Genomic dissection of the correlation between milk yield and various health traits using functional and evolutionary information about imputed sequence variants of 34,497 German Holstein cows.

Dairy cattle Functional information Genome annotation Genomic prediction Health traits Imputed whole genome sequence variants Milk production

Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
09 Mar 2024
Historique:
received: 17 08 2023
accepted: 13 02 2024
medline: 10 3 2024
pubmed: 10 3 2024
entrez: 9 3 2024
Statut: epublish

Résumé

Over the last decades, it was subject of many studies to investigate the genomic connection of milk production and health traits in dairy cattle. Thereby, incorporating functional information in genomic analyses has been shown to improve the understanding of biological and molecular mechanisms shaping complex traits and the accuracies of genomic prediction, especially in small populations and across-breed settings. Still, little is known about the contribution of different functional and evolutionary genome partitioning subsets to milk production and dairy health. Thus, we performed a uni- and a bivariate analysis of milk yield (MY) and eight health traits using a set of ~34,497 German Holstein cows with 50K chip genotypes and ~17 million imputed sequence variants divided into 27 subsets depending on their functional and evolutionary annotation. In the bivariate analysis, eight trait-combinations were observed that contrasted MY with each health trait. Two genomic relationship matrices (GRM) were included, one consisting of the 50K chip variants and one consisting of each set of subset variants, to obtain subset heritabilities and genetic correlations. In addition, 50K chip heritabilities and genetic correlations were estimated applying merely the 50K GRM. In general, 50K chip heritabilities were larger than the subset heritabilities. The largest heritabilities were found for MY, which was 0.4358 for the 50K and 0.2757 for the subset heritabilities. Whereas all 50K genetic correlations were negative, subset genetic correlations were both, positive and negative (ranging from -0.9324 between MY and mastitis to 0.6662 between MY and digital dermatitis). The subsets containing variants which were annotated as noncoding related, splice sites, untranslated regions, metabolic quantitative trait loci, and young variants ranked highest in terms of their contribution to the traits` genetic variance. We were able to show that linkage disequilibrium between subset variants and adjacent variants did not cause these subsets` high effect. Our results confirm the connection of milk production and health traits in dairy cattle via the animals` metabolic state. In addition, they highlight the potential of including functional information in genomic analyses, which helps to dissect the extent and direction of the observed traits` connection in more detail.

Sections du résumé

BACKGROUND BACKGROUND
Over the last decades, it was subject of many studies to investigate the genomic connection of milk production and health traits in dairy cattle. Thereby, incorporating functional information in genomic analyses has been shown to improve the understanding of biological and molecular mechanisms shaping complex traits and the accuracies of genomic prediction, especially in small populations and across-breed settings. Still, little is known about the contribution of different functional and evolutionary genome partitioning subsets to milk production and dairy health. Thus, we performed a uni- and a bivariate analysis of milk yield (MY) and eight health traits using a set of ~34,497 German Holstein cows with 50K chip genotypes and ~17 million imputed sequence variants divided into 27 subsets depending on their functional and evolutionary annotation. In the bivariate analysis, eight trait-combinations were observed that contrasted MY with each health trait. Two genomic relationship matrices (GRM) were included, one consisting of the 50K chip variants and one consisting of each set of subset variants, to obtain subset heritabilities and genetic correlations. In addition, 50K chip heritabilities and genetic correlations were estimated applying merely the 50K GRM.
RESULTS RESULTS
In general, 50K chip heritabilities were larger than the subset heritabilities. The largest heritabilities were found for MY, which was 0.4358 for the 50K and 0.2757 for the subset heritabilities. Whereas all 50K genetic correlations were negative, subset genetic correlations were both, positive and negative (ranging from -0.9324 between MY and mastitis to 0.6662 between MY and digital dermatitis). The subsets containing variants which were annotated as noncoding related, splice sites, untranslated regions, metabolic quantitative trait loci, and young variants ranked highest in terms of their contribution to the traits` genetic variance. We were able to show that linkage disequilibrium between subset variants and adjacent variants did not cause these subsets` high effect.
CONCLUSION CONCLUSIONS
Our results confirm the connection of milk production and health traits in dairy cattle via the animals` metabolic state. In addition, they highlight the potential of including functional information in genomic analyses, which helps to dissect the extent and direction of the observed traits` connection in more detail.

