Derivation and genome-wide association study of a principal component-based measure of heat tolerance in dairy cattle

Journal of Dairy Science

Volumn 100, Issue 6, 2017, Pages 4683-4697

  Macciotta, N P P ^a   Biffani, S ^b   Bernabucci, U ^c   Lacetera, N ^c   Vitali, A ^c   Ajmone Marsan, P ^d   Nardone, A ^c  

^a UNIVERSITY OF SASSARI   (Italy)

^b Associazione Italiana Allevatori   (Italy)

^c UNIVERSITY OF TUSCIA   (Italy)

^d UNIVERSITÀ CATTOLICA DEL SACRO CUORE   (Italy)

Author keywords

dairy cattle; genome wide association study; heat tolerance; heritability; principal component analysis

Indexed keywords

CALCIUM CHANNEL; GLYCOLIPID; GLYCOPROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; MILK FAT GLOBULE; MILK PROTEIN; VANILLOID RECEPTOR;

ANIMAL; BOVINE; BREEDING; FEMALE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HEAT TOLERANCE; ITALY; LACTATION; MALE; MILK; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; SECRETION (PROCESS); SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BREEDING; CALCIUM CHANNELS; CATTLE; FEMALE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; GLYCOLIPIDS; GLYCOPROTEINS; HEAT SHOCK TRANSCRIPTION FACTORS; ITALY; LACTATION; MALE; MILK; MILK PROTEINS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PRINCIPAL COMPONENT ANALYSIS; THERMOTOLERANCE; TRPV CATION CHANNELS;

EID: 85016510454     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2016-12249     Document Type: Article

References (69)

