1932

Abstract

I abandoned my original career choice of high school teaching to pursue dentistry and soon abandoned that path for genetics. The latter decision was due to a challenge by a professor that led to me reading Nobel speeches by pioneer geneticists before I had formal exposure to the subject. Even then, I was 15 years into my career before my interest in rodent genomes gave way to mapping cattle genes. Events behind these twists and turns in my career path comprise the first part of this review. The remainder is a review of the development of the field of bovine genomics from my personal perspective. I have had the pleasure of working with outstanding graduate students, postdocs, and colleagues to contribute my small part to a discipline that has evolved from a few individuals mapping an orphan genome to a discipline underlying a revolution in animal breeding.

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2019-02-15
2024-05-10
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Literature Cited

  1. 1.  Ruddle FH 1984. The William Allan Memorial Award address: reverse genetics and beyond. Am. J. Hum. Genet. 36:944–53
    [Google Scholar]
  2. 2.  Herskowitz IH 1962. Genetics Boston: Little, Brown
  3. 3.  Watson JD, Crick FHC 1953. Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–38
    [Google Scholar]
  4. 4.  Womack JE, Bogart R 1968. Effects of irradiation on selection response in mice. J. Hered. 59:269–74
    [Google Scholar]
  5. 5.  Womack JE, Bogart R 1969. Effects of X-irradiation on size of litters born to female mice radiated at various stages of the estrous cycle. Int. J. Fertil. 14:130–40
    [Google Scholar]
  6. 6.  Malling HV, Valcovic LR 1977. A biochemical specific locus mutation system in mice. Arch. Toxicol. 38:45–51
    [Google Scholar]
  7. 7.  Womack JE 1973. Biochemical genetics of rat esterases: polymorphism, tissue expression and linkage of four loci. Biochem. Genet. 9:13–24
    [Google Scholar]
  8. 8.  Womack JE, Sharp M 1976. Comparative autosomal linkage in mammals: genetics of esterases in Mus musculus and Rattus norvegicus. . Genetics 82:665–75
    [Google Scholar]
  9. 9.  Womack JE 1975. Esterase-6 (Es-6) in laboratory mice: hormone-influenced expression and linkage relationship to oligosyndactylism (Os), esterase-1(Es-1), and esterase-2 (Es-2) in chromosome 8. Biochem. Genet. 13:311–22
    [Google Scholar]
  10. 10.  Womack JE, Hawes NL, Soares ER, Roderick TH 1975. Mitochondrial malate dehydrogenase (Mor-1) in the mouse: linkage to chromosome 5 markers. Biochem. Genet. 13:519–25
    [Google Scholar]
  11. 11.  Eicher EM, Stern RH, Womack JE, Davisson MT, Roderick TH, Reynolds SC 1976. Evolution of mammalian carbonic anhydrase loci by tandem duplication: close linkage of Car-1 and Car-2 to the centromeric region of chromosome 3 in the mouse. Biochem. Genet. 14:651–60
    [Google Scholar]
  12. 12.  Roderick TH, Lalley PA, Davisson MT, O'Brien SJ, Womack JE et al. 1984. Report of the committee on comparative mapping, Human Gene Mapping 7. Cytogenet. Cell Genet. 37:312–39
    [Google Scholar]
  13. 13.  Potier M, Yan DLS, Womack JE 1979. Neuraminidase deficiency in the mouse. FEBS Lett 108:345–48
    [Google Scholar]
  14. 14.  Womack JE, Yan DLS, Potier M 1981. Gene for neuraminidase activity on mouse chromosome 17 near H-2: pleiotropic effects on multiple hydrolases. Science 212:63–65
    [Google Scholar]
  15. 15.  Womack JE, David CS 1982. Mouse gene for neuraminidase activity (Neu-1) maps to the D end of H-2. . Immunogenetics 16:177–80
    [Google Scholar]
  16. 16.  Daniel WL, Womack JE, Henthorn PS 1981. Murine liver arylsulfatase B processing influenced by region on chromosome 17. Biochem. Genet. 19:211–25
    [Google Scholar]
  17. 17.  Nadeau JH, Taylor BA 1984. Lengths of chromosomal segments conserved since divergence of man and mouse. PNAS 81:814–18
