Novel insights into genome-wide associations in Bos indicus reveal genetic linkages between fertility and growth

References

• Albarrán-Portillo B, Pollott GE. The relationship between fertility and lactation characteristics in Holstein cows on United Kingdom commercial dairy farms. J Dairy Sci. 2013; 96(1):635–646.
   PubMed Web of Science ®Google Scholar
• Sewalem A, Miglior F, Kistemaker GJ, et al. Relationship between reproduction traits and functional longevity in Canadian dairy cattle. J Dairy Sci. 2008;91(4):1660–1668.
   PubMed Web of Science ®Google Scholar
• Liu Z, Jaitner J, Reinhardt F, et al. Genetic evaluation of fertility traits of dairy cattle using a multiple-trait animal model. J Dairy Sci. 2008;91(11):4333–4343.
   PubMed Web of Science ®Google Scholar
• Sun C, Madsen P, Lund MS, et al. Improvement in genetic evaluation of female fertility in dairy cattle using multiple-trait models including milk production traits. J Anim Sci. 2010;88(3):871–878.
   PubMed Web of Science ®Google Scholar
• Waldron DF, Morris CA, Baker RL, et al. Maternal effects for growth traits in beef cattle. Livest Prod Sci. 1993;34(1-2):57–70.
   Google Scholar
• Lopes FB, Magnabosco CU, Paulini F, et al. Genetic analysis of growth traits in polled Nellore cattle raised on pasture in tropical region using Bayesian approaches. PLoS One. 2013;8(9):e75423.
   PubMed Web of Science ®Google Scholar
• Mu Y, Vander Voort G, Abo-Ismail MK, et al. Genetic correlations between female fertility and postweaning growth and feed efficiency traits in multibreed beef cattle. Can J Anim Sci. 2016;96(3):448–455.
   Web of Science ®Google Scholar
• Caetano SL, Savegnago RP, Boligon AA, et al. Estimates of genetic parameters for carcass, growth and reproductive traits in Nellore cattle. Livest Sci. 2013;155(1):1–7.
   Web of Science ®Google Scholar
• Silva AM, Alencar MM, Freitas AR, et al. Heritabilities and genetic correlations for weight and scrotal perimeter of males and reproductive and growth characteristics of females in the Canchim breed. R Bras Zootec. 2000; 29(6):2223–2230.
   Web of Science ®Google Scholar
• Poncheki JK, Canha MLS, Viechnieski SL, et al. Analysis of daily body weight of dairy cows in early lactation and associations withproductive and reproductive performance. R Bras Zootec. 2015;44(5):187–192.
   Web of Science ®Google Scholar
• Frischknecht M, Bapst B, Seefried FR, Intergenomics Consortium, et al. Genome-wide association studies of fertility and calving traits in Brown Swiss cattle using imputed whole-genome sequences. BMC Genomics. 2017;18(1):1–13.
   PubMedGoogle Scholar
• Terakado APN, Costa RB, De Camargo GMF, et al. Genome-wide association study for growth traits in Nelore cattle. Animal. 2018;12(7):1358–1362.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Ober U, Erbe M, et al. Improving the accuracy of whole genome prediction for complex traits using the results of genome wide association studies. PLoS One. 2014;9(3):e93017.
   PubMed Web of Science ®Google Scholar
• Khan MS, Rehman Z, Khan MA, et al. Genetic resources and diversity in Pakistani cattle. Pak Vet J. 2008;28(2):95–102.
   Web of Science ®Google Scholar
• Breed survey. 2013. Estimated Livestock Population breed-wise. Ministry of Agriculture and Farmers Welfare, Department of Animal Husbandry, Dairying and Fisheries, Government of India.
   Google Scholar
• Joshi BK, Singh A, Gandhi RS. Performance evaluation, conservation and improvement of Sahiwal cattle in India. Anim Genet Resour Inf. 2001; 31:43–54.
