakesh Kukatla 1, Rod A Wing 1, Andrew H Paterson 1, Stephen Kresovich 1
PMCID: PMC1470838  PMID: 15166170

Abstract

Levels of genetic variation and linkage disequilibrium (LD) are critical factors in association mapping methods as well as in identification of loci that have been targets of selection. Maize, an outcrosser, has a high level of sequence variation and a limited extent of LD. Sorghum, a closely related but largely self-pollinating panicoid grass, is expected to have higher levels of LD. As a first step in estimation of population genetic parameters in sorghum, we surveyed 27 diverse S. bicolor accessions for sequence variation at a total of 29,186 bp in 95 short regions derived from genetically mapped RFLPs located throughout the genome. Consistent with its higher level of inbreeding, the extent of LD is at least severalfold greater in sorghum than in maize. Total sequence variation in sorghum is about fourfold lower than that in maize, while synonymous variation is fivefold lower, suggesting a smaller effective population size in sorghum. Because we surveyed a species-wide sample, the mating system, which primarily affects population-level diversity, may not be primarily responsible for this difference. Comparisons of polymorphism and divergence suggest that both directional and diversifying selection have played important roles in shaping variation in the sorghum genome.

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Selected References

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

  1. Baudry E., Kerdelhué C., Innan H., Stephan W. Species and recombination effects on DNA variability in the tomato genus. Genetics. 2001 Aug;158(4):1725–1735. doi: 10.1093/genetics/158.4.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bergelson J., Kreitman M., Stahl E. A., Tian D. Evolutionary dynamics of plant R-genes. Science. 2001 Jun 22;292(5525):2281–2285. doi: 10.1126/science.1061337. [DOI] [PubMed] [Google Scholar]
  3. Bishop J. G., Dean A. M., Mitchell-Olds T. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5322–5327. doi: 10.1073/pnas.97.10.5322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boughaleb D., Mansourati J., Genet L., Barra J., Mondine P., Blanc J. J. Stimulation cardiaque définitive après remplacement valvulaire aortique: incidence, facteurs prédictifs et pronostic à long terme. Arch Mal Coeur Vaiss. 1994 Jul;87(7):925–930. [PubMed] [Google Scholar]
  5. Bowers John E., Abbey Colette, Anderson Sharon, Chang Charlene, Draye Xavier, Hoppe Alison H., Jessup Russell, Lemke Cornelia, Lennington Jennifer, Li Zhikang. A high-density genetic recombination map of sequence-tagged sites for sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses. Genetics. 2003 Sep;165(1):367–386. doi: 10.1093/genetics/165.1.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bustamante Carlos D., Nielsen Rasmus, Sawyer Stanley A., Olsen Kenneth M., Purugganan Michael D., Hartl Daniel L. The cost of inbreeding in Arabidopsis. Nature. 2002 Apr 4;416(6880):531–534. doi: 10.1038/416531a. [DOI] [PubMed] [Google Scholar]
  7. Charlesworth B. Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol. 1998 May;15(5):538–543. doi: 10.1093/oxfordjournals.molbev.a025953. [DOI] [PubMed] [Google Scholar]
  8. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clegg M. T., Cummings M. P., Durbin M. L. The evolution of plant nuclear genes. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7791–7798. doi: 10.1073/pnas.94.15.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eyre-Walker A., Gaut R. L., Hilton H., Feldman D. L., Gaut B. S. Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4441–4446. doi: 10.1073/pnas.95.8.4441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fay J. C., Wyckoff G. J., Wu C. I. Positive and negative selection on the human genome. Genetics. 2001 Jul;158(3):1227–1234. doi: 10.1093/genetics/158.3.1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gale M. D., Devos K. M. Plant comparative genetics after 10 years. Science. 1998 Oct 23;282(5389):656–659. doi: 10.1126/science.282.5389.656. [DOI] [PubMed] [Google Scholar]
  13. Gaut B. S., Doebley J. F. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6809–6814. doi: 10.1073/pnas.94.13.6809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hill W. G. Estimation of linkage disequilibrium in randomly mating populations. Heredity (Edinb) 1974 Oct;33(2):229–239. doi: 10.1038/hdy.1974.89. [DOI] [PubMed] [Google Scholar]
  15. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hudson R. R., Slatkin M., Maddison W. P. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992 Oct;132(2):583–589. doi: 10.1093/genetics/132.2.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kondrashov Fyodor A., Rogozin Igor B., Wolf Yuri I., Koonin Eugene V. Selection in the evolution of gene duplications. Genome Biol. 2002 Jan 14;3(2):RESEARCH0008–RESEARCH0008. doi: 10.1186/gb-2002-3-2-research0008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Liu F., Charlesworth D., Kreitman M. The effect of mating system differences on nucleotide diversity at the phosphoglucose isomerase locus in the plant genus Leavenworthia. Genetics. 1999 Jan;151(1):343–357. doi: 10.1093/genetics/151.1.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Long A. D., Langley C. H. The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res. 1999 Aug;9(8):720–731. [PMC free article] [PubMed] [Google Scholar]
