Domestic-animal genomics: deciphering the genetics of complex traits

[en] One of the 'grand challenges' in modern biology is to understand the genetic basis of phenotypic diversity within and among species. Thousands of years of selective breeding of domestic animals has created a diversity of phenotypes among breeds that is only matched by that observed among species in nature. Domestic animals therefore constitute a unique resource for understanding the genetic basis of phenotypic variation. When the genome sequences of domestic animals become available the identification of the mutations that underlie the transformation from a wild to a domestic species will be a realistic and important target.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Andersson, L.

Georges, Michel ; Université de Liège - ULiège > Département de productions animales > Génomique animale

Language :

English

Title :

Domestic-animal genomics: deciphering the genetics of complex traits

Publication date :

2004

Journal title :

Nature Reviews. Genetics

ISSN :

1471-0056

eISSN :

1471-0064

Publisher :

Nature Publishing Group, London, United Kingdom

Volume :

Issue :

Pages :

202-212

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 08 November 2011

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439

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420

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416

Bibliography

Darwin, C. On the Ongins of Species by Means of Natural Selection or The Preservation of Favoured Races in the Struggle for Life (John Murray, London, 1859).
Darwin, C. The Variation of Animals and Plants Under Domestication (John Murray, London, 1868).
Darvasi, A. & Pisante-Shalom, A. Complexities in the genetic dissection of quantitative trait loci. Trends Genet. 18, 489-491 (2002).
Glazier, A. M., Nadeau, J. H. & Aitman, T. J. Finding genes that underle complex traits. Science 298, 2345-2349 (2002).
Collins, F. S., Green, E. D., Guttmacher, A. E. & Guyer, M. S. A vision for the future of genomics research. Nature 422, 835-847 (2003).
Grisart, B. et al. Positional candidate cloning of a QTL in dairy cattle: Identification of a missense mutation in the bovine DGAT1 gene with major effect on milk yield and composition. Genome Res. 12, 222-231 (2002).
Van Laere, A. S. et al. Positional identification of a regulatory mutation in IGF2 causing a major QTL effect on muscle growth in the pig. Nature 425, 832-836 (2003).
Blott, S. et al. Molecular dissection of a QTL: a phenylalanine to tyrosine substitution in the transmembrane domain of the bovine growth hormone receptor is associated with a major effect on milk yield and composition. Genetics 163, 253-266 (2002).
Grisart, B. et al. Genetic and functional demonstration of the causality of the DGAT1 K232A mutation in the determinism of the BTA14 QTL affecting milk yield and composition. Proc. Natl Acad. Sci. USA (in the press).
Winter, A. et al. 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. Proc. Natl Acad. Sci. USA 99, 9300-9305 (2002). References 6, 9 and 10 show, by linkage and linkage-disequilibrium analysis combined with functional analysis, that a missense mutation underlies an important QTL for milk yield and composition in cattle.
Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer associates Inc., Sunderland, 1998).
Mackay, T. F. C. Quantitative trait loci in Drosophila. Nature Rev. Genet. 2, 11-21 (2001).
Andersson, L. Genetic dissection of phenotypic diversity in farm animals. Nature Rev. Genet. 2, 130-138 (2001).
Jansen, R. C. in Handbook of Statistical Genetics. 2nd edn (eds. Balding, D. J., Bishop, M. & Cannings, C.) 445-476 (Wiley, England, 2003).
Hoeschele, I. in Handbook of Statistical Genetics, 2nd edn (eds. Balding, D. J., Bishop, M. & Cannings, C.) 477-525 (Wiley England, 2003).
Brookmann, G. A. et al. Single QTL effects, epistasis, and pleiotropy account for two-thirds of the phenotypic F(2) variance of growth and obesity in DU6i × DBA/2 mice. Genome Res. 10, 1941-1957 (2000).
Carlborg, Ö. et al. A global search reveals epistatic interaction between QTLs for early growth in the chicken. Genome Res. 13 (2003). A global two-dimensional search that showed that epistatic interaction explains a considerable portion of the genetic variance for early growth in an intercross between the red junglefowl and White Leghorn chickens.