    [Google Scholar]
  18. 18.  O'Brien SJ, Nash WG 1982. Genetic mapping in mammals: chromosome map of the domestic cat. Science 216:257–65
    [Google Scholar]
  19. 19.  Shimizu M, Shimizu Y, Woods C, Wegner T 1981. The bovine genes for phosphoglycerate kinase, glucose-6-phosphate dehydrogenase, alpha-galactosidase, and hypoxanthine phosphoribosyltransferase are linked to the X chromosome in cattle-mouse cell hybrids. Cytogenet. Cell Genet. 29:26–31
    [Google Scholar]
  20. 20.  Heuertz S, Hors-Cayla M-C 1981. Cattle gene mapping by somatic cell hybridization: study of 17 enzyme markers. Cytogenet. Cell Genet. 30:137–45
    [Google Scholar]
  21. 21.  Womack JE 1984. A gene map of the cow. Genetic Maps SJ O'Brien New York: Cold Spring Harbor
    [Google Scholar]
  22. 22.  Womack JE, Moll YD 1986. Gene map of the cow: conservation of linkage with mouse and man. J. Hered. 77:2–7
    [Google Scholar]
  23. 23.  Fries R, Eggen A, Womack JE 1993. The bovine gene map. Mamm. Genome 4:405–28
    [Google Scholar]
  24. 24.  Popescu CP, Long S, Riggs P, Womack J, Schmutz S et al. 1996. Standardization of cattle karyotype nomenclature: report of the committee for the standardization of the cattle karyotype. Cytogenet. Cell Genet. 74:259–61
    [Google Scholar]
  25. 25.  Botstein D, White RI, Skolnick M, Davis RW 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am. J. Hum. Genet. 32:314–31
    [Google Scholar]
  26. 26.  Beckman JS, Soller M 1983. Restriction fragment length polymorphism in genetic improvement: methodologies, mapping and costs. Theor. Appl. Genet. 67:35–43
    [Google Scholar]
  27. 27.  Barendse W, Armitage SM, Kossarek LM, Shalom A, Kirkpatrick BW et al. 1994. A genetic linkage map of the bovine genome. Nat. Genet. 6:227–35
    [Google Scholar]
  28. 28.  Barendse W, Vaiman D, Kemp SJ, Sugimoto Y, Armitage SM et al. 1997. A medium-density genetic linkage map of the bovine genome. Mamm. Genome 8:21–28
    [Google Scholar]
  29. 29.  Georges M, Dietz AB, Mishra A, Nielsen D, Sargeant L et al. 1993. Microsatellite mapping of the gene causing weaver disease in cattle will allow the study of an associated quantitative trait locus. PNAS 90:1058–62
    [Google Scholar]
  30. 30.  Georges M, Drinkwater R, King T, Mishra A, Moore SS et al. 1993. Microsatellite mapping of a gene affecting horn development in Bos taurus. Nat. . Genet 4:206–10
    [Google Scholar]
  31. 31.  Georges M, Nielsen D, Mackinnon M, Mishra A, Okimoto R et al. 1995. Mapping quantitative trait loci controlling milk production in dairy cattle by exploiting progeny testing. Genetics 139:907–20
    [Google Scholar]
  32. 32.  Charlier C, Denys B, Belanche JI, Coppieters W, Grobet L et al. 1996. Microsatellite mapping of the bovine roan locus: a major determinant of White Heifer disease. Mamm. Genome 7:138–42
    [Google Scholar]
  33. 33.  Winter A, Kramer W, Werner FA, Kollers S, Kata S et al. 2000. Association of a lysine-232/alanine polymorphism in a bovine gene encoding acyl-CoA:diacylglycerol acyltransferase (DGAT1) with variation at a quantitative trait locus for milk fat content. PNAS 99:9300–5
    [Google Scholar]
  34. 34.  Takeda H, Takami M, Oguni T, Tsuji T, Yoneda K et al. 2002. Positional cloning of the gene LIMBIN responsible for bovine chondrodysplastic dwarfism. PNAS 99:10549–54
    [Google Scholar]
  35. 35.  O'Brien SJ, Womack JE, Lyons LA, Moore KJ, Jenkins NA, Copeland NG 1993. Anchored reference loci for comparative genome mapping in mammals. Nat. Genet. 3:103–12
    [Google Scholar]
  36. 36.  Lyons LA, Laughlin TF, Copeland NG, Jenkins NA, Womack JE, O'Brien SJ 1997. Comparative anchor tagged sequences (CATS) for integrative mapping of mammalian genomes. Nat. Genet. 15:47–56
    [Google Scholar]
