Skip to main content
Log in

Genome-wide copy number variation in Hanwoo, Black Angus, and Holstein cattle

  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

Hanwoo, Korean native cattle, is indigenous to the Korean peninsula. They have been used mainly as draft animals for about 5,000 years; however, in the last 30 years, their main role has been changed to meat production by selective breeding which has led to substantial increases in their productivity. Massively parallel sequencing technology has recently made possible the systematic identification of structural variations in cattle genomes. In particular, copy number variation (CNV) has been recognized as an important genetic variation complementary to single-nucleotide polymorphisms that can be used to account for variations of economically important traits in cattle. Here we report genome-wide copy number variation regions (CNVRs) in Hanwoo cattle obtained by comparing the whole genome sequence of Hanwoo with Black Angus and Holstein sequence datasets. We identified 1,173 and 963 putative CNVRs representing 16.7 and 7.8 Mbp from comparisons between Black Angus and Hanwoo and between Holstein and Hanwoo, respectively. The potential functional roles of the CNVRs were assessed by Gene Ontology enrichment analysis. The results showed that response to stimulus, immune system process, and cellular component organization were highly enriched in the genic-CNVRs that overlapped with annotated cattle genes. Of the 11 CNVRs that were selected for validation by quantitative real-time PCR, 9 exhibited the expected copy number differences. The results reported in this study show that genome-wide CNVs were detected successfully using massively parallel sequencing technology. The CNVs may be a valuable resource for further studies to correlate CNVs and economically important traits in cattle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alkan C, Coe BP, Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12:363–376

    Article  PubMed  CAS  Google Scholar 

  • Bae JS, Cheong HS, Kim LH, NamGung S, Park TJ, Chun JY, Kim JY, Pasaje CF, Lee JS, Shin HD (2010) Identification of copy number variations and common deletion polymorphisms in cattle. BMC Genomics 11:232

    Article  PubMed  Google Scholar 

  • Barendse W, Harrison BE, Bunch RJ, Thomas MB, Turner LB (2009) Genome wide signatures of positive selection: the comparison of independent samples and the identification of regions associated to traits. BMC Genomics 10:178

    Article  PubMed  Google Scholar 

  • Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, Fitzgerald T, Hu M, Ihm CH, Kristiansson K, Macarthur DG, Macdonald JR, Onyiah I, Pang AW, Robson S, Stirrups K, Valsesia A, Walter K, Wei J, Tyler-Smith C, Carter NP, Lee C, Scherer SW, Hurles ME (2010) Origins and functional impact of copy number variation in the human genome. Nature 464:704–712

    Article  PubMed  CAS  Google Scholar 

  • Coppage KH, Sun X, Baker RS, Clark KE (2005) Expression of phosphodiesterase 5 in maternal and fetal sheep. Am J Obstet Gynecol 193:1005–1010

    Article  PubMed  CAS  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–70

    Article  PubMed  CAS  Google Scholar 

  • Eck SH, Benet-Pages A, Flisikowski K, Meitinger T, Fries R, Strom TM (2009) Whole genome sequencing of a single Bos taurus animal for single nucleotide polymorphism discovery. Genome Biol 10:R82

