Journal of Zhejiang University SCIENCE B

, Volume 13, Issue 6, pp 438–451 | Cite as

Population structure and linkage disequilibrium in elite barley breeding germplasm from the United States

Article

Abstract

Cultivated barley is known to have a complex population structure and extensive linkage disequilibrium (LD). To conduct robust association mapping (AM) studies of economically important traits in US barley breeding germplasm, population structure and LD decay were examined in a complete panel of US barley breeding germplasm (3 840 lines) genotyped with 3 072 single nucleotide polymorphisms (SNPs). Nine subpopulations (sp1–sp9) were identified by the program STRUCTURE and subsequently confirmed by principle component analysis (PCA). Out of the nine subpopulations, seven were very similar to the respective subpopulations identified by Hamblin et al. (2010) which were based on half of the germplasm and half of the SNP markers, but two subpopulations were found to be new. One subpopulation was dominated by six-rowed spring lines from Utah State University (UT) and the other was composed of six-rowed spring lines from multiple breeding programs (USDA-ARS Aberdeen (AB), Busch Agricultural Resources Inc. (BA), UT, and Washington State University (WA)). LD was found to decay across a range from 4.0 to 19.8 cM. This result indicates that the germplasm genotyped with 3 072 SNPs would be robust for mapping and possibly identifying the causal polymorphisms contributing to disease resistance and perhaps other traits.

Key words

Association mapping (AM) Structure Linkage disequilibrium (LD) 