Shimomura, K. et al. Genome-wide epistatic interaction analysis reveals complex genetic determinants of circadian behavior in mice. Genome Res. 11, 959-980 (2001).
Steinmetz, L. M. et al. Dissecting the architecture of a quantitative trait locus in yeast. Nature 416, 326-330 (2002).
Nezer, C. et al. Haplotype sharing refines the location of an imprinted QTL with major effect on muscle mass to a 250 Kb chromosome segment containing the porcineIGF2 gene. Genetics 165, 277-285 (2003).
Fujii, J. et al. Identification of a mutation in the porcine ryanodine receptor that is associated with malignant hyperthermia. Science 253, 448-451 (1991).
Marklund, S. et al. Molecular basis for the dominant white phenotype in the domestic pig. Genome Res. 8, 826-833 (1998).
Seitz, J. J., Schmutz, S. M., Thue, T. D. & Buchanan, F. C. A missense mutation in the bovine MGF gene is associated with the roan phenotype in Belgian Blue and Shorthorn cattle. Mamm. Genome 10, 710-712 (1999).
Milan, D. et al. A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle. Science 288, 1248-1251 (2000).
Ciobanu, D. et al. Evidence for new alleles in the protein kinase adenosine monophosphate-activated γ3-subunit gene associated with low glycogen content in pig skeletal muscle and improved meat quality. Genetics 159, 1151-1162 (2001).
Lindahl, G. et al. A second mutant allele (V199I) at the PRKAG3 (RN) locus-I. Effect on technological meat quality of pork loin. Meat Science 66, 609-619 (2003).
Lindahl, G. et al. A second mutant allele (V199I) at the PRKAG3 (RN) locus-II. Effect on colour characteristics of pork loin. Meat Science 66, 621-627 (2003).
Scott, J. W. et al. CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J. Clin. Invest. 113, 274-284 (2004).
Darvasi, A. Experimental strategies for the genetic dissection of complex traits in animal models. Nature Genetics 18, 19-24 (1998).
Meuwissen, T. H. & Goddard, M. E. Fine mapping of quantitative trait loci using linkage disequilibria with closely linked marker loci. Genetics 155, 421-430 (2000).
Meuwissen, T. H. & Goddard, M. E. Prediction of identity by descent probabilities from marker-haplotypes. Genet. Sel. Evol. 33, 605-634 (2001).
Farnir, F. et al. Simultaneous mining of linkage and linkage disequilibrium to fine map quantitative trait loci in outbred half-sib pedigrees: revisiting the location of a quantitative trait locus with major effect on milk production on bovine chromosome 14. Genetics 161, 275-287 (2002).
Perez-Enciso, M. Fine mapping of complex trait genes combining pedigree and linkage disequilibrium information: a Bayesian unified framework. Genetics 163, 1497-1510 (2003). References 30-33 describe a statistical methodology that exploits linkage disequilibrium for high-resolution mapping in domestic animals.
Maynard-Smith, J. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23-35 (1974). A classic paper that shows that a selective sweep of a favourable mutation causes a 'hitch-hiking' effect at linked loci.
Meuwissen, T. H., Kadsen, A., Lien, S., Olsaker, I. & Goddard, M. E. Fine mapping of a quantitative trait locus for twinning rate using combined linkage and linkage disequilibrium mapping. Genetics 161, 373-379 (2002).
Silver, L. M. Mouse Genetics (Oxford University Press, New York, 1995).
Beck, J. A. et al. Genealogies of mouse inbred strains. Nature Genet. 24, 23-25 (2000).
Nadeau, J. H. & Frankel, W. N. The roads from phenotypic variation to gene discovery: mutagenesis versus QTLs. Nature Genet. 25, 381-384 (2000).
Kirkness, E. F. et al. The dog genome: survey sequencing and comparative analysis. Science 301, 1898-1903 (2003).
Ostrander, E. A. & Krugiyak, L. Unleashing the canine genome. Genome Res. 10, 1271-1274 (2000).
Ungaas, F. et al. A mutation in the canine BHD gene is associated with hereditary multifocal renal cystadeno-carcinoma and nodular dermatofibrosis in the German Shepherd dog. Hum. Mol. Genet. 12, 3043-3053 (2003).
Springer, M. S., Murphy, W. J., Eizirik, E. & O'Brien, S. J. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc. Natl Acad. Sci. USA 100, 1056-1061 (2003).
Stone, R. T. et al. Use of bovine EST data and human genomic sequences to map 100 gene-specific bovine markers. Anim. Genet. 13, 211-215 (2002).