Identifiants

pubmed: 38461236
doi: 10.1186/s12864-024-10115-6
pii: 10.1186/s12864-024-10115-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

265

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : BE3703/15-1
Organisme : Deutsche Forschungsgemeinschaft
ID : TE622/6-1
Organisme : Deutsche Forschungsgemeinschaft
ID : TE622/6-1
Organisme : Deutsche Forschungsgemeinschaft
ID : BE3703/15-1

Informations de copyright

© 2024. The Author(s).

Références

(VIT) Vereinigte Informationssysteme Tierhaltung w.V. 2022. Jahresbericht 2022. Accessed 11 June 2023. https://www.vit.de/fileadmin/Wir-sind-vit/Jahresberichte/vit-JB2022-gesamt.pdfRCo .
Weber A, Stamer E, Junge W, Thaller G. Genetic parameters for lameness and claw and leg diseases in dairy cows. J Dairy Sci. 2013;96:3310–8.
pubmed: 23477816 doi: 10.3168/jds.2012-6261
Becker VAE, Stamer E, Spiekers H, Thaller G. Residual energy intake, energy balance, and liability to diseases: Genetic parameters and relationships in German Holstein dairy cows. J Dairy Sci. 2021;104:10970–8.
pubmed: 34334207 doi: 10.3168/jds.2021-20382
Miglior F, Muir BL, van Doormaal BJ. Selection indices in Holstein cattle of various countries. J Dairy Sci. 2005;88:1255–63.
pubmed: 15738259 doi: 10.3168/jds.S0022-0302(05)72792-2
Mostert PF, van Middelaar CE, de Boer I, Bokkers E. The impact of foot lesions in dairy cows on greenhouse gas emissions of milk production. Agric Syst. 2018;167:206–12.
doi: 10.1016/j.agsy.2018.09.006
Dolecheck KA, Overton MW, Mark TB, Bewley JM. Use of a stochastic simulation model to estimate the cost per case of digital dermatitis, sole ulcer, and white line disease by parity group and incidence timing. J Dairy Sci. 2019;102:715–30.
pubmed: 30415843 doi: 10.3168/jds.2018-14901
Knapp JR, Laur GL, Vadas PA, Weiss WP, Tricarico JM. Invited review: Enteric methane in dairy cattle production: quantifying the opportunities and impact of reducing emissions. J Dairy Sci. 2014;97:3231–61.
pubmed: 24746124 doi: 10.3168/jds.2013-7234
Adesogan AT, Havelaar AH, McKune SL, Eilittä M, Dahl GE. Animal source foods: Sustainability problem or malnutrition and sustainability solution? Perspective matters. Glob Food Secur. 2020;25:100325.
doi: 10.1016/j.gfs.2019.100325
Manzanilla-Pech CIV, L Vendahl P, Mansan Gordo D, Difford GF, Pryce JE, Schenkel F, et al. Breeding for reduced methane emission and feed-efficient Holstein cows: An international response. J Dairy Sci. 2021;104:8983–9001.
Kern C, Wang Y, Xu X, Pan Z, Halstead M, Chanthavixay G, et al. Functional annotations of three domestic animal genomes provide vital resources for comparative and agricultural research. Nat Commun. 2021;12:1821.
pubmed: 33758196 pmcid: 7988148 doi: 10.1038/s41467-021-22100-8
Meuwissen TH, Hayes BJ, Goddard ME. Prediction of total genetic value using genome-wide dense marker maps. Genetics. 2001;157:1819–29.
pubmed: 11290733 pmcid: 1461589 doi: 10.1093/genetics/157.4.1819
Calus MPL. Genomic breeding value prediction: methods and procedures. Animal. 2010;4:157–64.
pubmed: 22443868 doi: 10.1017/S1751731109991352
van den Berg I, Xiang R, Jenko J, Pausch H, Boussaha M, Schrooten C, et al. Meta-analysis for milk fat and protein percentage using imputed sequence variant genotypes in 94,321 cattle from eight cattle breeds. Genet Sel Evol. 2020;52:37.
pubmed: 32635893 pmcid: 7339598 doi: 10.1186/s12711-020-00556-4