   Google Scholar
• Hemme T, Garcia O, Saha A. A review of milk production in India with particular emphasis on small-scale producers. FAO,PPLPI Work Pap No2 20031-58. 2003
   Google Scholar
• Ratwan P, Chakravarty AK, Kumar M, et al. Production performance and estimation of genetic parameters of production traits in Sahiwal cattle. Ind J Dairy Sci. 2018;71(6):592–597.
   Web of Science ®Google Scholar
• Ratwan P, Chakravarty AK, Kumar M. Assessment of relation among production and reproduction traits in Sahiwal cattle at an organized herd of northern India. Biol Rhythm Res. 2019; doi:10.1080/09291016.2019.1628391
   PubMed Web of Science ®Google Scholar
• Sambrook J, Russell DW. Rapid isolation of yeast DNA. Cold Spring Harb Protoc. 2006;doi:10.1101/pdb.prot4039.
   Google Scholar
• https://www.nddb.coop/services/animalbreeding/geneticimprovement/genomic. Last accessed on 09-04-2020
   Google Scholar
• Purcell S, Chang C. PLINK 1.9. www.cog-genomics.org/plink/1.9/. Last accessed on 09-04-2020
   Google Scholar
• Chang CC, Chow CC, Tellier LC, et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015; 4(1):7–015.
   PubMedGoogle Scholar
• Villemereuil P. On the relevance of Bayesian statistics and MCMC for animal models. J Anim Breed Genet. 2019;136(5):339–340.
   PubMed Web of Science ®Google Scholar
• Van De Schoot R, Broere JJ, Perryck KH, et al. Analyzing small data sets using Bayesian estimation: The case of posttraumatic stress symptoms following mechanical ventilation in burn survivors. Eur J Psychotraumatol. 2015;6(1):25216.
   PubMed Web of Science ®Google Scholar
• Hadfield JD. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw. 2010;33(2):1–22.
   PubMed Web of Science ®Google Scholar
• Meyer K. WOMBAT—A tool for mixed model analyses in quantitative genetics by restricted maximum likelihood (REML. ).J Zhejiang Univ Sci B. 2007;8(11):815–821.
   PubMedGoogle Scholar
• Zhang Z, Ersoz E, Lai CQ, et al. Mixed linear model approach adapted for genome-wide association studies. Nat Genet. 2010;42(4):355–360.
   PubMed Web of Science ®Google Scholar
• Lipka AE, Tian F, Wang Q, et al. GAPIT: genome association and prediction integrated tool. Bioinformatics. 2012;28(18):2397–2399.
   PubMed Web of Science ®Google Scholar
• https://github.com/sahirbhatnagar/manhattanly/. last accessed on 10-04-2020
   Google Scholar
• Meredith B, Lynn D, Berry D, et al. A genome-wide association study for somatic cell score using the Illumina high-density bovine beadchip identifies several novel QTL potentially related to mastitis susceptibility. Front Genet. 2013;4:229.
   PubMedGoogle Scholar
• Kurz JP, Yang Z, Weiss RB, et al. A genome-wide association study for mastitis resistance in phenotypically well-characterized Holstein dairy cattle using a selective genotyping approach. Immunogenetics. 2019;71(1):35–47.
   PubMed Web of Science ®Google Scholar
• https://www.animalgenome.org/cgi-bin/QTLdb/BT/index. last accessed on 01-09-2020
   Google Scholar
• Zimin AV, Delcher AL, Florea L, et al. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 2009;10(4):R42.
   PubMed Web of Science ®Google Scholar
• https://genome.ucsc.edu/. Last accessed on 10-04-2020
   Google Scholar
• Szkiba D, Kapun M, von Haeseler A, et al. SNP2GO: functional analysis of genome-wide association studies. Genetics. 2014;197(1):285–289.
   PubMed Web of Science ®Google Scholar
• Baruch-Suchodolsky R, Fischer B. Abeta40, either soluble or aggregated, is a remarkably potent antioxidant in cell-free oxidative systems. Biochemistry. 2009;48(20):4354–4370.