    Article  PubMed  Google Scholar 

  • Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, Elnitski L, Guigo R, Hamernik DL, Kappes SM, Lewin HA, Lynn DJ, Nicholas FW, Reymond A, Rijnkels M, Skow LC, Zdobnov EM, Schook L, Womack J, Alioto T, Antonarakis SE, Astashyn A, Chapple CE, Chen HC, Chrast J, Camara F, Ermolaeva O, Henrichsen CN, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Kokocinski F, Landrum M, Maglott D, Pruitt K, Sapojnikov V, Searle SM, Solovyev V, Souvorov A, Ucla C, Wyss C, Anzola JM, Gerlach D, Elhaik E, Graur D, Reese JT, Edgar RC, McEwan JC, Payne GM, Raison JM, Junier T, Kriventseva EV, Eyras E, Plass M, Donthu R, Larkin DM, Reecy J, Yang MQ, Chen L, Cheng Z, Chitko-McKown CG, Liu GE, Matukumalli LK, Song J, Zhu B, Bradley DG, Brinkman FS, Lau LP, Whiteside MD, Walker A, Wheeler TT, Casey T, German JB, Lemay DG, Maqbool NJ, Molenaar AJ, Seo S, Stothard P, Baldwin CL, Baxter R, Brinkmeyer-Langford CL, Brown WC, Childers CP, Connelley T, Ellis SA, Fritz K, Glass EJ, Herzig CT, Iivanainen A, Lahmers KK, Bennett AK, Dickens CM, Gilbert JG, Hagen DE, Salih H, Aerts J, Caetano AR, Dalrymple B, Garcia JF, Gill CA, Hiendleder SG, Memili E, Spurlock D, Williams JL, Alexander L, Brownstein MJ, Guan L, Holt RA, Jones SJ, Marra MA, Moore R, Moore SS, Roberts A, Taniguchi M, Waterman RC, Chacko J, Chandrabose MM, Cree A, Dao MD, Dinh HH, Gabisi RA, Hines S, Hume J, Jhangiani SN, Joshi V, Kovar CL, Lewis LR, Liu YS, Lopez J, Morgan MB, Nguyen NB, Okwuonu GO, Ruiz SJ, Santibanez J, Wright RA, Buhay C, Ding Y, Dugan-Rocha S, Herdandez J, Holder M, Sabo A, Egan A, Goodell J, Wilczek-Boney K, Fowler GR, Hitchens ME, Lozado RJ, Moen C, Steffen D, Warren JT, Zhang J, Chiu R, Schein JE, Durbin KJ, Havlak P, Jiang H, Liu Y, Qin X, Ren Y, Shen Y, Song H, Bell SN, Davis C, Johnson AJ, Lee S, Nazareth LV, Patel BM, Pu LL, Vattathil S, Williams RL Jr, Curry S, Hamilton C, Sodergren E, Wheeler DA, Barris W, Bennett GL, Eggen A, Green RD, Harhay GP, Hobbs M, Jann O, Keele JW, Kent MP, Lien S, McKay SD, McWilliam S, Ratnakumar A, Schnabel RD, Smith T, Snelling WM, Sonstegard TS, Stone RT, Sugimoto Y, Takasuga A, Taylor JF, Van Tassell CP, Macneil MD, Abatepaulo AR, Abbey CA, Ahola V, Almeida IG, Amadio AF, Anatriello E, Bahadue SM, Biase FH, Boldt CR, Carroll JA, Carvalho WA, Cervelatti EP, Chacko E, Chapin JE, Cheng Y, Choi J, Colley AJ, de Campos TA, De Donato M, Santos IK, de Oliveira CJ, Deobald H, Devinoy E, Donohue KE, Dovc P, Eberlein A, Fitzsimmons CJ, Franzin AM, Garcia GR, Genini S, Gladney CJ, Grant JR, Greaser ML, Green JA, Hadsell DL, Hakimov HA, Halgren R, Harrow JL, Hart EA, Hastings N, Hernandez M, Hu ZL, Ingham A, Iso-Touru T, Jamis C, Jensen K, Kapetis D, Kerr T, Khalil SS, Khatib H, Kolbehdari D, Kumar CG, Kumar D, Leach R, Lee JC, Li C, Logan KM, Malinverni R, Marques E, Martin WF, Martins NF, Maruyama SR, Mazza R, McLean KL, Medrano JF, Moreno BT, More DD, Muntean CT, Nandakumar HP, Nogueira MF, Olsaker I, Pant SD, Panzitta F, Pastor RC, Poli MA, Poslusny N, Rachagani S, Ranganathan S, Razpet A, Riggs PK, Rincon G, Rodriguez-Osorio N, Rodriguez-Zas SL, Romero NE, Rosenwald A, Sando L, Schmutz SM, Shen L, Sherman L, Southey BR, Lutzow YS, Sweedler JV, Tammen I, Telugu BP, Urbanski JM, Utsunomiya YT, Verschoor CP, Waardenberg AJ, Wang Z, Ward R, Weikard R, Welsh TH Jr, White SN, Wilming LG, Wunderlich KR, Yang J, Zhao FQ (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522–528