Xiang R, MacLeod IM, Daetwyler HD, de Jong G, O’Connor E, Schrooten C, et al. Genome-wide fine-mapping identifies pleiotropic and functional variants that predict many traits across global cattle populations. Nat Commun. 2021;12:860.
pubmed: 33558518 pmcid: 7870883 doi: 10.1038/s41467-021-21001-0
Clark EL, Archibald AL, Daetwyler HD, Groenen MAM, Harrison PW, Houston RD, et al. From FAANG to fork: application of highly annotated genomes to improve farmed animal production. Genome Biol. 2020;21:285.
pubmed: 33234160 pmcid: 7686664 doi: 10.1186/s13059-020-02197-8
van Binsbergen R, Calus MPL, Bink MCAM, van Eeuwijk FA, Schrooten C, Veerkamp RF. Genomic prediction using imputed whole-genome sequence data in Holstein Friesian cattle. Genet Sel Evol. 2015;47:71.
pubmed: 26381777 pmcid: 4574568 doi: 10.1186/s12711-015-0149-x
Vanraden PM, Tooker ME, O’Connell JR, Cole JB, Bickhart DM. Selecting sequence variants to improve genomic predictions for dairy cattle. Genet Sel Evol. 2017;49:32.
pubmed: 28270096 pmcid: 5339980 doi: 10.1186/s12711-017-0307-4
Liu S, Gao Y, Canela-Xandri O, Wang S, Yu Y, Cai W, et al. A multi-tissue atlas of regulatory variants in cattle. Nat Genet. 2022;54:1438–47.
pubmed: 35953587 pmcid: 7613894 doi: 10.1038/s41588-022-01153-5
Sanna S, Li B, Mulas A, Sidore C, Kang HM, Jackson AU, et al. Fine mapping of five loci associated with low-density lipoprotein cholesterol detects variants that double the explained heritability. PLoS Genet. 2011;7:e1002198.
pubmed: 21829380 pmcid: 3145627 doi: 10.1371/journal.pgen.1002198
Xiang R, van den Berg I, MacLeod IM, Hayes BJ, Prowse-Wilkins CP, Wang M, et al. Quantifying the contribution of sequence variants with regulatory and evolutionary significance to 34 bovine complex traits. Proc Natl Acad Sci U S A. 2019;116:19398–408.
pubmed: 31501319 pmcid: 6765237 doi: 10.1073/pnas.1904159116
Schaub MA, Boyle AP, Kundaje A, Batzoglou S, Snyder M. Linking disease associations with regulatory information in the human genome. Genome Res. 2012;22:1748–59.
pubmed: 22955986 pmcid: 3431491 doi: 10.1101/gr.136127.111
Albert FW, Kruglyak L. The role of regulatory variation in complex traits and disease. Nat Rev Genet. 2015;16:197–212.
pubmed: 25707927 doi: 10.1038/nrg3891
Bouwman AC, Daetwyler HD, Chamberlain AJ, Ponce CH, Sargolzaei M, Schenkel FS, et al. Meta-analysis of genome-wide association studies for cattle stature identifies common genes that regulate body size in mammals. Nat Genet. 2018;50:362–7.
pubmed: 29459679 doi: 10.1038/s41588-018-0056-5
Xiang R, Hayes BJ, Vander Jagt CJ, MacLeod IM, Khansefid M, Bowman PJ, et al. Genome variants associated with RNA splicing variations in bovine are extensively shared between tissues. BMC Genomics. 2018;19:521.
pubmed: 29973141 pmcid: 6032541 doi: 10.1186/s12864-018-4902-8
Fang L, Sahana G, Ma P, Su G, Yu Y, Zhang S, et al. Exploring the genetic architecture and improving genomic prediction accuracy for mastitis and milk production traits in dairy cattle by mapping variants to hepatic transcriptomic regions responsive to intra-mammary infection. Genet Sel Evol. 2017;49:44.
pubmed: 28499345 pmcid: 5427631 doi: 10.1186/s12711-017-0319-0
Fang L, Sahana G, Ma P, Su G, Yu Y, Zhang S, et al. Use of biological priors enhances understanding of genetic architecture and genomic prediction of complex traits within and between dairy cattle breeds. BMC Genomics. 2017;18:604.
pubmed: 28797230 pmcid: 5553760 doi: 10.1186/s12864-017-4004-z