Fahrenkrug, S. C., Freking, B. A., Smith, T. P., Rohrer, G. A. & Keele, J. W. Single nucleotide polymorphism (SNP) discovery in porcine expressed genes. Anim. Genet. 33, 186-195 (2002).
Wade, C. M. et al. The mosaic structure of variation in the laboratory mouse genome. Nature 420, 574-578 (2002).
The International HapMap Consortium. The international HapMap project. Nature 426, 789-796 (2003).
Farnir, F. et al. Extensive genome-wide linkage disequilibrium in cattle. Genome Res. 10, 220-227 (2000).
Giuffra, E. et al. The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 154, 1785-1791 (2000).
Bruford, M. W., Bradley, D. G. & Luikart, G. DNA markers reveal the complexity of livestock domestication. Nature Rev. Genet. 4, 900-910 (2003). A review on the complexity of livestock domestication.
Jansen, R. C. & Nap, J. P. Genetical genomics: the added value from segregation. Trends Genet. 17, 388-391 (2001).
Schadt, E. E. et al. Genetics of gene expression surveyed in maize, mouse and man. Nature 422, 297-302 (2003).
Sellers, T. A. & Yates, J. R. Review of proteomics with applications to genetic epidemiology, Genet. Epidemiol. 24, 83-98 (2003).
Olson, M. V. & Varki, A. Sequencing the chimpanzee genome: insights into human evolution and disease. Nature Rev. Genet. 4, 20-28 (2003).
Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869-872 (2002).
Clark, A. G. et al. Inferring nonneutral evolution from human-chimp-mouse orthotogous gene trios. Science 302, 1960-1963 (2003).
Mouse Genome Sequencing Consortium, Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562 (2002).
Thomas, J. W. et al. Comparative analyses of multi-species sequences from targeted genomic regions. Nature 424, 786-793 (2003).
Margulies, E. H., Blanchette, M., Haussler, D. & Green, E. D. Identification and characterization of multi-species conserved sequences. Genome Res. 13, 2507-2518 (2003). References 57-58 show the power of multi-species comparative sequence analysis for detecting evolutionary conserved sequences.
Silvers, W. K. The Coat Colors of Mice. A Model for Mammalian Gene Action and Interaction. (Springer-Verlag, New York, 1979).
Hartman, J. L. T., Garvik, B. & Hartwell, L. Principles for the buffering of genetic varation. Science 291, 1001-1004 (2001).
Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genet. 33 (Suppl.), 245-254 (2003).
Morgan, H. D., Sutherland, H. G., Martin, D. I. & Whitelaw, E. Epigenetic inheritance at the agouti locus in the mouse. Nature Genet. 23, 314-318 (1999).
Grewal, S. I. & Klar, A. J. Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 86, 95-101 (1996).
Cavalli, G. & Paro, R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 93, 505-518 (1998).
Sollars, V. et al. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nature Genet. 33, 70-74 (2003).
Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161 (1999).
Kakutani, T. Epi-alleles in plants: inheritance of epigenetic information over generations. Plant Cell 43, 1106-1111 (2002).
Martienssen, R. A. & Colot, V. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293, 1070-1074 (2001). References 62-68 illustrate the fact that epimutations can be inherited and can contribute to phenotypic variation.
Jeon, J.-T. et al. A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to the IGF2 locus. Nature Genet. 21, 157-158 (1999).
Nezer, C. et al. An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs. Nature Genet, 21, 155-156 (1999).
Kijas, J. M. H. & Andersson, L. A phytogenetic study of the origin of the domestic pig estimated from the near complete mtDNA genome. J. Mol. Evol. 52, 302-308 (2001).
Grobet, L. et al. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genet. 17, 71-74 (1997).
Grobet, L. et al. Molecular definition of an allelic series of mutations disrupting the myostatin function and causing double-muscling in cattle. Mamm. Genome 9, 210-213 (1998).
Kambadur, R., Sharma, M., Smith, T. P. & Bass, J. J. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res. 7, 910-916 (1997).
McPherron, A. C. & Lee, S. J. Double muscling in cattle due to mutations in the myostatin gene, Proc. Natl Acad. Sci. USA 94, 12457-12461 (1997).
Klungland, H., Vage, D. I., Gomez-Raya, L., Adalsteinsson, S. & Lien, S. The role of melanocyte-stimulating hormone (MSH) receptor in bovine coat color determination. Mamm. Genome 6, 636-639 (1995).