   PubMed Web of Science ®Google Scholar
• Ruder EH, Hartman TJ, Goldman MB. Impact of oxidative stress on female fertility. Curr Opin Obstet Gynecol. 2009;21(3):219–222.
   PubMed Web of Science ®Google Scholar
• Nakano FY, Leão RDBF, Esteves SC. Insights into the role of cervical mucus and vaginal pH in unexplained infertility. Med Express. 2015;2(2):1–8.
   Google Scholar
• Guo D, Li S, Behr B, et al. Hypertension and male fertility. World J Mens Health. 2017; 35(2):59–64.
   PubMedGoogle Scholar
• Nobles CJ, Mendola P, Mumford SL, et al. Preconception blood pressure levels and reproductive outcomes in a prospective cohort of women attempting pregnancy. Hypertension. 2018;71(5):904–910.
   PubMed Web of Science ®Google Scholar
• Garcia-Segura LM, Lorenz B, DonCarlos LL. The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction. 2008;135(4):419–429.
   PubMed Web of Science ®Google Scholar
• Li Z, Palaniyandi S, Zeng R, et al. Transfer of IgG in the female genital tract by MHC class I-related neonatal Fc receptor (FcRn) confers protective immunity to vaginal infection. Proc Natl Acad Sci U S A. 2011;108(11):4388–4393.
   PubMed Web of Science ®Google Scholar
• Lyons RA, Saridogan E, Djahanbakhch O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update. 2006;12(4):363–372.
   PubMed Web of Science ®Google Scholar
• Girardet L, Augière C, Asselin MP, et al. Primary cilia: biosensors of the male reproductive tract. Andrology. 2019; 7(5):588–602.
   PubMed Web of Science ®Google Scholar
• Vordermeier M, Ameni G, Berg S, et al. The influence of cattle breed on susceptibility to bovine tuberculosis in Ethiopia. Comp Immunol Microbiol Infect Dis. 2012;35(3):227–232.
   PubMed Web of Science ®Google Scholar
• Manoj M, Gandhi RS, Raja TV, et al. Genetic parameters of body weights at different ages in Sahiwal heifers. Ind Jour of Anim Rese. 2014;48(3):217–220.
   Web of Science ®Google Scholar
• Sundrum A. Metabolic disorders in the transition period indicate that the dairy Cows' Ability to Adapt is Overstressed. Animals (Basel)). 2015;5(4):978–1020.
   PubMedGoogle Scholar
• Pascottini OB, Probo M, LeBlanc SJ, et al. Assessment of associations between transition diseases and reproductive performance of dairy cows using survival analysis and decision tree algorithms. Prev Vet Med. 2020;176:104908.
   PubMed Web of Science ®Google Scholar
• McNeish D. On using Bayesian methods to address small sample problems. Struct Equ Model. 2016;23(5):750–773.
   Web of Science ®Google Scholar
• Seidel GE. Brief introduction to whole-genome selection in cattle using single nucleotide polymorphisms. Reprod Fertil Dev. 2010;22(1):138–144.
   PubMed Web of Science ®Google Scholar
• Yodklaew P, Koonawootrittriron S, Elzo MA, et al. Genome-wide association study for lactation characteristics, milk yield and age at first calving in a Thai multibreed dairy cattle population. Agric Nat Resour. 2017; 51(3):223–230.
   Google Scholar
• Schmid M, Bennewitz J. Invited review: Genome-wide association analysis for quantitative traits in livestock–a selective review of statistical models and experimental designs. Arch Anim Breed. 2017;60(3):335–346.
   Web of Science ®Google Scholar
• Joo JWJ, Hormozdiari F, Han B, et al. Multiple testing correction in linear mixed models. Genome Biol. 2016;17(1):1–18.
   PubMedGoogle Scholar
• Qanbari S. On the extent of linkage disequilibrium in the genome of farm animals. Front Genet. 2020;10(1304):1–11.
   Google Scholar
• Fadista J, Manning AK, Florez JC, et al. The (in) famous GWAS P-value threshold revisited and updated for low-frequency variants. Eur J Hum Genet. 2016;24(8):1202–1205.