  37. 37.  O'Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J et al. 1999. The promise of comparative genomics in mammals. Science 286:458–81
    [Google Scholar]
  38. 38.  Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G et al. 2005. Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–17
    [Google Scholar]
  39. 39.  Riggs PK, Owens KE, Rexroad CE III, Amaral MEJ, Womack JE 1997. Development and initial characterization of a Bos taurus × B.gaurus interspecific hybrid backcross panel. J. Hered. 88:373–79
    [Google Scholar]
  40. 40.  Gao Q, Womack JE 1997. A genetic map of bovine Chromosome 7 with an interspecific hybrid backcross panel. Mamm. Genome 8:258–61
    [Google Scholar]
  41. 41.  Yang Y-P, Womack JE 1997. Construction of a bovine Chromosome 19 map with an interspecies hybrid backcross. Mamm. Genome 8:262–66
    [Google Scholar]
  42. 42.  Womack JE, Johnson JS, Owens EK, Rexroad CE, Schlapfer J, Yang Y-P 1997. A whole-genome radiation hybrid panel for bovine gene mapping. Mamm. Genome 8:854–56
    [Google Scholar]
  43. 43.  Rexroad CE III, Owens EK, Johnson JS, Womack JE 2000. A 12,000 rad whole genome radiation hybrid panel for high resolution mapping in cattle: characterization of the centromeric end of chromosome 1. Anim. Genet. 31:262–65
    [Google Scholar]
  44. 44.  Yang Y-P, Womack JE 1998. Parallel radiation hybrid mapping: a powerful tool for high-resolution genomic comparison. Genome Res 8:731–36
    [Google Scholar]
  45. 45.  Rexroad CE III, Womack JE 1999. Parallel RH mapping of BTA1 with HSA3 and HSA21. Mamm. Genome 10:1095–97
    [Google Scholar]
  46. 46.  Womack JE, Kata SR 1995. Bovine genome mapping: evolutionary inference and the power of comparative genomics. Curr. Opin. Genet. Dev. 5:725–33
    [Google Scholar]
  47. 47.  Schläpfer J, Yang Y-P, Rexroad CE III, Womack JE 1998. A radiation hybrid framework map of the bovine chromosome 13. Chrom. Res. 5:511–19
    [Google Scholar]
  48. 48.  Yang Y-P, Rexroad CE III, Schlapfer J, Womack JE 1998. An integrated radiation hybrid map of bovine chromosome 19 and ordered comparative mapping with human chromosome 17. Genomics 48:93–99
    [Google Scholar]
  49. 49.  Gu Z, Womack JE, Kirkpatrick BW 1999. A radiation hybrid map of the bovine Chromosome 7 and comparative mapping with human Chromosome 19 p arm. Mamm. Genome 10:1112–14
    [Google Scholar]
  50. 50.  Rexroad CE, Schlapfer JS, Yang Y-P, Harlizius B, Womack JE 1999. A radiation hybrid map of bovine chromosome one. Anim. Genet. 30:325–32
    [Google Scholar]
  51. 51.  Ozawa A, Band MR, Larson JH, Donovan J, Green CA et al. 2000. Comparative organization of cattle chromosome 5 revealed by comparative mapping by annotation and sequence similarity and radiation hybrid mapping. PNAS 97:4150–55
    [Google Scholar]
  52. 52.  Ashwell MS, Sonstegard TS, Kata S, Womack JE 2002. A radiation hybrid map of bovine chromosome 27. Anim. Genet. 33:75–76
    [Google Scholar]
  53. 53.  Goldammer T, Kata SR, Brunner RM, Dorroch U, Sanftleben H et al. 2002. A comparative radiation hybrid map of bovine chromosome 18 and homologous chromosomes in human and mice. PNAS 99:2106–11
    [Google Scholar]
  54. 54.  Amaral MEJ, Kata SR, Womack JE 2002. A radiation hybrid map of bovine X Chromosome (BTAX). Mamm. Genome 13:268–71
    [Google Scholar]
  55. 55.  Band MR, Larson JH, Rebeiz M, Green CA, Heyen DW et al. 2000. An ordered comparative map of the cattle and human genomes. Genome Res 10:1359–68
    [Google Scholar]
  56. 56.  Everts-van der Wind A, Kata SR, Band MR, Rebeiz M, Larkin DM et al. 2004. A 1463 gene cattle–human comparative map with anchor points defined by human genome sequence coordinates. Genome Res 14:1424–37
    [Google Scholar]
  57. 57.  Larkin DM, Everts-van der Wind AE, Rebeiz M, Schweitzer PA, Bachman S et al. 2003. A cattle-human comparative map built with cattle BAC-ends and human genome sequence. Genome Res 13:1966–73