Xu L, Gao N, Wang Z, Xu L, Liu Y, Chen Y, et al. Incorporating genome annotation into genomic prediction for carcass traits in Chinese Simmental beef cattle. Front Genet. 2020;11:481.
pubmed: 32499816 pmcid: 7243208 doi: 10.3389/fgene.2020.00481
Xiang R, Breen EJ, Prowse-Wilkins CP, Chamberlain AJ, Goddard ME. Bayesian genome-wide analysis of cattle traits using variants with functional and evolutionary significance; 2021. Anim Prod Sci. 2021;61:1818–27.
doi: 10.1071/AN21061
Heidaritabar M, Calus MPL, Megens H-J, Vereijken A, Groenen MAM, Bastiaansen JWM. Accuracy of genomic prediction using imputed whole-genome sequence data in white layers. J Anim Breed Genet. 2016;133:167–79.
pubmed: 26776363 doi: 10.1111/jbg.12199
Schneider H, Segelke D, Tetens J, Thaller G, Bennewitz J. A genomic assessment of the correlation between milk production traits and claw and udder health traits in Holstein dairy cattle. J Dairy Sci. 2023;106:1190–205. https://doi.org/10.3168/jds.2022-22312 .
doi: 10.3168/jds.2022-22312 pubmed: 36460501
Križanac A-M, Reimer C, Heise J, Liu Z, Pryce J, Bennewitz J, et al. Sequence-based GWAS in 180 000 German Holstein cattle reveals new candidate genes for milk production traits. bioRxiv. 2023. https://doi.org/10.1101/2023.12.06.570350 .
Browning BL, Browning SR. A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet. 2009;84:210–23.
pubmed: 19200528 pmcid: 2668004 doi: 10.1016/j.ajhg.2009.01.005
Yang J, Lee SH, Goddard ME, Visscher PM. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet. 2011;88:76–82.
pubmed: 21167468 pmcid: 3014363 doi: 10.1016/j.ajhg.2010.11.011
McLaren W, Gil L, Hunt SE, Riat HS, Ritchie GRS, Thormann A, et al. The ensembl variant effect predictor. Genome Biol. 2016;17:122.
pubmed: 27268795 pmcid: 4893825 doi: 10.1186/s13059-016-0974-4
Grant JR, Arantes AS, Liao X, Stothard P. In-depth annotation of SNPs arising from resequencing projects using NGS-SNP. Bioinformatics. 2011;27:2300–1.
pubmed: 21697123 pmcid: 3150039 doi: 10.1093/bioinformatics/btr372
Khansefid M, Pryce JE, Bolormaa S, Chen Y, Millen CA, Chamberlain AJ, et al. Comparing allele specific expression and local expression quantitative trait loci and the influence of gene expression on complex trait variation in cattle. BMC Genomics. 2018;19:793.
pubmed: 30390624 pmcid: 6215656 doi: 10.1186/s12864-018-5181-0
Liu Z, Moate P, Cocks B, Rochfort S. Comprehensive polar lipid identification and quantification in milk by liquid chromatography-mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2015;978–979:95–102.
pubmed: 25531876 doi: 10.1016/j.jchromb.2014.11.036
Villar D, Berthelot C, Aldridge S, Rayner TF, Lukk M, Pignatelli M, et al. Enhancer evolution across 20 mammalian species. Cell. 2015;160:554–66.
pubmed: 25635462 pmcid: 4313353 doi: 10.1016/j.cell.2015.01.006
Zhao C, Carrillo JA, Tian F, Zan L, Updike SM, Zhao K, et al. Genome-Wide H3K4me3 Analysis in Angus Cattle with Divergent Tenderness. PLoS One. 2015;10:e0115358.
pubmed: 26086782 pmcid: 4473007 doi: 10.1371/journal.pone.0115358
Field Y, Boyle EA, Telis N, Gao Z, Gaulton KJ, Golan D, et al. Detection of human adaptation during the past 2000 years. Science. 2016;354:760–4.
pubmed: 27738015 pmcid: 5182071 doi: 10.1126/science.aag0776
Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 2005;15:1034–50.
pubmed: 16024819 pmcid: 1182216 doi: 10.1101/gr.3715005
Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, et al. Common SNPs explain a large proportion of the heritability for human height. Nat Genet. 2010;42:565–9.
pubmed: 20562875 pmcid: 3232052 doi: 10.1038/ng.608
R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org .
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–75.
pubmed: 17701901 pmcid: 1950838 doi: 10.1086/519795
Weissbrod O, Hormozdiari F, Benner C, Cui R, Ulirsch J, Gazal S, et al. Functionally informed fine-mapping and polygenic localization of complex trait heritability. Nat Genet. 2020;52:1355–63.
pubmed: 33199916 pmcid: 7710571 doi: 10.1038/s41588-020-00735-5
Heringstad B, Egger-Danner C, Charfeddine N, Pryce JE, Stock KF, Kofler J, et al. Invited review: genetics and claw health: opportunities to enhance claw health by genetic selection. J Dairy Sci. 2018;101:4801–21.
pubmed: 29525301 doi: 10.3168/jds.2017-13531
König S, Wu XL, Gianola D, Heringstad B, Simianer H. Exploration of relationships between claw disorders and milk yield in Holstein cows via recursive linear and threshold models. J Dairy Sci. 2008;91:395–406.
pubmed: 18096964 doi: 10.3168/jds.2007-0170
Gernand E, Rehbein P, von Borstel UU, König S. Incidences of and genetic parameters for mastitis, claw disorders, and common health traits recorded in dairy cattle contract herds. J Dairy Sci. 2012;95:2144–56.
pubmed: 22459859 doi: 10.3168/jds.2011-4812
Haile-Mariam M, Nieuwhof GJ, Beard KT, Konstatinov KV, Hayes BJ. Comparison of heritabilities of dairy traits in Australian Holstein-Friesian cattle from genomic and pedigree data and implications for genomic evaluations. J Anim Breed Genet. 2013;130:20–31.
pubmed: 23317062 doi: 10.1111/j.1439-0388.2012.01001.x
Cai Z, Dusza M, Guldbrandtsen B, Lund MS, Sahana G. Distinguishing pleiotropy from linked QTL between milk production traits and mastitis resistance in Nordic Holstein cattle. Genet Sel Evol. 2020;52:19.
pubmed: 32264818 pmcid: 7137482 doi: 10.1186/s12711-020-00538-6
Griesemer D, Xue JR, Reilly SK, Ulirsch JC, Kukreja K, Davis JR, et al. Genome-wide functional screen of 3’UTR variants uncovers causal variants for human disease and evolution. Cell. 2021;184:5247-5260.e19.
pubmed: 34534445 pmcid: 8487971 doi: 10.1016/j.cell.2021.08.025
Wittkopp PJ, Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet. 2011;13:59–69.
pubmed: 22143240 doi: 10.1038/nrg3095
Xiang R, Fang L, Liu S, MacLeod IM, Liu Z, Breen EJ, et al. Gene expression and RNA splicing explain large proportions of the heritability for complex traits in cattle; 2022. https://doi.org/10.1101/2022.05.30.494093 . Assessed the 17 June 2023.
Mackay TFC. The genetic architecture of quantitative traits: lessons from Drosophila. Curr Opin Genet Dev. 2004;14:253–7.
pubmed: 15172667 doi: 10.1016/j.gde.2004.04.003
Finucane HK, Bulik-Sullivan B, Gusev A, Trynka G, Reshef Y, Loh P-R, et al. Partitioning heritability by functional annotation using genome-wide association summary statistics. Nat Genet. 2015;47:1228–35.
pubmed: 26414678 pmcid: 4626285 doi: 10.1038/ng.3404
Hanslik S, Harr B, Brem G, Schlötterer C. Microsatellite analysis reveals substantial genetic differentiation between contemporary New World and Old World Holstein Friesian populations. Anim Genet. 2000;31:31–8.
pubmed: 10690359 doi: 10.1046/j.1365-2052.2000.00569.x
de Roos APW, Hayes BJ, Spelman RJ, Goddard ME. Linkage disequilibrium and persistence of phase in Holstein-Friesian Jersey and Angus cattle. Genetics. 2008;179:1503–12.