   PubMed Web of Science ®Google Scholar
• Kaler AS, Purcell LC. Estimation of a significance threshold for genome-wide association studies. BMC Genomics. 2019;20(1):618.
   PubMedGoogle Scholar
• Caballero A, Tenesa A, Keightley PD. The nature of genetic variation for complex traits revealed by GWAS and regional heritability mapping analyses. Genetics. 2015;201(4):1601–1613.
   PubMed Web of Science ®Google Scholar
• Martínez R, Bejarano D, Gómez Y, et al. Genome-wide association study for birth, weaning and yearling weight in Colombian Brahman cattle. Genet Mol Biol. 2017;40(2):453–459.
   PubMed Web of Science ®Google Scholar
• Kamal MM, Van Eetvelde M, Depreester E, et al. Age at calving in heifers and level of milk production during gestation in cows are associated with the birth size of Holstein calves. J Dairy Sci. 2014;97(9):5448–5458.
   PubMed Web of Science ®Google Scholar
• Hoffman PC, Funk DA. Applied dynamics of dairy replacement growth and management. J Dairy Sci. 1992;75(9):2504–2516.
   Web of Science ®Google Scholar
• Almeida TP, Kern EL, Daltro DDS, et al. Genetic associations between reproductive and linear-type traits of Holstein cows in Brazil. R Bras Zootec. 2017;46(2):91–98.
   Web of Science ®Google Scholar
• Cole JB, Gaddis KP, Null DJ, et al. Genome-wide association study and gene network analysis of fertility, retained placenta, and metritis in US Holstein cattle. In World. 2018;1:171
   Google Scholar
• Mota LF, Lopes FB, Júnior GAF, et al. Genome-wide scan highlights the role of candidate genes on phenotypic plasticity for age at first calving in Nellore heifers. Sci Rep. 2020;10(1):1–13.
   PubMed Web of Science ®Google Scholar
• Gutman GA, Chandy KG, Grissmer S, et al. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev. 2005;57(4):473–508.
   PubMed Web of Science ®Google Scholar
• Yang S, Zhou X, Pei Y, et al. Identification of differentially expressed genes in porcine ovaries at proestrus and estrus stages using RNA-Seq technique. Biomed Res Int. 2018;2018:9150723
   PubMed Web of Science ®Google Scholar
• Brązert M, Kranc W, Celichowski P, et al. Expression of genes involved in neurogenesis, and neuronal precursor cell proliferation and development: Novel pathways of human ovarian granulosa cell differentiation and transdifferentiation capability in vitro. Mol Med Rep. 2020; 21(4):1749–1760.
   PubMed Web of Science ®Google Scholar
• Pegolo S, Cecchinato A, Mele M, et al. Effects of candidate gene polymorphisms on the detailed fatty acids profile determined by gas chromatography in bovine milk. J Dairy Sci. 2016;99(6):4558–4573.
   PubMed Web of Science ®Google Scholar
• Han B, Yuan Y, Liang R, et al. Genetic effects of LPIN1 polymorphisms on milk production traits in dairy cattle. Genes. 2019;10(4):265.
   PubMed Web of Science ®Google Scholar
• Rahbar R, Abdullahpour R, Sefidmazgi AS. Effect of calf birth weight on milk production of Holstein dairy cattle in desert climate. JABB. 2016;4(3):65–70.
   Google Scholar
• Hodgkinson K, Forrest LA, Vuong N, Garson K, Djordjevic B, Vanderhyden BC. GREB1 is an estrogen receptor-regulated tumour promoter that is frequently expressed in ovarian cancer. Oncogene. 2018;37(44):5873–5886.
   PubMed Web of Science ®Google Scholar
• Espetvedt Finstad S, Emaus A, Potischman N, et al. Influence of birth weight and adult body composition on 17β-estradiol levels in young women. Cancer Causes Control. 2009;20(2):233–242.
   PubMed Web of Science ®Google Scholar
• Zhang L, Liu J, Zhao F, et al. Genome-wide association studies for growth and meat production traits in sheep. PLoS One. 2013;8(6):e66569.
