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Whole-Genome Resequencing Analysis of Hanwoo and Yanbian Cattle to Identify Genome-Wide SNPs and Signatures of Selection

  • Choi, Jung-Woo (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Choi, Bong-Hwan (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Lee, Seung-Hwan (Division of Animal and Dairy Science, Chung Nam National University) ;
  • Lee, Seung-Soo (Animal Genetic and Breeding Division, National Institute of Animal Science) ;
  • Kim, Hyeong-Cheol (Hanwoo Experiment Station, National Institute of Animal Science, RDA) ;
  • Yu, Dayeong (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Chung, Won-Hyong (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Lee, Kyung-Tai (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Chai, Han-Ha (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Cho, Yong-Min (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration) ;
  • Lim, Dajeong (Animal Genomics and Bioinformatics Division, National Institute of Animal Science, Rural Development Administration)
  • Received : 2015.01.27
  • Accepted : 2015.03.13
  • Published : 2015.05.31

Abstract

Over the last 30 years, Hanwoo has been selectively bred to improve economically important traits. Hanwoo is currently the representative Korean native beef cattle breed, and it is believed that it shared an ancestor with a Chinese breed, Yanbian cattle, until the last century. However, these two breeds have experienced different selection pressures during recent decades. Here, we whole-genome sequenced 10 animals each of Hanwoo and Yanbian cattle (20 total) using the Illumina HiSeq 2000 sequencer. A total of approximately 3.12 and 3.07 billion sequence reads were mapped to the bovine reference sequence assembly (UMD 3.1) at an average of approximately 10.71- and 10.53-fold coverage for Hanwoo and Yanbian cattle, respectively. A total of 17,936,399 single nucleotide polymorphisms (SNPs) were yielded, of which 22.3% were found to be novel. By annotating the SNPs, we further retrieved numerous nonsynonymous SNPs that may be associated with traits of interest in cattle. Furthermore, we performed whole-genome screening to detect signatures of selection throughout the genome. We located several promising selective sweeps that are potentially responsible for economically important traits in cattle; the PPP1R12A gene is an example of a gene that potentially affects intramuscular fat content. These discoveries provide valuable genomic information regarding potential genomic markers that could predict traits of interest for breeding programs of these cattle breeds.