1. Aguilar, I., Misztal, I., Tsuruta, S., Genetic components of heat stress for dairy cattle with multiple lactations. J. Dairy Sci. 92 (2009), 5702–5711 19841230.
2. Aguilar, I., Misztal, I., Tsuruta, S., Short communication: Genetic trends of milk yield under heat stress for US Holsteins. J. Dairy Sci. 93 (2010), 1754–1758 20338455.
3. Ali, A.K.A., Shook, G.E., An optimum transformation for somatic cell concentration in milk. J. Dairy Sci. 63 (1980), 487–490.
4. Amin, N., van Duijn, C.M., Aulchenko, Y.S., A genomic background based method for association analysis in related individuals. PLoS One, 2, 2007, e1274 18060068.
5. Aulchenko, Y.S., Ripke, S., Isaacs, A., van Duijn, C.M., GenABEL: An R package for genome-wide association analysis. Bioinformatics 23 (2007), 1294–1296.
6. Basiricò, L., Morera, P., Primi, V., Lacetera, N., Nardone, A., Bernabucci, U., Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows. Cell Stress Chaperones 16 (2011), 441–448 21274669.
7. Bastin, C., Gengler, N., Soyeurt, H., Phenotypic and genetic variability of production traits and milk fatty acid contents across days in milk for Walloon Holstein first-parity cows. J. Dairy Sci. 94 (2011), 4152–4163 21787950.
8. Bernabucci, U., Biffani, S., Buggiotti, L., Vitali, A., Lacetera, N., Nardone, A., The effect of heat stress in Italian Holstein dairy cattle. J. Dairy Sci. 97 (2014), 471–486 24210494.
9. Bernabucci, U., Lacetera, L.H., Baumgard, R.P., Rhoads, B., Ronchi, B., Nardone, A., Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4 (2010), 1167–1183 22444615.
10. Biffani, S., Bernabucci, U., Vitali, A., Lacetera, N., Nardone, A., Short communication: Effect of heat stress on nonreturn rate of Italian Holstein cows. J. Dairy Sci. 99 (2016), 5837–5843 27108174.
11. Bohmanova, J., Misztal, I., Tsuruta, S., Norman, H.D., Lawlor, T.J., Short communication: Genotype by Environment Interaction Due to Heat Stress. J. Dairy Sci. 91 (2008), 840–846 18218772.
12. Brügemann, K., Gernand, E., von Borstel, U.U., König, S., Genetic analyses of protein yield in dairy cows applying random regression models with time-dependent and temperature x humidity-dependent covariates. J. Dairy Sci. 94 (2011), 4129–4139 21787948.
13. Buitenhuis, B., Janss, L.L.G., Poulsen, N.A., Larsen, L.B., Larsen, M.K., Sørensen, P., Genome-wide association and biological pathway analysis for milk-fat composition in DanishHolstein and Danish Jersey cattle. BMC Genomics, 15, 2014, 1112 25511820.
14. Capomaccio, S., Milanesi, M., Bomba, L., Cappelli, K., Nicolazzi, E.L., Williams, J.L., Ajmone-Marsan, P., Stefanon, B., Searching new signals for production traits through gene-based association analysis in three Italian cattle breeds. Anim. Genet. 46 (2015), 361–370 25997511.
15. Carabaño, M.J., Bachaga, K., Ramon, M., Diaz, C., Modeling heat stress effect on Holstein cows under hot and dry conditions: selection tools. J. Dairy Sci. 97 (2014), 7889–7904 25262182.
16. Carabaño, M.J., Logar, B., Bormann, J., Minet, J., Vanrobays, M.L., Diaz, C., Tychon, B., Gengler, N., Hammami, H., Modeling heat stress under different environmental conditions. J. Dairy Sci. 99 (2016), 3798–3814 26923054.
17. Cole, J.B., Wiggans, G.R., Ma, L., Sonstegard, T.S., Lawlor, T.J. Jr., Crooker, B.A., Van Tassell, C.P., Yang, J., Wang, S., Matukumalli, L.K., Da, Y., Genome-wide association analysis of thirty one production, health, reproduction and body conformation traits in contemporary U.S. Holstein cows. BMC Genomics, 12, 2011, 408 21831322.
18. Collier, R.J., Collier, J.L., Rhoads, R.P., Baumgard, L.H., Invited review: Genes involved in the bovine heat stress response. J. Dairy Sci. 91 (2008), 445–454 18218730.
19. Dikmen, S., Cole, J.B., Null, D.J., Hansen, P.J., Heritability of rectal temperature and genetic correlations with production and reproduction traits in dairy cattle. J. Dairy Sci. 95 (2012), 3401–3405 22612974.