    Article  PubMed  Google Scholar 

  • Fadista J, Thomsen B, Holm LE, Bendixen C (2010) Copy number variation in the bovine genome. BMC Genomics 11:284

    Article  PubMed  Google Scholar 

  • Feuk L, Carson AR, Scherer SW (2006) Structural variation in the human genome. Nat Rev Genet 7:85–97

    Article  PubMed  CAS  Google Scholar 

  • Flicek P, Amode MR, Barrell D, Beal K, Brent S, Chen Y, Clapham P, Coates G, Fairley S, Fitzgerald S, Gordon L, Hendrix M, Hourlier T, Johnson N, Kahari A, Keefe D, Keenan S, Kinsella R, Kokocinski F, Kulesha E, Larsson P, Longden I, McLaren W, Overduin B, Pritchard B, Riat HS, Rios D, Ritchie GR, Ruffier M, Schuster M, Sobral D, Spudich G, Tang YA, Trevanion S, Vandrovcova J, Vilella AJ, White S, Wilder SP, Zadissa A, Zamora J, Aken BL, Birney E, Cunningham F, Dunham I, Durbin R, Fernandez-Suarez XM, Herrero J, Hubbard TJ, Parker A, Proctor G, Vogel J, Searle SM (2011) Ensembl 2011. Nucleic Acids Res 39:D800–806

    Article  PubMed  CAS  Google Scholar 

  • Gibbs RA, Taylor JF, Van Tassell CP, Barendse W, Eversole KA, Gill CA, Green RD, Hamernik DL, Kappes SM, Lien S, Matukumalli LK, McEwan JC, Nazareth LV, Schnabel RD, Weinstock GM, Wheeler DA, Ajmone-Marsan P, Boettcher PJ, Caetano AR, Garcia JF, Hanotte O, Mariani P, Skow LC, Sonstegard TS, Williams JL, Diallo B, Hailemariam L, Martinez ML, Morris CA, Silva LO, Spelman RJ, Mulatu W, Zhao K, Abbey CA, Agaba M, Araujo FR, Bunch RJ, Burton J, Gorni C, Olivier H, Harrison BE, Luff B, Machado MA, Mwakaya J, Plastow G, Sim W, Smith T, Thomas MB, Valentini A, Williams P, Womack J, Woolliams JA, Liu Y, Qin X, Worley KC, Gao C, Jiang H, Moore SS, Ren Y, Song XZ, Bustamante CD, Hernandez RD, Muzny DM, Patil S, San Lucas A, Fu Q, Kent MP, Vega R, Matukumalli A, McWilliam S, Sclep G, Bryc K, Choi J, Gao H, Grefenstette JJ, Murdoch B, Stella A, Villa-Angulo R, Wright M, Aerts J, Jann O, Negrini R, Goddard ME, Hayes BJ, Bradley DG, Barbosa da Silva M, Lau LP, Liu GE, Lynn DJ, Panzitta F, Dodds KG (2009) Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324:528–532

    Article  PubMed  CAS  Google Scholar 

  • Haider S, Ballester B, Smedley D, Zhang J, Rice P, Kasprzyk A (2009) BioMart central portal–unified access to biological data. Nucleic Acids Res 37:W23–27

    Article  PubMed  CAS  Google Scholar 

  • Hayes BJ, Chamberlain AJ, Maceachern S, Savin K, McPartlan H, MacLeod I, Sethuraman L, Goddard ME (2009) A genome map of divergent artificial selection between Bos taurus dairy cattle and Bos taurus beef cattle. Anim Genet 40:176–184

    Article  PubMed  CAS  Google Scholar 

  • Hou Y, Liu GE, Bickhart DM, Cardone MF, Wang K, Kim ES, Matukumalli LK, Ventura M, Song J, VanRaden PM, Sonstegard TS, Van Tassell CP (2011) Genomic characteristics of cattle copy number variations. BMC Genomics 12:127

    Article  PubMed  Google Scholar 

  • Jiang L, Liu J, Sun D, Ma P, Ding X, Yu Y, Zhang Q (2010) Genome wide association studies for milk production traits in Chinese Holstein population. PLoS One 5:e13661