Keywords

References

  1. Cheng, P. (1984). Livestock breeds of China. FAO Animal Production and Health Paper 46.
  2. Choi, J.W., Chung, W.H., Lee, K.T., Lee, J.W., Jung, K.S., Cho, Y., Kim, N., and Kim, T.H. (2013a). Whole genome resequencing of Heugu (Korean Black Cattle) for the genome-wide SNP discovery. Korean J. Food Sci. An. 33, 715-722. https://doi.org/10.5851/kosfa.2013.33.6.715
  3. Choi, J.W., Liao, X., Park, S., Jeon, H.J., Chung, W.H., Stothard, P., Park, Y.S., Lee, J.K., Lee, K.T., Kim, S.H., et al. (2013b). Massively parallel sequencing of Chikso (Korean brindle cattle) to discover genome-wide SNPs and InDels. Mol. Cells 36, 203-211. https://doi.org/10.1007/s10059-013-2347-0
  4. Choi, J.W., Liao, X., Stothard, P., Chung, W.H., Jeon, H.J., Miller, S.P., Choi, S.Y., Lee, J.K., Yang, B., Lee, K.T., et al. (2014). Whole-genome analyses of Korean native and Holstein cattle breeds by massively parallel sequencing. PLoS One 9, e101127. https://doi.org/10.1371/journal.pone.0101127
  5. Cingolani, P., Platts, A., Wang le, L., Coon, M., Nguyen, T., Wang, L., Land, S.J., Lu, X. and Ruden, D.M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80-92. https://doi.org/10.4161/fly.19695
  6. Dadi, H., Lee, S.H., Lee, S.S., Park, C., and Kim, K.S. (2014). Interand intra-population genetic divergence of East Asian cattle populations: focusing on Korean cattle. Genes Genom. 36, 261-265. https://doi.org/10.1007/s13258-013-0146-9
  7. Daetwyler, H.D., Capitan, A., Pausch, H., Stothard, P., van Binsbergen, R., Brondum, R.F., Liao, X., Djari, A., Rodriguez, S.C., Grohs, C., et al. (2014). Whole-genome sequencing of 234 bulls facilitates mapping of monogenic and complex traits in cattle. Nat. Genet. 46, 858-865. https://doi.org/10.1038/ng.3034
  8. Eck, S.H., Benet-Pages, A., Flisikowski, K., Meitinger, T., Fries, R., and Strom, T.M. (2009). Whole genome sequencing of a single Bos taurus animal for single nucleotide polymorphism discovery. Genome Biol. 10, R82. https://doi.org/10.1186/gb-2009-10-8-r82
  9. Elsik, C.G., Tellam, R.L., Worley, K.C., Gibbs, R.A., Muzny, D.M., Weinstock, G.M., Adelson, D.L., Eichler, E.E., et al. (2009). The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324, 522-528. https://doi.org/10.1126/science.1169588
  10. Food and Agriculture Organization (FAO). (2014). Domestic Animal Diversity Information Service (DAD-IS). http://dad.fao.org/, Accessed September 5, 2014.
  11. Fujimoto, A., Nakagawa, H., Hosono, N., Nakano, K., Abe, T., Boroevich, K.A., Nagasaki, M., Yamaguchi, R., Shibuya, T., Kubo, M., et al. (2010). Whole-genome sequencing and comprehensive variant analysis of a Japanese individual using massively parallel sequencing. Nat. Genet. 42, 931-936. https://doi.org/10.1038/ng.691
  12. Hu, Z.L., Park, C.A., Wu, X.L., and Reecy, J.M. (2013). Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic Acids Res. 41, D871-879. https://doi.org/10.1093/nar/gks1150
  13. Huang da, W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57. https://doi.org/10.1038/nprot.2008.211
  14. Ito, M., Nakano, T., Erdodi, F., and Hartshorne, D.J. (2004). Myosin phosphatase: structure, regulation and function. Mol. Cell. Biochem. 259, 197-209. https://doi.org/10.1023/B:MCBI.0000021373.14288.00
  15. Kawahara-Miki, R., Tsuda, K., Shiwa, Y., Arai-Kichise, Y., Matsumoto, T., Kanesaki, Y., Oda, S., Ebihara, S., Yajima, S., Yoshikawa, H., et al. (2011). Whole-genome resequencing shows numerous genes with nonsynonymous SNPs in the Japanese native cattle Kuchinoshima-Ushi. BMC Genomics 12, 103. https://doi.org/10.1186/1471-2164-12-103
  16. Kim, B.J., Kim, Y.H., Cho, W.H., Bok, K.K., Kim, B.J., and Kang, C.M. (1981). Yanbian Cattle. Yanbian People Publishing House, 1-5.
  17. Kozova, M., Kalac, P., and Pelikanova, T. (2009). Changes in the content of biologically active polyamines during beef loin storage and cooking. Meat Sci. 81, 607-611. https://doi.org/10.1016/j.meatsci.2008.10.018
  18. Lee, K.T., Chung, W.H., Lee, S.Y., Choi, J.W., Kim, J., Lim, D., Lee, S., Jang, G.W., Kim, B., Choy, Y.H., et al. (2013). Wholegenome resequencing of Hanwoo (Korean cattle) and insight into regions of homozygosity. BMC Genomics 14, 519. https://doi.org/10.1186/1471-2164-14-519
  19. Lee, S.H., Park, B.H., Sharma, A., Dang, C.G., Lee, S.S., Choi, T.J., Choy, Y.H., Kim, H.C., Jeon, K.J., Kim, S.D., et al. (2014). Hanwoo cattle: origin, domestication, breeding strategies and genomic selection. J. Anim. Sci. Technol. 56.
  20. Li, H., and Durbin, R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595. https://doi.org/10.1093/bioinformatics/btp698
  21. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., and Genome Project Data Processing, S. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
  22. Liu, M., Nauta, A., Francke, C., and Siezen, R.J. (2008). Comparative genomics of enzymes in flavor-forming pathways from amino acids in lactic acid bacteria. Appl. Environ. Microbiol. 74, 4590-4600. https://doi.org/10.1128/AEM.00150-08
  23. Liu, Y., Qin, X., Song, X.Z., Jiang, H., Shen, Y., Durbin, K.J., Lien, S., Kent, M.P., Sodeland, M., Ren, Y., et al. (2009). Bos taurus genome assembly. BMC Genomics 10, 180. https://doi.org/10.1186/1471-2164-10-180