Lundén, A., Marklund, S., Gustafsson, V. & Andersson, L. A nonsense mutation in the FMO3 gene underlies fishy off-flavor in cow's milk. Genome Res. 12, 1885-1888 (2003).
Tobita-Teramoto, T. et al. Autosomal albino chicken mutation (c(a)/c(a)) deletes hexanucleotide (-Delta GACTGG817) at a copper-binding site of the tyrosinase gene. Poult. Sci. 79, 46-50 (2000).
Kerje, S., Lind, J., Schütz, K., Jensen, P. & Andersson, L. Melanocortin 1-receptor (MC1R) mutations are associated with plumage colour in chicken. Animal Genetics 34, 241-248 (2003).
Kerje, S. Mapping Genes Affecting Phenotypic Traits in Chicken. Thesis, Uppsala Univ., Sweden (2003).
Lin, L. et al. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98, 365-376 (1999).
Schmutz, M., Berryere, T. G., Blinwood, N. M., Kerns, J. A. & Barsh, G. S. MC1R studies in dogs with melanistic mask or brindle patterns. J. Hered. 94, 69-73 (2003).
Pailhoux, E. et al. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nature Genet, 29, 453-458 (2001) In this paper, positional cloning showed that an 11.7-kb deletion of an intergenic region causes lack of horns and intersexuality in goats.
Marklund, L., Moller, M. J., Sandberg, K. & Andersson, L. A missense mutation in the gene for melanocyte-stimulating hormone receptor (MC1R) is associated with the chestnut coat color in horses. Mamm. Genome 7, 895-899 (1996).
Rieder, S., Taourit, S., Mariat, D., Langlois, B. & Guerin, G. Mutations in the agouti (ASIP), the extension (MC1R), and the brown (TYRP1) loci and their association to coat color phenotypes in horses (Equus caballus). Mamm. Genome 12, 450-455 (2001).
Mariat, D., Taourit, S. & Guerin, G. A mutation in the MATP gene causes the cream coat cotour in the horse. Genet. Sel. Evol. 35, 119-133 (2003).
Santschi, E. M. et al. Endothelin receptor B polymorphism associated with lethal white foal syndrome in horses. Mamm. Genome 9, 306-309 (1998).
Metallinos, D. L., Bowling, A. T. & Rine, J. A missense mutation in the endothelin-B receptor gene is associated with Lethal White Foal Syndrome: an equine version of Hirschsprung disease. Mamm. Genome 9, 426-431 (1998)
Yang, G. C. et al. A dinudeotide mutation in the endothelin-B receptor gene is associated with lethal white foal syndrome (LWFS); a horse variant of Hirschsprung disease. Hum. Mol. Genet. 7, 1047-1052 (1998).
Johansson Moller, M. et al. Pigs with the dominant white coat color phenotype carry a duplication of the KIT gene encoding the mast/stem cell growth factor receptor. Mamm. Genome 7, 822-830 (1996).
Giuffra, E. et al. A large duplication associated with Dominant White color in pigs originated by homologous recombination between LINE elements flanking KIT. Mamm. Genome 13, 569-577 (2002).
Hasler-Rapacz, J. et al. Identification of a mutation in the low density lipoprotein receptor gene associated with recessive familial hypercholesterolemia in swine. Am. J. Med. Genet. 76, 379-386 (1998).
Kijas, J. M. H. et al. Melanocortin receptor 1 (MC1R) mutations and coat color in pigs. Genetics 150, 1177-1185 (1998).
Kijas, J. M. H., Moller, M., Plastow, G. & Andersson, L. A frameshift mutation in MC1R and a high frequency of somatic reversions cause black spotting in pigs. Genetics 158, 779-785 (2001).
Meijerink, E. et al. A DNA polymorphism influencing alpha(1,2)fucosytransferase activity of the pig FUT1 enzyme determines susceptibility of small intestinal epithelium to Escherihia coli F18 adhesion. Immunogenet, 52, 129-136 (2000).
Galloway, S. M. et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nature Genet, 25, 279-283 (2000).
Mulsant, P. et al. Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc. Natl Acad. Sci. USA 98, 5104-5109 (2001).
Freking, B. A. et al. Identification of the single base change causing the callipyge muscle hypertrophy phenotype, the only known example of polar overdominance in mammals. Genome Res. 12, 1496-1506 (2002).
Charlier, C. et al. The callipyge mutation enhances the expression of coregulated imprinted genes in cis without affecting their imprinting status. Nature Genet. 27, 367-369 (2002). References 98-99 show that a single nucleotide substitution in an intergenic region upregulates several imprinted genes in cis, which in turn leads to muscle hypertrophy in sheep.
Meuwissen, T. H. E & Goddard, M. E. Mapping multiple QTL using linkage disequilibhum and linkage analysis informaton and multiple traits. Genet. Sol. Evol. (in the press).