20. Dikmen, S., Cole, J.B., Null, D.J., Hansen, P.J., Genome-wide association mapping for identification of quantitative trait loci for rectal temperature during heat stress in Holstein cattle. PLoS One, 8, 2013, e69202 23935954.
21. Dikmen, S., Wang, X.Z., Ortega, M.S., Cole, J.B., Null, D.J., Hansen, P.J., Single nucleotide polymorphisms associated with thermoregulation in lactating dairy cows exposed to heat stress. J. Anim. Breed. Genet. 132 (2015), 409–419 26198991.
22. Fontanesi, L., Calò, D.G., Galimberti, G., Negrini, R., Marino, R., Nardone, A., Ajmone-Marsan, P., Russo, V., A candidate gene association study for nine production traits in Italian Holstein sires. Anim. Genet. 45 (2014), 576–580 24796806.
23. Garner, J.B., Douglas, M.L., Williams, S.R.O., Wales, W.J., Marett, L.C., Nguyen, T.T.T., Reich, C.M., Hayes, B.J., Genomic selection improves heat tolerance in dairy cattle. Sci. Rep., 2016 10.1038/srep34114.
24. Grisart, B., Coppieters, W., Farnir, F., Karim, L., Ford, C., Berzi, P., Cambisano, N., Mni, M., Reid, S., Simon, P., Spelman, R., Georges, M., Snell, R., 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 (2002), 222–231 11827942.
25. Guettouche, T., Boellmann, F., Lane, W.S., Voellmy, R., Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem., 6, 2005, 4 10.1186/1471-2091-6-4 15760475.
26. Gusev, A., Bhatia, G., Zaitien, N., Vilhjalmsson, B.J., Diogo, D., Stahl, E.A., Gregersen, P.K., Worthington, J., Klareskog, L., Rayachaudhri, S., Plenge, R.M., Pasanius, B., Price, A.L., Quantifying missing heritability at known GWAS loci. PLoS Genet., 9, 2013, e1003993 24385918.
27. Hammami, H., Vandenplas, J., Vanrobays, M.-L., Rekik, B., Bastin, C., Gengler, N., Genetic analysis of heat stress effects on yield traits, udder health, and fatty acids of Walloon Holstein cows. J. Dairy Sci. 98 (2015), 4956–4968 25958288.
28. Hansen, P.J., Exploitation of genetic and physiological determinants of embryonic resistance to elevated temperature to improve embryonic survival in dairy cattle during heat stress. Theriogenology 68 (2007), S242–S249 17482669.
29. Hatzirodos, N., Irving-Rodgers, H.F., Hummitzsch, K., Harland, M.L., Morris, S.E., Rodgers, R.J., Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes. BMC Genomics, 15, 2014, 24 24422759.
30. Hayes, B.J., Bowman, P.J., Chamberlain, A.J., Savin, K., van Tassell, C.P., Sostengard, T.S., Goddard, M.E., A validated genome wide association study to breed cattle adapted to an environment altered by climate changes. PLoS One, 4, 2009, e6676 19688089.
31. Jiang, L., Liu, X., Yang, J., Wang, H., Jiang, J., Liu, L., He, S., Ding, X., Liu, J., Zhang, Q., Targeted resequencing of GWAS loci reveals novel genetic variants for milk production traits. BMC Genomics, 15, 2014, 1105 25510969.
32. Kadzere, C.T., Murphy, M.R., Silanikove, N., Maltz, E., Heat stress in lactating dairy cows: a review. Livest. Prod. Sci. 77 (2002), 59–91.
33. Katz, M.J., Gandara, L., De Lella Ezcurra, A.L., Wappner, P., Hydroxylation and translational adaptation to stress: Some answers lie beyond the STOP codon. Cell. Mol. Life Sci. 73 (2016), 1881–1893 26874685.
34. Kelly, C.F., Bond, T.E., Bioclimatic factors and their measurements. A Guide to Environmental Research in Animals, 1971, Natl. Acad. Sci., Washington, DC, 7.
35. Kemper, K.E., Saxton, S.J., Bolormaa, S., Hayes, B.J., Goddard, M.E., Document selection for complex traits leaves little or no classic signatures of selection. BMC Genomics, 15, 2014, 246 24678841.
36. Kitamoto, T., Kitamoto, A., Yoneda, M., Hyogo, H., Ochi, H., Nakamura, T., Teranishi, H., Mizusawa, S., Ueno, T., Chayama, K., Nakajima, A., Nakao, K., Sekine, A., Hotta, K., Genome-wide scan revealed that polymorphisms in the PNPLA3, SAMM50, and PARVB genes are associated with development and progression of nonalcoholic fatty liver disease in Japan. Hum. Genet. 132 (2013), 783–792 23535911.