pubmed: 18622038 pmcid: 2475750 doi: 10.1534/genetics.107.084301
Hulsegge I, Oldenbroek K, Bouwman A, Veerkamp R, Windig J. Selection and drift: a comparison between historic and recent dutch friesian cattle and recent Holstein Friesian using WGS data. Animals (Basel). 2022;12(3):329.
pubmed: 35158654 doi: 10.3390/ani12030329
Gibbs RA, Taylor JF, van Tassell CP, Barendse W, Eversole KA, Gill CA, et al. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science. 2009;324:528–32.
pubmed: 19390050 doi: 10.1126/science.1167936
Wang XG, Ju ZH, Hou MH, Jiang Q, Yang CH, Zhang Y, et al. Deciphering transcriptome and complex alternative splicing transcripts in mammary gland tissues from cows naturally infected with staphylococcus aureus mastitis. PLoS One. 2016;11:e0159719.
pubmed: 27459697 pmcid: 4961362 doi: 10.1371/journal.pone.0159719
Zhang Z, Zhang J, Diao L, Han L. Small non-coding RNAs in human cancer: function, clinical utility, and characterization. Oncogene. 2021;40:1570–7.
pubmed: 33452456 doi: 10.1038/s41388-020-01630-3
Ambros V. The functions of animal microRNAs. Nature. 2004;431:350–5.
pubmed: 15372042 doi: 10.1038/nature02871
Cai Z, Guldbrandtsen B, Lund MS, Sahana G. Weighting sequence variants based on their annotation increases the power of genome-wide association studies in dairy cattle. Genet Sel Evol. 2019;51:20.
pubmed: 31077144 pmcid: 6511139 doi: 10.1186/s12711-019-0463-9
Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet. 2006;15 Spec No 1:R17-29.
Yang L, Li P, Yang W, Ruan X, Kiesewetter K, Zhu J, Cao H. Integrative transcriptome analyses of metabolic responses in mice define pivotal LncRNA metabolic regulators. Cell Metab. 2016;24:627–39.
pubmed: 27667668 pmcid: 5181118 doi: 10.1016/j.cmet.2016.08.019
Nolte W, Weikard R, Brunner RM, Albrecht E, Hammon HM, Reverter A, Kühn C. Biological network approach for the identification of regulatory long non-coding RNAs associated with metabolic efficiency in cattle. Front Genet. 2019;10:1130.
pubmed: 31824560 pmcid: 6883949 doi: 10.3389/fgene.2019.01130
Nolte W, Weikard R, Albrecht E, Hammon HM, Kühn C. Metabogenomic analysis to functionally annotate the regulatory role of long non-coding RNAs in the liver of cows with different nutrient partitioning phenotype. Genomics. 2022;114:202–14.
pubmed: 34923089 doi: 10.1016/j.ygeno.2021.12.004
Tan JY, Smith AAT, Da Ferreira Silva M, Matthey-Doret C, Rueedi R, Sönmez R, et al. cis-Acting Complex-Trait-associated lincRNA expression correlates with modulation of chromosomal architecture. Cell Rep. 2017;18:2280–8.
pubmed: 28249171 doi: 10.1016/j.celrep.2017.02.009
Lu W, Cao F, Wang S, Sheng X, Ma J. LncRNAs: The Regulator of Glucose and Lipid Metabolism in Tumor Cells. Front Oncol. 2019;9:1099.
pubmed: 31850189 pmcid: 6901916 doi: 10.3389/fonc.2019.01099
Muret K, Désert C, Lagoutte L, Boutin M, Gondret F, Zerjal T, Lagarrigue S. Long noncoding RNAs in lipid metabolism: literature review and conservation analysis across species. BMC Genomics. 2019;20:882.
pubmed: 31752679 pmcid: 6868825 doi: 10.1186/s12864-019-6093-3
Venkat M, Chia LW, Lambers TT. Milk polar lipids composition and functionality: a systematic review. Crit Rev Food Sci Nutr. 2022:1–45.
Razzaghi A, Ghaffari MH, Rico DE. The impact of environmental and nutritional stresses on milk fat synthesis in dairy cows. Domest Anim Endocrinol. 2023;83:106784.