   PubMed Web of Science ®Google Scholar
• Le TH, Christensen OF, Nielsen B, et al. Genome-wide association study for conformation traits in three Danish pig breeds. Genet Sel Evol. 2017;49(1):12.
   PubMedGoogle Scholar
• Neupane M, Geary TW, Kiser JN, et al. Loci and pathways associated with uterine capacity for pregnancy and fertility in beef cattle. PLoS One. 2017;12(12):e0188997.
   PubMed Web of Science ®Google Scholar
• Silva BA, Eler JP, Santana ML, Jr, et al. Genetic association between mature weight and early growth and heifer pregnancy traits in Nellore cattle. Livest Sci. 2018;211:61–65.
   Web of Science ®Google Scholar
• Yamamoto RT, Nogi Y, Dodd JA, et al. RRN3 gene of Saccharomyces cerevisiae encodes an essential RNA polymerase I transcription factor which interacts with the polymerase independently of DNA template. Embo J. 1996;15(15):3964–3973.
   PubMed Web of Science ®Google Scholar
• Roohani N, Hurrell R, Kelishadi R, et al. Zinc and its importance for human health: An integrative review. J Res Med Sci. 2013;18(2):144–157.
   PubMed Web of Science ®Google Scholar
• Tizioto PC, Meirelles SL, Veneroni GB, et al. A SNP in ASAP1 gene is associated with meat quality and production traits in Nelore breed. Meat Sci. 2012;92(4):855–857.
   PubMed Web of Science ®Google Scholar
• Serão NV, Gonzalez-Pena D, Beever JE, et al. Bivariate genome-wide association analysis of the growth and intake components of feed efficiency. PLoS One. 2013;8(10):e78530.
   PubMed Web of Science ®Google Scholar
• Guan D, Luo N, Tan X, et al. Scanning of selection signature provides a glimpse into important economic traits in goats (Capra hircus). Sci Rep. 2016;6:36372.
   PubMed Web of Science ®Google Scholar
• Moon DH, Segal M, Boyraz B, et al. Poly (A)-specific ribonuclease (PARN) mediates 3′-end maturation of the telomerase RNA component. Nat Genet. 2015;47(12):1482–1488.
   PubMed Web of Science ®Google Scholar
• Welendorf C, Nicoletti CF, de Souza Pinhel MA, et al. Obesity, weight loss, and influence on telomere length: New insights for personalized nutrition. Nutrition. 2019;66:115–121.
   PubMed Web of Science ®Google Scholar
• Doyle JL, Berry DP, Veerkamp RF, et al. Genomic regions associated with muscularity in beef cattle differ in five contrasting cattle breeds. Genet Sel Evol. 2020;52(1):2.
   PubMed Web of Science ®Google Scholar
• Fonseca LFS, Gimenez DFJ, dos Santos Silva DB, et al. Differences in global gene expression in muscle tissue of Nellore cattle with divergent meat tenderness. BMC Genomics. 2017;18(1):1–12.
   PubMedGoogle Scholar
• Riihonen R, Supuran CT, Parkkila S, et al. Membrane-bound carbonic anhydrases in osteoclasts. Bone. 2007;40(4):1021–1031.
   PubMed Web of Science ®Google Scholar
• Montfort A, Martin PG, Levade T, et al. FAN (factor associated with neutral sphingomyelinase activation), a moonlighting protein in TNF-R1 signaling. J Leukoc Biol. 2010;88(5):897–903.
   PubMed Web of Science ®Google Scholar
• Smith JL, Wilson ML, Nilson SM, et al. Genome-wide association and genotype by environment interactions for growth traits in US Gelbvieh cattle. BMC Genomics. 2019;20(1):926.
   PubMed Web of Science ®Google Scholar
• Ramayo-Caldas Y, Mármol-Sánchez E, Ballester M, et al. Integrating genome-wide co-association and gene expression to identify putative regulators and predictors of feed efficiency in pigs. Genet Sel Evol. 2019;51(1):48.