37. Kolmodin, R., Bijma, P., Response to mass selection when the genotype by environment interaction is modeled as a linear reaction norm. Genet. Sel. Evol. 36 (2004), 435–454 15231233.
38. Kumar, A., Ashrafa, S., Sridhar Gouda, T., Grewalc, A., Singha, S.V., Yadavb, B.R., Upadhyaya, R.C., Expression profiling of major heat shock protein genes during different seasons in cattle (Bos indicus) and buffalo (Bubalus bubalis) under tropical climatic condition. J. Therm. Biol. 51 (2015), 55–64 25965018.
39. Li, Q.L., Ju, Z.H., Huang, J.M., Li, J.B., Li, R.L., Hou, M.H., Wang, C.F., Zhong, J.F., Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle. DNA Cell Biol. 30 (2011), 247–254 21189066.
40. Loyau, T., Hennequet-Antier, C., Coustham, V., Berri, C., Leduc, M., Crochet, S., Sannier, M., Duclos, M.J., Mignon-Grasteau, S., Tesseraud, S., Brionne, A., Métayer-Coustard, S., Moroldo, M., Lecardonnel, J., Martin, P., Lagarrigue, S., Yahav, S., Collin, A., Thermal manipulation of the chicken embryo triggers differential gene expression in response to a later heat challenge. BMC Genomics, 17, 2016, 329 27142519.
41. Ma, S., Nowak, F.V., The RhoGAP domain-containing protein, Porf-2, inhibits proliferation and enhances apoptosis in neural stem cells. Mol. Cell. Neurosci. 46 (2011), 573–582 21185940.
42. Macciotta, N.P.P., Gaspa, G., Bomba, L., Vicario, D., Dimauro, C., Cellesi, M., Ajmone-Marsan, P., Genome-wide association analysis in Italian Simmental cows for lactation curve traits using a low-density (7K) SNP panel. J. Dairy Sci. 98 (2015), 8175–8185 26387014.
43. Macciotta, N.P.P., Vicario, D., Cappio-Borlino, A., Use of multivariate analysis to extract latent variables related to level of production and lactation persistency in dairy cattle. J. Dairy Sci. 89 (2006), 3188–3194 16840636.
44. Misztal, I., Tsuruta, S., Strabel, T., Auvray, B., Druet, T., Lee, D.H., BLUPF90 and related programs (BGF90). Proceedings of the 7th World Congress on Genetics Applied to Livestock Production, Montpellier, France, 2002, INRA, France, 743–744.
45. Nardone, A., Lacetera, N., Bernabucci, U., Ronchi, B., Composition of colostrum from dairy heifers exposed to high air temperatures during late pregnancy and the early postpartum period. J. Dairy Sci. 80 (1997), 838–844 9178123.
46. Nardone, A., Ronchi, B., Lacetera, N., Ranieri, M.S., Bernabucci, U., Effects of climate changes on animal production and sustainability of livestock systems. Livest. Sci. 130 (2010), 57–69.
47. Nayeri, S., Sargolzaei, M., Abo-Ismail, M.K., May, N., Miller, S.P., Schenkel, F., Moore, S.S., Stothard, P., Genome-wide association for milk production and female fertility traits in Canadian dairy Holstein cattle. BMC Genet., 17, 2016, 75 27287773.
48. Newton, J.R., De Santis, C., Jerry, D.R., The gene expression response of the catadromous perciform barramundi Latescalcarifer to an acute heat stress. J. Fish Biol. 81 (2012), 81–93 22747805.
49. Nguyen, T.T.T., Bowman, P.J., Haile-Mariam, M., Pryce, J.E., Hayes, B.J., Genomic selection for tolerance to heat stress in Australian dairy cattle. J. Dairy Sci. 99 (2016), 2849–2862 27037467.
50. Perano, K.M., Usack, J.G., Angenent, L.T., Gebremedhin, K.G., Production and physiological responses of heat-stressed lactating dairy cattle to conductive cooling. J. Dairy Sci. 98 (2015), 5252–5261 26074243.
51. Ravagnolo, O., Misztal, I., Genetic component of heat stress in dairy cattle, parameter estimation. J. Dairy Sci. 83 (2000), 2126–2130.
52. Raven, L.A., Cocks, B.G., Hayes, B.J., Multibreed genome wide association can improve precision of mapping causative variants underlying milk production in dairy cattle. BMC Genomics, 15, 2014, 62.