CLC number

Q344+.4 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Atwell, S., Huang, Y.S., Vilhjálmsson, B.J., Willems, G., Horton, M., Li, Y., Meng, D., Platt, A., Tarone, A.M., Hu, T.T., 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature, 465(7298):627–631. [doi:10.1038/nature08800]PubMedCrossRefGoogle Scholar
  2. Barrett, J.C., Fry, B., Maller, J., Daly, M.J., 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics, 21(2):263–265. [doi:10.1093/bioinformatics/ bth457]PubMedCrossRefGoogle Scholar
  3. Bhangale, T.R., Rieder, M.J., Nickerson, D.A., 2008. Estimating coverage and power for genetic association studies using near-complete variation data. Nat. Genet., 40(7):841–843. [doi:10.1038/ng.180]PubMedCrossRefGoogle Scholar
  4. Boyko, A.R., Boyko, R.H., Boyko, C.M., Parker, H.G., Castelhano, M., Corey, L., Degenhardt, J.D., Auton, A., Hedimbi, M., Kityo, R., 2009. Complex population structure in African village dogs and its implications for inferring dog domestication history. PNAS, 106(33):13903–13908. [doi:10.1073/pnas.0902129106]PubMedCrossRefGoogle Scholar
  5. Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y., Buckler, E.S., 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics, 23(19):2633–2635. [doi:10.1093/bioinformatics/ btm308]PubMedCrossRefGoogle Scholar
  6. Breseghello, F., Sorrells, M.E., 2006. Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics, 172(2):1165–1177. [doi:10. 1534/genetics.105.044586]PubMedCrossRefGoogle Scholar
  7. Chao, S., Zhang, W., Dubcovsky, J., Sorrells, M., 2007. Evaluation of genetic diversity and genome-wide linkage disequilibrium among US wheat (Triticum aestivum L.) germplasm representing different market classes. Crop Sci., 47(3):1018–1030. [doi:10.2135/cropsci2006.06.0434]CrossRefGoogle Scholar
  8. Cleveland, W.S., 1979. Robust locally weighted regression and smoothing scatterplots. J. Am. Stat. Assoc., 74(368): 829–836. [doi:10.1080/01621459.1979.10481038]Google Scholar
  9. Close, T.J., Bhat, P.R., Lonardi, S., Wu, Y., Rostoks, N., Ramsay, L., Druka, A., Stein, N., Svensson, J.T., Wanamaker, S., et al., 2009. Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics, 10(1):582. [doi:10.1186/1471-2164-10-582]PubMedCrossRefGoogle Scholar
  10. Comadran, J., Thomas, W.T.B., van Eeuwijk, F.A., Ceccarelli, S., Grando, S., Stanca, A.M., Pecchioni, N., Akar, T., Al-Yassin, A., Benbelkacem, A., 2009. Patterns of genetic diversity and linkage disequilibrium in a highly structured Hordeum vulgare association-mapping population for the Mediterranean basin. Theor. Appl. Genet., 119(1):175–187. [doi:10.1007/s00122-009-1027-0]PubMedCrossRefGoogle Scholar
  11. Condón, F., Gustus, C., Rasmusson, D.C., Smith, K.P., 2008. Effect of advanced cycle breeding on genetic diversity in barley breeding germplasm. Crop Sci., 48(3):1027–1036. [doi:10.2135/cropsci2007.07.0415]CrossRefGoogle Scholar
  12. Cornuet, J.M., Luikart, G., 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144(4): 2001–2014.PubMedGoogle Scholar
  13. D’Hoop, B.B., Paulo, M.J., Mank, R.A., van Eck, H.J., van Eeuwijk, F.A., 2008. Association mapping of quality traits in potato (Solanum tuberosum L.). Euphytica, 161(1–2):47–60. [doi:10.1007/s10681-007-9565-5]CrossRefGoogle Scholar
  14. Dragalin, V., Fedorov, V., Patterson, S., Jones, B., 2003. Kullback-Leibler divergence for evaluating bioequivalence. Stat. Med., 22(6):913–930. [doi:10.1002/sim.1451]PubMedCrossRefGoogle Scholar
  15. Ewens, W.J., Spielman, R.S., 1995. The transmission/ disequilibrium test: history, subdivision, and admixture. Am. J. Hum. Genet., 57(2):455–464.PubMedGoogle Scholar
  16. Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data linked loci and correlated allele frequencies. Genetics, 164(4):1567–1587.PubMedGoogle Scholar
  17. Fan, J.B., Oliphant, A., Shen, R., Kermani, B.G., Garcia, F., Gunderson, K.L., Hansen, M., Steemers, F., Butler, S.L., Deloukas, P., et al., 2003. Highly parallel SNP genotyping. Cold Spring Harb. Symp. Quant. Biol., 68:69–78. [doi:10.1101/sqb.2003.68.69]PubMedCrossRefGoogle Scholar
  18. Flint-Garcia, S.A., Thornsberry, J.M., 2003. Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol., 54(1):357–374. [doi:10.1146/annurev.arplant.54.031902.134907]PubMedCrossRefGoogle Scholar
  19. Frazer, K.A., Ballinger, D.G., Cox, D.R., Hinds, D.A., Stuve, L.L., Gibbs, R.A., Belmont, J.W., Boudreau, A., Hardenbol, P., Leal, S.M., 2007. A second generation human haplotype map of over 3.1 million SNPs. Nature, 449(7164):851–861. [doi:10.1038/nature06258]PubMedCrossRefGoogle Scholar
  20. González-Martínez, S.C., Wheeler, N.C., Ersoz, E., Nelson, C.D., Neale, D.B., 2007. Association genetics in Pinus taeda L. I. Wood property traits. Genetics, 175(1): 399–409. [doi:10.1534/genetics.106.061127]PubMedCrossRefGoogle Scholar