   PubMed Web of Science ®Google Scholar
• Atorino ES, Hata S, Funaya C, et al. CEP44 ensures the formation of bona fide centriole wall, a requirement for the centriole-to-centrosome conversion. Nat Commun. 2020;11(1):1–15.
   PubMed Web of Science ®Google Scholar
• Wang X, Li N, Liu B, et al. A novel human phosphatidylethanolamine-binding protein resists tumor necrosis factor alpha-induced apoptosis by inhibiting mitogen-activated protein kinase pathway activation and phosphatidylethanolamine externalization. J Biol Chem. 2004;279(44):45855–45864.
   PubMed Web of Science ®Google Scholar
• Wu MH, Rajkovic A, Burns KH, et al. Sequence and expression of testis-expressed gene 14 (Tex14): a gene encoding a protein kinase preferentially expressed during spermatogenesis. Gene Expr Patterns. 2003;3(2):231–236.
   PubMed Web of Science ®Google Scholar
• Stafuzza NB, Costa e Silva EVD, Silva RMDO, et al. Genome‐wide association study for age at puberty in young Nelore bulls. J Anim Breed Genet. 2020;137(2):234–244.
   PubMed Web of Science ®Google Scholar
• Taylor JF, Schnabel RD, Sutovsky P. Review: Genomics of bull fertility. Animal. 2018;12(s1):s172–s183.
   PubMedGoogle Scholar
• Liu Y, Tarsounas M, O'regan P, West SC. Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J Biol Chem. 2007;282(3):1973–1979.
   PubMed Web of Science ®Google Scholar
• Alayev A, Salamon RS, Manna S, Schwartz NS, Berman AY, Holz MK. Estrogen induces RAD51C expression and localization to sites of DNA damage. Cell Cycle. 2016;15(23):3230–3239.
   PubMed Web of Science ®Google Scholar
• http://www.fao.org/3/x6533e/x6533e01.htm. last accessed on 24-04-2020
   Google Scholar
• Wang P, Drackley JK, Stamey-Lanier JA, Keisler D, Loor JJ. Effects of level of nutrient intake and age on mammalian target of rapamycin, insulin, and insulin-like growth factor-1 gene network expression in skeletal muscle of young Holstein calves. J Dairy Sci. 2014;97(1):383–391.
   PubMed Web of Science ®Google Scholar
• Somashekar L, Selvaraju S, Parthipan S, et al. Comparative sperm protein profiling in bulls differing in fertility and identification of phosphatidylethanolamine‐binding protein 4, a potential fertility marker. Andrology. 2017;5(5):1032–1051.
   PubMed Web of Science ®Google Scholar
• Chen Q, Huang B, Zhan J, et al. Whole-genome analyses identify loci and selective signals associated with body size in cattle. J Anim Sci. 2020;98(3):skaa068.
   PubMed Web of Science ®Google Scholar
• Yang X, Wang L, Wang Q, et al. MiR-183 inhibits osteosarcoma cell growth and invasion by regulating LRP6-Wnt/β-catenin signaling pathway. Biochem Biophys Res Commun. 2018;496(4):1197–1203.
   PubMed Web of Science ®Google Scholar
• Liu C, Gao H, Zhai S, Liu B. Molecular characterization, chromosomal localization, expression profile and association analysis with carcass traits of the porcine dickkopf homolog1 gene. Mol Biol Rep. 2011;38(3):1929–1934.
   PubMed Web of Science ®Google Scholar
• Doyle JL, Berry DP, Veerkamp RF, et al. Genomic regions associated with skeletal type traits in beef and dairy cattle are common to regions associated with carcass traits, feed intake and calving difficulty. Front Genet. 2020;11:20.
   PubMed Web of Science ®Google Scholar
• Salilew-Wondim D, Hölker M, Rings F, et al. Depletion of BIRC6 leads to retarded bovine early embryonic development and blastocyst formation in vitro. Reprod Fertil Dev. 2010;22(3):564–579.
   PubMed Web of Science ®Google Scholar