    [Google Scholar]
  58. 58.  Everts-van der Wind A, Larkin DM, Green CA, Elliott JS, Olmstead C et al. 2006. A high-resolution whole-genome cattle-human comparative map reveals details of mammalian chromosome evolution. PNAS 102:18526–31
    [Google Scholar]
  59. 59.  Weikard R, Goldammer T, Laurent P, Womack JE, Kuehn C 2006. A gene-based high-resolution comparative radiation hybrid map as a framework for genome sequence assembly of a bovine chromosome 6 region associated with QTL for growth, body composition, and milk performance traits. BMC Genom 7:53
    [Google Scholar]
  60. 60.  Snelling WM, Chiu R, Schein JE, Hobbs M, Abbey CA et al. 2007. A physical map of the bovine genome. Genome Biol 8:R165
    [Google Scholar]
  61. 61. Bov. Genome Seq. Anal. Consort. Elsik CG, Tellam RL, Worley KC 2009. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522–28
    [Google Scholar]
  62. 62.  Gallagher DS, Womack JE 1992. Chromosome conservation in the Bovidae. J. Hered. 83:287–98
    [Google Scholar]
  63. 63.  Gallagher DS Jr., Derr JN, Womack JE 1994. Chromosome conservation among the advanced pecorans and determination of the primitive bovid karyotype. J. Hered. 85:204–10
    [Google Scholar]
  64. 64.  Iannuzzi L, Gallagher DS, Ryan AM, Di Meo GP, Womack JE 1993. Chromosomal localization of omega and trophoblast interferon genes in cattle and river buffalo by sequential R-banding and fluorescent in situ hybridization. Cytogenet. Cell Genet. 62:224–27
    [Google Scholar]
  65. 65.  Iannuzzi L, Gallagher DS, Womack JE, Di Meo GP, Skow LC, Ferrara L 1993. Chromosomal localization of the major histocompatibility complex in cattle and river buffalo by fluorescent in situ hybridization. Hereditas 118:187–90
    [Google Scholar]
  66. 66.  Iannuzzi L, Gallagher DS, Di Meo GP, Ryan AM, Perucatti A et al. 1993. Chromosomal localization of the lysozyme gene cluster in river buffalo (Bubalus bubalis L.). Chrom. Res. 1:253–55
    [Google Scholar]
  67. 67.  Iannuzzi L, Di Meo GP, Gallagher DS, Ryan AM, Ferrara L, Womack JE 1993. Chromosomal localization of omega and trophoblast interferon genes in goat and sheep by fluorescent in situ hybridization. J. Hered. 84:301–4
    [Google Scholar]
  68. 68.  Iannuzzi L, Skow L, Di Meo GP, Gallagher DS, Womack JE 1997. Comparative FISH-mapping of villin (VIL) gene in river buffalo, sheep and goat chromosomes. Chromosome Res 5:199–202
    [Google Scholar]
  69. 69.  De Hondt HA, Gallagher D, Oraby HO, Othman OE, Bosma AA et al. 1997. Gene mapping in the river buffalo (Bubalus bubalis L.): five syntenic groups. J. Anim. Breed. Genet. 114:79–85
    [Google Scholar]
  70. 70.  El Nahas SM, Oraby HO, Othman OE, DeHondt HA, Bosma AA, Womack JE 1997. Use of molecular markers for the identification of River Buffalo chromosomes: chromosome one. J. Anim. Breed. Genet. 114:451–55
    [Google Scholar]
  71. 71.  Amaral MEJ, Owens KE, Elliott J, Fickey C, Schaffer AA et al. 2007. Construction of a river buffalo (Bubalus bubalis) whole-genome radiation hybrid panel and preliminary RH mapping of chromosomes 3 and 10. Anim. Genet. 38:311–14
    [Google Scholar]
  72. 72.  Goldammer T, Weikard R, Miziara MN, Brunner RM, Agarwala R et al. 2007. A radiation hybrid map of river buffalo (Bubalus bubalis) chromosome 7 and comparative mapping to the cattle and human genomes. Cytogenet. Genome Res. 119:235–41
    [Google Scholar]
  73. 73.  Amaral ME, Grant JR, Riggs PK, Stafuzza NB, Fiho E et al. 2008. A first generation whole genome RH map of the river buffalo with comparison to domestic cattle. BMC Genom 9:631
    [Google Scholar]
  74. 74.  Wu CH, Nomura K, Goldammer T, Hadfield T, Womack JE, Cockett NE 2007. An ovine whole-genome radiation hybrid panel used to construct an RH map of ovine chromosome 9. Anim. Genet. 38:534–36