  21. Gunderson, K.L., Kruglyak, S., Graige, M.S., Garcia, F., Kermani, B.G., Zhao, C., Che, D., Dickinson, T., Wickham, E., Bierle, J., 2004. Decoding randomly ordered DNA arrays. Genome Res., 14(5):870–877. [doi:10.1101/ gr.2255804]PubMedCrossRefGoogle Scholar
  22. Haldane, J.B.S., 1919. The combination of linkage values and the calculation of distances between the loci of linked factors. J. Genet., 8(29):309–320.Google Scholar
  23. Hamblin, M.T., Close, T.J., Bhat, P.R., Chao, S., Kling, J.G., Abraham, K.J., Blake, T., Brooks, W.S., Cooper, B., Griffey, C.A., et al., 2010. Population structure and linkage disequilibrium in US barley germplasm: implications for association mapping. Crop Sci., 50(2):556–566. [doi:10.2135/cropsci2009.04.0198]CrossRefGoogle Scholar
  24. Horsley, R.D., Schwarz, P.B., Hammond, J.J., 1995. Genetic diversity in malt quality of North American six-rowed spring barley. Crop Sci., 35(1):113–118. [doi:10.2135/ cropsci1995.0011183X003500010021x]CrossRefGoogle Scholar
  25. Hyten, D.L., Choi, I.Y., Song, Q., Shoemaker, R.C., Nelson, R.L., Costa, J.M., Specht, J.E., Cregan, P.B., 2007. Highly variable patterns of linkage disequilibrium in multiple soybean populations. Genetics, 175(4):1937–1944. [doi:10.1534/genetics.106.069740]PubMedCrossRefGoogle Scholar
  26. Jannink, J.L., Walsh, B., 2002. Association Mapping in Plant Populations. In: Kang, M.S. (Ed.), Quantitative Genetics Genomics and Plant Breeding. CAB International, Wallingford, UK, p.59–68.Google Scholar
  27. Jolliffe, I., 2002. Principal Component Analysis. Springer-Verlag, New York, NY.Google Scholar
  28. Kang, H.M., Sul, J.H., 2010. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet., 42(4):348–354. [doi:10.1038/ng.548]PubMedCrossRefGoogle Scholar
  29. Kang, H.M., Zaitlen, N.A., Wade, C.M., Kirby, A., Heckerman, D., Daly, M.J., Eskin, E., 2008. Efficient control of population structure in model organism association mapping. Genetics, 178(3):1709–1723. [doi:10.1534/ genetics.107.080101]PubMedCrossRefGoogle Scholar
  30. Ku, C.S., Loy, E.Y., Pawitan, Y., Chia, K.S., 2010. The pursuit of genome-wide association studies: where are we now? J. Hum. Genet., 55(4):195–206. [doi:10.1038/jhg.2010.19]PubMedCrossRefGoogle Scholar
  31. Malysheva-Otto, L.V., Ganal, M.W., Roder, M.S., 2006. Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genet., 7(1):6–18. [doi:10.1186/1471-2156-7-6]PubMedCrossRefGoogle Scholar
  32. Mangin, B., Siberchicot, A., Nicolas, S., Doligez, A., This, P., Cierco-Ayrolles, C., 2012. Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity, 108(3):285–291. [doi:10.1038/hdy.2011.73]PubMedCrossRefGoogle Scholar
  33. Martin, J.M., 1991. Diversity among North American spring barley cultivars based on coefficients of parentage. Crop Sci., 31(5):1131–1137. [doi:10.2135/cropsci1991.00111 83X003100050009x]CrossRefGoogle Scholar
  34. Massman, J., Cooper, B., Horsley, R., Neate, S., Dill-Macky, R., Chao, S., Dong, Y., Schwarz, P., Muehlbauer, G.J., Smith, K.P., 2011. Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol. Breed., 27(4):439–454. [doi:10. 1007/s11032-010-9442-0]CrossRefGoogle Scholar
  35. McVean, G., 2009. A genealogical interpretation of principal components analysis. PLoS Genet., 5(10):e1000686. [doi:10.1371/journal.pgen.1000686]PubMedCrossRefGoogle Scholar
  36. Metzker, M.L., 2009. Sequencing technologies—the next generation. Nat. Rev. Genet., 11(1):31–46. [doi:10.1038/ nrg2626]PubMedCrossRefGoogle Scholar
  37. Mezmouk, S., Dubreuil, P., Bosio, M., Décousset, L., Charcosset, A., Praud, S., Mangin, B., 2011. Effect of population structure corrections on the results of association mapping tests in complex maize diversity panels. Theor. Appl. Genet., 122(6):1149–1160. [doi:10.1007/s00122-010-1519-y]PubMedCrossRefGoogle Scholar
  38. Mikel, M.A., Kolb, F.L., 2008. Genetic diversity of contemporary North American barley. Crop Sci., 48(4): 1399–1407. [doi:10.2135/cropsci2008.01.0029]CrossRefGoogle Scholar
  39. Nordborg, M., Borevitz, J.O., Bergelson, J., Berry, C.C., Chory, J., Hagenblad, J., Kreitman, M., Maloof, J.N., Noyes, T., Oefner, P.J., 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet., 30(2): 190–193. [doi:10.1038/ng813]PubMedCrossRefGoogle Scholar
  40. Palaisa, K., Morgante, M., Tingey, S., Rafalski, A., 2004. Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. PNAS, 101(26):9885–9890. [doi:10.1073/pnas.0307839101]PubMedCrossRefGoogle Scholar
  41. Pallotta, M.A., Asayama, S., Reinheimer, J.M., Davies, P.A., Barr, A.R., Jefferies, S.P., Chalmers, K.J., Lewis, J., Collins, H.M., Roumeliotis, S., et al., 2003. Mapping and QTL analysis of the barley population Amagi Nijo× WI2585. Aust. J. Agric. Res., 54(12):1141–1144. [doi:10. 1071/AR02218]CrossRefGoogle Scholar