  24. Lu, D., Miller, S., Sargolzaei, M., Kelly, M., Vander Voort, G., Caldwell, T., Wang, Z., Plastow, G., and Moore, S. (2013). Genome-wide association analyses for growth and feed efficiency traits in beef cattle. J. Anim. Sci. 91, 3612-3633. https://doi.org/10.2527/jas.2012-5716
  25. Matsumura, F., and Hartshorne, D.J. (2008). Myosin phosphatase target subunit: Many roles in cell function. Biochem. Biophys. Res. Commun. 369, 149-156. https://doi.org/10.1016/j.bbrc.2007.12.090
  26. McClure, M.C., Morsci, N.S., Schnabel, R.D., Kim, J.W., Yao, P., Rolf, M.M., McKay, S.D., Gregg, S.J., Chapple, R.H., Northcutt, S.L., et al. (2010). A genome scan for quantitative trait loci influencing carcass, post-natal growth and reproductive traits in commercial Angus cattle. Anim. Genet. 41, 597-607. https://doi.org/10.1111/j.1365-2052.2010.02063.x
  27. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010). The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303. https://doi.org/10.1101/gr.107524.110
  28. Merico, D., Isserlin, R., Stueker, O., Emili, A., and Bader, G.D. (2010). Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 5, e13984. https://doi.org/10.1371/journal.pone.0013984
  29. Mishra, C., Palai, T.K., Sarangi, L.N., Prusty, B.R. and Maharana, B.R. (2013). Candidate gene markers for sperm quality and fertility in bulls. Veterinary World 6, 905-910. https://doi.org/10.14202/vetworld.2013.905-910
  30. Nalaila, S.M., Stothard, P., Moore, S.S., Li, C., and Wang, Z. (2012). Whole-genome QTL scan for ultrasound and carcass merit traits in beef cattle using Bayesian shrinkage method. J. Anim. Breed. Genet. 129, 107-119. https://doi.org/10.1111/j.1439-0388.2011.00954.x
  31. Norman, H., Powell, R., Wright, J., and Sattler, C. (2003). Timeliness and effectiveness of progeny testing through artificial insemination. J. Dairy Sci. 86, 1513-1525. https://doi.org/10.3168/jds.S0022-0302(03)73737-0
  32. Ostermeier, G.C., Sargeant, G.A., Yandell, B.S., Evenson, D.P., and Parrish, J.J. (2001). Relationship of bull fertility to sperm nuclear shape. J. Androl. 22, 595-603.
  33. Peters, S.O., Kizilkaya, K., Garrick, D.J., Fernando, R.L., Reecy, J.M., Weaber, R.L., Silver, G.A., and Thomas, M.G. (2012). Bayesian genome-wide association analysis of growth and yearling ultrasound measures of carcass traits in Brangus heifers. J. Anim. Sci. 90, 3398-3409. https://doi.org/10.2527/jas.2011-4507
  34. Qanbari, S., Pausch, H., Jansen, S., Somel, M., Strom, T.M., Fries, R., Nielsen, R., and Simianer, H. (2014). Classic selective sweeps revealed by massive sequencing in cattle. PLoS Genet. 10, e1004148. https://doi.org/10.1371/journal.pgen.1004148
  35. Quang, N., and Zarkadas, C.G. (1989). Comparison of the amino acid composition and connective tissue protein contents of selected bovine skeletal muscles. J. Agric. Food Chem. 37, 1279-1286. https://doi.org/10.1021/jf00089a017
  36. Rubin, C.J., Zody, M.C., Eriksson, J., Meadows, J.R., Sherwood, E., Webster, M.T., Jiang, L., Ingman, M., Sharpe, T., Ka, S., et al. (2010). Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464, 587-591. https://doi.org/10.1038/nature08832
  37. Rubin, C.J., Megens, H.J., Martinez Barrio, A., Maqbool, K., Sayyab, S., Schwochow, D., Wang, C., Carlborg, O., Jern, P., Jorgensen, C.B., et al. (2012). Strong signatures of selection in the domestic pig genome. Proc. Nati. Acad. Sci. USA 109, 19529-19536. https://doi.org/10.1073/pnas.1217149109
  38. Stothard, P., Choi, J.W., Basu, U., Sumner-Thomson, J.M., Meng, Y., Liao, X., and Moore, S.S. (2011). Whole genome resequencing of black Angus and Holstein cattle for SNP and CNV discovery. BMC Genomics 12, 559. https://doi.org/10.1186/1471-2164-12-559
  39. Sun, W.X., Wang, H.H., Jiang, B.C., Zhao, Y.Y., Xie, Z.R., Xiong, K., and Chen, J. (2013). Global comparison of gene expression between subcutaneous and intramuscular adipose tissue of mature Erhualian pig. Genet. Mol. Res. 12, 5085-5101. https://doi.org/10.4238/2013.October.29.3
  40. Utsunomiya, Y.T., O'Brien, A.M.P., Sonstegard, T.S., Van Tassell, C.P., do Carmo, A.S., Meszaros, G., Soelkner, J., and Garcia, J.F. (2013). Detecting loci under recent positive selection in dairy and beef cattle by combining different genome-wide scan methods. PLoS One 8, e64280. https://doi.org/10.1371/journal.pone.0064280
  41. Wasseriwan, A. (1979) Symposium on meat flavor chemial basis for meat flavor:A Review. J. Food Sci. 44, 6-11. https://doi.org/10.1111/j.1365-2621.1979.tb09993.x
  42. Zhang, X., Ma, D., Caruso, M., Lewis, M., Qi, Y., and Yi, Z. (2014). Quantitative phosphoproteomics reveals novel phosphorylation events in insulin signaling regulated by protein phosphatase 1 regulatory subunit 12A. J. Proteomics 109, 63-75. https://doi.org/10.1016/j.jprot.2014.06.010
  43. Zimin, A.V., Delcher, A.L., Florea, L., Kelley, D.R., Schatz, M.C., Puiu, D., Hanrahan, F., Pertea, G., Van Tassell, C.P., Sonstegard, T.S., et al. (2009). A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 10, R42. https://doi.org/10.1186/gb-2009-10-4-r42

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