    [Google Scholar]
  75. 75.  Wu CH, Nomura K, Goldammer T, Hadfiled T, Dalrymple BP et al. 2008. A high resolution comparative radiation hybrid map of ovine chromosomal regions that are homologous to human chromosome 6 (HSA6). Anim. Genet. 39:459–67
    [Google Scholar]
  76. 76.  Goldammer T, Brunner RM, Rebl A, Wu CH, Nomura K et al. 2009. A high-resolution radiation hybrid map of sheep chromosome X and comparison with human and cattle. Cytogenet. Genome Res. 125:40–45
    [Google Scholar]
  77. 77.  Du X, Servin B, Womack JE, Cao J, Yu M et al. 2014. An update of the goat genome assembly using dense radiation hybrid maps allows detailed analysis of evolutionary rearrangements in Bovidae. BMC Genom 15:625
    [Google Scholar]
  78. 78.  Karere GM, Froenicke L, Millon L, Womack JE, Lyons LA 2008. A high resolution radiation hybrid map of rhesus macaque chromosome 5 identifies rearrangements in the genome assembly. Genomics 92:210–18
    [Google Scholar]
  79. 79.  Gao W, Chen ZJ, Yu JZ, Raska D, Kohel RJ et al. 2004. Wide-cross whole-genome radiation hybrid mapping of cotton. Genetics 167:1317–29
    [Google Scholar]
  80. 80.  Soh YQ, Alföldi J, Pyntikova T, Brown LG, Graves T et al. 2014. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159:800–13
    [Google Scholar]
  81. 81. Bov. HapMap Consort. 2009. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324:528–32
    [Google Scholar]
  82. 82.  White SN, Kata SR, Womack JE 2003. Comparative fine maps of bovine toll-like receptor 4 and toll-like receptor 2 regions. Mamm. Genome 14:149–55
    [Google Scholar]
  83. 83.  Taylor KH, Taylor JF, White SN, Womack JE 2006. Identification of genetic variation and putative regulatory regions in bovine CARD15. Mamm. . Genome 17:892–901
    [Google Scholar]
  84. 84.  Seabury CM, Cargill EJ, Womack JE 2007. Sequence variability and protein domain architectures for bovine Toll-like receptors 1, 5 and 10. Genomics 90:502–15
    [Google Scholar]
  85. 85.  Brinkmeyer-Langford CL, Childers CP, Fritz KL, Gustafson-Seabury AL, Cothran M et al. 2009. A high resolution RH map of the bovine major histocompatibility complex. BMC Genom 10:182
    [Google Scholar]
  86. 86.  Gillenwaters EN, Seabury CM, Elliott JS, Womack JE 2009. Sequence analysis and polymorphism discovery in 4 members of the bovine cathelicidin gene family. J. Hered. 100:241–45
    [Google Scholar]
  87. 87.  Seabury CM, Seabury PM, Decker JE, Schnabel RD, Womack JE 2010. Diversity and evolution of 11 innate immune genes in Bos taurus taurus and Bos taurus indicus cattle. PNAS 107:151–56
    [Google Scholar]
  88. 88.  Lee MO, Kim EH, Jang HJ, Park MN, Woo HJ et al. 2012. Effects of a single nucleotide polymorphism in the chicken NK-lysin gene on antimicrobial activity and cytotoxicity of cancer cells. PNAS 109:12087–92
    [Google Scholar]
  89. 89.  Lee MO, Bornelov S, Andersson L, Lamont SJ, Chen J, Womack JE 2016. Duplication of chicken defensin 7 gene generated by gene conversion and homologous recombination. PNAS 113:13815–20
    [Google Scholar]
  90. 90.  Chen J, Huddleston J, Buckley RM, Malig M, Lawhon SD et al. 2015. Bovine NK-lysin: copy number variation and functional diversification. PNAS 112:52e7223–29
    [Google Scholar]
  91. 91.  Neibergs HL, Seabury CM, Wojtowicz AJ, Wang Z, Scraggs E et al. 2014. Susceptibility loci revealed for bovine respiratory disease complex in pre-weaned Holstein calves. BMC Genom 15:1164
    [Google Scholar]
  92. 92.  Van Eenennaam A, Neibergs H, Seabury C, Taylor J, Wang Z et al. 2014. Results of the BRD CAP project: progress toward identifying genetic markers associated with BRD susceptibility. Anim. Health Res. Rev. 15:157–60
    [Google Scholar]
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