  42. Patterson, N., Price, A.L., Reich, D., 2006. Population structure and eigenanalysis. PLoS Genet., 2(12):e190. [doi:10. 1371/journal.pgen.0020190]PubMedCrossRefGoogle Scholar
  43. Pritchard, J.K., Rosenberg, N.A., 1999. Use of unlinked genetic markers to detect population stratification in association studies. Am. J. Hum. Genet., 65(1):220–228. [doi:10.1086/302449]PubMedCrossRefGoogle Scholar
  44. Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2):945.PubMedGoogle Scholar
  45. Rafalski, A., 2002. Applications of single nucleotide polymorphisms in crop genetics. Curr. Opin. Plant Biol., 5(2): 94–100. [doi:10.1016/S1369-5266(02)00240-6]PubMedCrossRefGoogle Scholar
  46. Remington, D.L., Thornsberry, J.M., Matsuoka, Y., Wilson, L.M., Whitt, S.R., Doebley, J., Kresovich, S., Goodman, M.M., Buckler IV, E.S., 2001. Structure of linkage disequilibrium and phenotypic associations in the maize genome. PNAS, 98(20):11479–11484. [doi:10.1073/pnas.201394398]PubMedCrossRefGoogle Scholar
  47. Risch, N., Merikangas, K., 1996. The future of genetic studies of complex human diseases. Science, 273(5281): 1516–1517. [doi:10.1126/science.273.5281.1516]PubMedCrossRefGoogle Scholar
  48. Rostoks, N., Ramsay, L., MacKenzie, K., Cardle, L., Bhat, P.R., Roose, M.L., Svensson, J.T., Stein, N., Varshney, R.K., Marshall, D.F., 2006. Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. PNAS, 103(49): 18656–18661. [doi:10.1073/pnas.0606133103]PubMedCrossRefGoogle Scholar
  49. Saisho, D., Purugganan, M.D., 2007. Molecular phylogeography of domesticated barley traces expansion of agriculture in the old world. Genetics, 177(3):1765–1776. [doi:10.1534/genetics.107.079491]PubMedCrossRefGoogle Scholar
  50. Skøt, L., Humphreys, J., Humphreys, M.O., Thorogood, D., Gallagher, J., Sanderson, R., Armstead, I.P., Thomas, I.D., 2007. Association of candidate genes with flowering time and water-soluble carbohydrate content in Lolium perenne (L.). Genetics, 177(1):535–547. [doi:10.1534/ genetics.107.071522]PubMedCrossRefGoogle Scholar
  51. Song, B.H., Windsor, A.J., Schmid, K.J., Ramos-Onsins, S., Schranz, M.E., Heidel, A.J., Mitchell-Olds, T., 2009. Multilocus patterns of nucleotide diversity, population structure and linkage disequilibrium in Boechera stricta, a wild relative of Arabidopsis. Genetics, 181(3): 1021–1033. [doi:10.1534/genetics.108.095364]PubMedCrossRefGoogle Scholar
  52. Thornsberry, J.M., Goodman, M.M., Doebley, J., Kresovich, S., Nielsen, D., Buckler, E.S., 2001. Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet., 28(3):286–289. [doi:10.1038/90135]PubMedCrossRefGoogle Scholar
  53. Watterson, G.A., Guess, H.A., 1977. Is the most frequent allele the oldest? Theor. Popul. Biol., 11(2):141–160. [doi:10. 1016/0040-5809(77)90023-5]PubMedCrossRefGoogle Scholar
  54. Wei, X., Jackson, P.A., McIntyre, C.L., Aitken, K.S., Croft, B., 2006. Associations between DNA markers and resistance to diseases in sugarcane and effects of population substructure. Theor. Appl. Genet., 114(1):155–164. [doi:10. 1007/s00122-006-0418-8]PubMedCrossRefGoogle Scholar
  55. Wilson, L.M., Whitt, S.R., Ibáñez, A.M., Rocheford, T.R., Goodman, M.M., Buckler, E.S., 2004. Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell, 16(10):2719–2733. [doi:10.1105/tpc.104.025700]PubMedCrossRefGoogle Scholar
  56. Würschum, T., Maurer, H.P., Kraft, T., Janssen, G., Nilsson, C., Reif, J.C., 2011. Genome-wide association mapping of agronomic traits in sugar beet. Theor. Appl. Genet., 2(2):1–11.Google Scholar
  57. Wych, R.D., Rasmusson, D.C., 1983. Genetic improvement in malting barley cultivars since 1920. Crop Sci., 23(6): 1037–1040. [doi:10.2135/cropsci1983.0011183X0023000 60004x]CrossRefGoogle Scholar
  58. Yu, J., Pressoir, G., Briggs, W.H., Bi, I.V., Yamasaki, M., Doebley, J.F., McMullen, M.D., Gaut, B.S., Nielsen, D.M., Holland, J.B., 2005. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet., 38(2):203–208. [doi:10.1038/ng1702]PubMedCrossRefGoogle Scholar
  59. Zhang, Z., Ersoz, E., Lai, C.Q., Todhunter, R.J., Tiwari, H.K., Gore, M.A., Bradbury, P.J., Yu, J., Arnett, D.K., Ordovas, J.M., 2010. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet., 42(4): 355–360. [doi:10.1038/ng.546]PubMedCrossRefGoogle Scholar
  60. Zhou, H., 2011. Association Mapping of Multiple Disease Resistance in US Barley Breeding Germplasm. PhD Thesis, University of Minnesota, St. Paul, USA.Google Scholar
  61. Zhu, C.G., Buckler, M., Yu, E.S., 2008. Status and prospects of association mapping in plants. Plant Genome, 1(1):5–20. [doi:10.3835/plantgenome2008.02.0089]CrossRefGoogle Scholar

Copyright information

© Zhejiang University and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Plant PathologyUniversity of MinnesotaSt. PaulUSA
  2. 2.Department of Agronomy and Plant GeneticsUniversity of MinnesotaSt. PaulUSA

Personalised recommendations