pubmed: 36586193 doi: 10.1016/j.domaniend.2022.106784
Ingvartsen KL. Feeding- and management-related diseases in the transition cow. Anim Feed Sci Technol. 2006;126:175–213.
doi: 10.1016/j.anifeedsci.2005.08.003
Grisart B, Coppieters W, Farnir F, Karim L, Ford C, Berzi P, 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. 2002;12:222–31.
pubmed: 11827942 doi: 10.1101/gr.224202
Winter A, Krämer W, Werner FAO, Kollers S, Kata S, Durstewitz G, 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. PNAS. 2002;99:9300–5.
pubmed: 12077321 pmcid: 123135 doi: 10.1073/pnas.142293799
Manga I, Říha H. The DGAT1 gene K232A mutation is associated with milk fat content, milk yield and milk somatic cell count in cattle (Short Communication). Arch Anim Breed. 2011;54:257–63.
doi: 10.5194/aab-54-257-2011
Qanbari S, Pimentel ECG, Tetens J, Thaller G, Lichtner P, Sharifi AR, Simianer H. The pattern of linkage disequilibrium in German Holstein cattle. Anim Genet. 2010;41:346–56.
pubmed: 20055813 doi: 10.1111/j.1365-2052.2009.02011.x
Qanbari S, Pausch H, Jansen S, Somel M, Strom TM, Fries R, et al. Classic selective sweeps revealed by massive sequencing in cattle. PLoS Genet. 2014;10:e1004148.
pubmed: 24586189 pmcid: 3937232 doi: 10.1371/journal.pgen.1004148
Wellmann R, Bennewitz J. Bayesian models with dominance effects for genomic evaluation of quantitative traits. Genet Res (Camb). 2012;94:21–37.
pubmed: 22353246 doi: 10.1017/S0016672312000018
Karaman E, Cheng H, Firat MZ, Garrick DJ, Fernando RL. An upper bound for accuracy of prediction using GBLUP. PLoS One. 2016;11:e0161054.
pubmed: 27529480 pmcid: 4986954 doi: 10.1371/journal.pone.0161054
McVean G. The structure of linkage disequilibrium around a selective sweep. Genetics. 2007;175:1395–406.
pubmed: 17194788 pmcid: 1840056 doi: 10.1534/genetics.106.062828
Kim E-S, Kirkpatrick BW. Linkage disequilibrium in the North American Holstein population. Anim Genet. 2009;40:279–88.
pubmed: 19220233 doi: 10.1111/j.1365-2052.2008.01831.x
Gonzalez-Recio O, Daetwyler HD, MacLeod IM, Pryce JE, Bowman PJ, Hayes BJ, Goddard ME. Rare variants in transcript and potential regulatory regions explain a small percentage of the missing heritability of complex traits in cattle. PLoS One. 2015;10:e0143945.
pubmed: 26642058 pmcid: 4671594 doi: 10.1371/journal.pone.0143945
Zhang Q, Calus MPL, Guldbrandtsen B, Lund MS, Sahana G. Contribution of rare and low-frequency whole-genome sequence variants to complex traits variation in dairy cattle. Genet Sel Evol. 2017;49:60.
pubmed: 28764638 pmcid: 5539983 doi: 10.1186/s12711-017-0336-z

Auteurs

Helen Schneider (H)

Institute of Animal Science, University of Hohenheim, 70599, Stuttgart, Germany. helen.schneider@uni-hohenheim.de.

Ana-Marija Krizanac (AM)

Department of Animal Sciences, University of Göttingen, 37077, Göttingen, Germany.

Clemens Falker-Gieske (C)

Department of Animal Sciences, University of Göttingen, 37077, Göttingen, Germany.

Johannes Heise (J)

Vereinigte Informationssysteme Tierhaltung w.V. (VIT), 27283, Verden, Germany.

Jens Tetens (J)

Department of Animal Sciences, University of Göttingen, 37077, Göttingen, Germany.

Georg Thaller (G)

Institute of Animal Breeding and Husbandry, Christian-Albrechts University of Kiel, 24098, Kiel, Germany.

Jörn Bennewitz (J)

Institute of Animal Science, University of Hohenheim, 70599, Stuttgart, Germany.

Classifications MeSH