    Article  PubMed  Google Scholar 

  • Kim KH, Lee JH, Lee SC, Park WY, Oh YG, Kang SW, Ko YD (2005) The optimal TDN levels of concentrates and slaughter age in Hanwoo steers. J Anim Sci Technol 47:731–744

    Article  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  Google Scholar 

  • Liu GE, Hou Y, Zhu B, Cardone MF, Jiang L, Cellamare A, Mitra A, Alexander LJ, Coutinho LL, Dell’Aquila ME, Gasbarre LC, Lacalandra G, Li RW, Matukumalli LK, Nonneman D, Regitano LC, Smith TP, Song J, Sonstegard TS, Van Tassell CP, Ventura M, Eichler EE, McDaneld TG, Keele JW (2010) Analysis of copy number variations among diverse cattle breeds. Genome Res 20:693–703

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Qin X, Song XZ, Jiang H, Shen Y, Durbin KJ, Lien S, Kent MP, Sodeland M, Ren Y, Zhang L, Sodergren E, Havlak P, Worley KC, Weinstock GM, Gibbs RA (2009) Bos taurus genome assembly. BMC Genomics 10:180

    Article  PubMed  Google Scholar 

  • Matukumalli LK, Lawley CT, Schnabel RD, Taylor JF, Allan MF, Heaton MP, O’Connell J, Moore SS, Smith TP, Sonstegard TS, Van Tassell CP (2009) Development and characterization of a high density SNP genotyping assay for cattle. PLoS One 4:e5350

    Article  PubMed  Google Scholar 

  • Nguyen DQ, Webber C, Ponting CP (2006) Bias of selection on human copy-number variants. PLoS Genet 2:e20

    Article  PubMed  Google Scholar 

  • NIAS (2011) Annual report for Hanwoo genetic evaluation. In: Annual report for livestock improvement in 2010

  • Pinto D, Marshall C, Feuk L, Scherer SW (2007) Copy-number variation in control population cohorts. Hum Mol Genet 16(2):R168–R173

    Article  PubMed  CAS  Google Scholar 

  • Rudolph MC, McManaman JL, Hunter L, Phang T, Neville MC (2003) Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation, and involution. J Mammary Gland Biol Neoplasia 8:287–307

    Article  PubMed  Google Scholar 

  • Sherman EL, Nkrumah JD, Moore SS (2010) Whole genome single nucleotide polymorphism associations with feed intake and feed efficiency in beef cattle. J Anim Sci 88:16–22

    Article  PubMed  CAS  Google Scholar 

  • Smith SB, Gill CA, Lunt DK, Brooks MA (2009) Regulation of fat and fatty acid composition in beef cattle. Asian Australas J Anim Sci 22:1225–1233

    CAS  Google Scholar 

  • Stothard P, Choi JW, Basu U, Sumner-Thomson JM, Meng Y, Liao X, Moore SS (2011) Whole genome resequencing of black Angus and Holstein cattle for SNP and CNV discovery. BMC Genomics 12:559

    Article  PubMed  CAS  Google Scholar 

  • Xie C, Tammi MT (2009) CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics 10:80

    Article  PubMed  Google Scholar 

  • Zimin AV, Delcher AL, Florea L, Kelley DR, Schatz MC, Puiu D, Hanrahan F, Pertea G, Van Tassell CP, Sonstegard TS, Marcais G, Roberts M, Subramanian P, Yorke JA, Salzberg SL (2009) A whole-genome assembly of the domestic cow Bos taurus. Genome Biol 10:R42

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant (No. PJ007197) from the BioGreen21 program, Rural Development Administration (RDA), Korea, and through University of Alberta program funds provided to Professor Moore. Xiaoping Liao is funded by the Genome Canada project entitled “Whole Genome Selection Through Genome Wide Imputation in Beef Cattle.”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tae-Hun Kim.

Additional information

Jung-Woo Choi and Kyung-Tai Lee contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 179 kb)

Supplementary material 2 (XLSX 92 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Choi, JW., Lee, KT., Liao, X. et al. Genome-wide copy number variation in Hanwoo, Black Angus, and Holstein cattle. Mamm Genome 24, 151–163 (2013). https://doi.org/10.1007/s00335-013-9449-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-013-9449-z

Keywords

Navigation