53. Raven, L.A., Cocks, B.G., Kemper, K.E., Chamberlain, A.J., Goddard, M.E., Hayes, B.J., Targeted imputation of sequence variants and gene expression profiling identifies twelve candidate genes associated with lactation volume, composition and calving interval in dairy cattle. Mamm. Genome 27 (2016), 81–97.
54. Richardson, I.W., Berry, D.P., Wiencko, H.L., Higgins, I.M., More, S.J., McClure, J., Lynn, D.J., Bradley, D.G., A genome-wide association study for genetic susceptibility to Mycobacterium bovis infection in dairy cattle identifies a susceptibility QTL on chromosome 23. Genet. Sel. Evol., 48, 2016, 19 26960806.
55. Saatchi, M., Schnabel, R.D., Taylor, J.F., Garrick, D.J., Large-effect pleiotropic or closely linked QTL segregate within and across ten US cattle breeds. BMC Genomics 15 (2014), 442–458 24906442.
56. Sánchez, J.P., Misztal, I., Aguilar, I., Zumbach, B., Rekaya, R., Genetic determination of the onset of heat stress on daily milk production in the US Holstein cattle. J. Dairy Sci. 92 (2009), 4035–4045 19620687.
57. Santana, M.L., Bignardi, A.B., Pereira, R.J., Stefani, G., El Faro, L., Genetics of heat tolerance for milk yield and quality in Holsteins. Animal 11 (2017), 4–14 10.1017/S1751731116001725 27532229.
58. SAS Institute, SAS/STAT version 9.2, 2008, SAS Inst. Inc., Cary, NC.
59. Segnalini, M., Nardone, A., Bernabucci, U., Vitali, A., Ronchi, B., Lacetera, N., Dynamics of the temperature-humidity index in the Mediterranean basin. Int. J. Biometeorol. 55 (2011), 253–263 20524014.
60. Shahzad, K., Akbar, H., Vailati-Riboni, M., Basiricò, L., Morera, P., Rodriguez-Zas, S.L., Nardone, A., Bernabucci, U., Loor, J.J., The effect of calving in the summer on the hepatic transcriptome of Holstein cows during the peripartal period. J. Dairy Sci. 98 (2015), 5401–5413 26074246.
61. Shariati, M.M., Su, G., Madsen, P., Sorensen, D., Analysis of milk production traits in early lactation using a reaction norm model with unknown covariates. J. Dairy Sci. 90 (2007), 5759–5766 18024770.
62. Sturm, R.A., Duffy, D.L., Human pigmentation genes under environmental selection. Genome Biol., 13, 2012, 248 23110848.
63. Tizioto, P.C., Taylor, J.F., Decker, J.E., Gromboni, C.F., Mudadu, M.A., Schnabel, R.D., Coutinho, L.L., Mourão, G.B., Oliveira, P.S.N., Souza, M.M., Reecy, J.M., Nassu, R.T., Bressani, F.A., Tholon, P., Sonstegard, T.S., Alencar, M.M., Tullio, R.R., Nogueira, A.R.A., Regitano, L.C.A., Detection of quantitative trait loci for mineral content of Nelore longissimus dorsi muscle. Genet. Sel. Evol., 47, 2015, 15 25880074.
64. van den Berg, I., Fritz, S., Rodriguez, S., Rocha, D., Boussaha, M., Lund, M.S., Boichard, D., Concordance analysis for QTL detection in dairy cattle: A case study of leg morphology. Genet. Sel. Evol., 46, 2014, 31 24884971.
65. Wang, X., Ma, P., Liu, J., Zhang, Q., Zhang, Y., Ding, X., Jiang, L., Wang, Y., Zhang, Y., Sun, D., Zhang, S., Su, G., Yu, Y., Genome-wide association study in Chinese Holstein cows reveal two candidate genes for somatic cell score as an indicator for mastitis susceptibility. BMC Genet., 16, 2015, 111 26370837.
66. Wang, X., Wurmser, C., Pausch, H., Jung, S., Reinhardt, F., Tetens, J., Thaller, G., Fries, R., Identification and dissection of four major QTL affecting milk fat content in the German Holstein-Friesian population. PLoS One, 7, 2012, e40711 22792397.
67. Zhang, B., Peñagaricano, F., Driver, A., Chen, H., Khatib, H., Differential expression of heat shock protein genes and their splice variants in bovine preimplantation embryos. J. Dairy Sci. 94 (2011), 4174–4182 21787952.
68. Zhang, G.X., Fan, Q.C., Zhang, T., Wang, J.Y., Wang, W.H., Xue, Q., Wang, Y.J., Genome-wide association study of growth traits in the Jinghai Yellow chicken. Genet. Mol. Res. 14 (2015), 15331–15338 26634498.
69. 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., Marçais, G., Roberts, M., Subramanian, P., Yorke, J.A., Salzberg, S.L., A whole-genome assembly of the domestic cow. Genom. Biol., 10, 2009, R42 19393038.