  20. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  21. Morrell Peter L., Lundy Karen E., Clegg Michael T. Distinct geographic patterns of genetic diversity are maintained in wild barley (Hordeum vulgare ssp. spontaneum) despite migration. Proc Natl Acad Sci U S A. 2003 Sep 8;100(19):10812–10817. doi: 10.1073/pnas.1633708100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nordborg M., Donnelly P. The coalescent process with selfing. Genetics. 1997 Jul;146(3):1185–1195. doi: 10.1093/genetics/146.3.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nordborg Magnus, Borevitz Justin O., Bergelson Joy, Berry Charles C., Chory Joanne, Hagenblad Jenny, Kreitman Martin, Maloof Julin N., Noyes Tina, Oefner Peter J. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet. 2002 Jan 7;30(2):190–193. doi: 10.1038/ng813. [DOI] [PubMed] [Google Scholar]
  24. Ohta T. Pattern of nucleotide substitutions in growth hormone-prolactin gene family: a paradigm for evolution by gene duplication. Genetics. 1993 Aug;134(4):1271–1276. doi: 10.1093/genetics/134.4.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ohta Tomoko. Near-neutrality in evolution of genes and gene regulation. Proc Natl Acad Sci U S A. 2002 Dec 2;99(25):16134–16137. doi: 10.1073/pnas.252626899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Paterson A. H., Lin Y. R., Li Z., Schertz K. F., Doebley J. F., Pinson S. R., Liu S. C., Stansel J. W., Irvine J. E. Convergent domestication of cereal crops by independent mutations at corresponding genetic Loci. Science. 1995 Sep 22;269(5231):1714–1718. doi: 10.1126/science.269.5231.1714. [DOI] [PubMed] [Google Scholar]
  27. Pollak E. On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics. 1987 Oct;117(2):353–360. doi: 10.1093/genetics/117.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rafalski Antoni. Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol. 2002 Apr;5(2):94–100. doi: 10.1016/s1369-5266(02)00240-6. [DOI] [PubMed] [Google Scholar]
  29. Remington D. L., Thornsberry J. M., Matsuoka Y., Wilson L. M., Whitt S. R., Doebley J., Kresovich S., Goodman M. M., Buckler E. S., 4th Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci U S A. 2001 Sep 18;98(20):11479–11484. doi: 10.1073/pnas.201394398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  31. Savolainen O., Langley C. H., Lazzaro B. P., Fr H. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol Biol Evol. 2000 Apr;17(4):645–655. doi: 10.1093/oxfordjournals.molbev.a026343. [DOI] [PubMed] [Google Scholar]
  32. Schloss J., Mitchell E., White M., Kukatla R., Bowers E., Paterson H., Kresovich S. Characterization of RFLP probe sequences for gene discovery and SSR development in Sorghum bicolor (L.) Moench. Theor Appl Genet. 2002 Jul 30;105(6-7):912–920. doi: 10.1007/s00122-002-0991-4. [DOI] [PubMed] [Google Scholar]
  33. Shepard Kristen A., Purugganan Michael D. Molecular population genetics of the Arabidopsis CLAVATA2 region. The genomic scale of variation and selection in a selfing species. Genetics. 2003 Mar;163(3):1083–1095. doi: 10.1093/genetics/163.3.1083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sunyaev S. R., Lathe W. C., 3rd, Ramensky V. E., Bork P. SNP frequencies in human genes an excess of rare alleles and differing modes of selection. Trends Genet. 2000 Aug;16(8):335–337. doi: 10.1016/s0168-9525(00)02058-8. [DOI] [PubMed] [Google Scholar]
  35. Tenaillon M. I., Sawkins M. C., Long A. D., Gaut R. L., Doebley J. F., Gaut B. S. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci U S A. 2001 Jul 24;98(16):9161–9166. doi: 10.1073/pnas.151244298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vigouroux Y., McMullen M., Hittinger C. T., Houchins K., Schulz L., Kresovich S., Matsuoka Y., Doebley J. Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc Natl Acad Sci U S A. 2002 Jul 8;99(15):9650–9655. doi: 10.1073/pnas.112324299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wakeley J., Aliacar N. Gene genealogies in a metapopulation. Genetics. 2001 Oct;159(2):893–905. doi: 10.1093/genetics/159.2.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wakeley J. The variance of pairwise nucleotide differences in two populations with migration. Theor Popul Biol. 1996 Feb;49(1):39–57. doi: 10.1006/tpbi.1996.0002. [DOI] [PubMed] [Google Scholar]
  39. Wang R. L., Stec A., Hey J., Lukens L., Doebley J. The limits of selection during maize domestication. Nature. 1999 Mar 18;398(6724):236–239. doi: 10.1038/18435. [DOI] [PubMed] [Google Scholar]
  40. Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
  41. White S. E., Doebley J. F. The molecular evolution of terminal ear1, a regulatory gene in the genus Zea. Genetics. 1999 Nov;153(3):1455–1462. doi: 10.1093/genetics/153.3.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wright Stephen I., Lauga Beatrice, Charlesworth Deborah. Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol Ecol. 2003 May;12(5):1247–1263. doi: 10.1046/j.1365-294x.2003.01743.x. [DOI] [PubMed] [Google Scholar]

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