Abstract
Scrotal circumference (SC) is a commonly used trait related to sexual precocity in bulls. Genome-wide association studies have uncovered a lot of genes related to this trait, however, only those present on autosomes. The inclusion of the second biggest chromosome (BTAX) can improve the knowledge of the genetic architecture of this trait. In this study, we performed a weighted, single-step, genome-wide association study using a 777 k BovineHD BeadChip (IllumHD) to analyze the association between SNPs and SC in Brazilian Nelore cattle. Phenotypes from 79,300 males and 3263 genotypes (2017 from females and 1246 from males)—(39,367 SNPs markers located at ChrX) were used. We identified eight regions on chromosome X that displayed important associations with SC. The results showed that together the genomic windows explained 28.52% of the genetic variance for the examined trait. Genes with potential functions in reproduction and fertility regulation were highlighted as candidates for sexual precocity rates in Nelore cattle (AFF2 and PJA1). Moreover, we found 10 genes that had not previously been identified as being associated with sexual precocity traits in cattle. These findings will further advance our understanding of the genetic architecture, considering mainly the presence of the chromosome X, for indicine cattle reproductive traits, being useful in the context of genomic prediction in beef cattle.
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Our research was accomplished using data from commercial farms and Nelore breeding programs that are not publicly available.
References
Bourdon RM, Brinks JS (1986) Scrotal circumference in yearling Hereford bulls: adjustment factors, heritabilities and genetic, environmental and phenotypic relationships with growth traits. J Anim Sci 62:958–967. https://doi.org/10.2527/jas1986.624958x
Brumatti RC, Ferraz JBS, Eler JP, Formigonni IB (2011) Desenvolvimento de índice de seleção em gado corte sob o enfoque de um modelo bioeconômico. Archivos De Zootecnia 60:205–213. https://doi.org/10.4321/S0004-05922011000200005
Buzanskas ME, Pires PS, Chud TCS et al (2017) Parameter estimates for reproductive and carcass traits in Nelore beef cattle. Theriogenology 92:204–209. https://doi.org/10.1016/j.theriogenology.2016.09.057
Cooke RF, Cardoso RC, Cerri RLA, et al (2020) Cattle adapted to tropical and subtropical environments: genetic and reproductive considerations. J Anim Sci 98. https://doi.org/10.1093/jas/skaa015
Costa RB, Camargo GMF, Diaz ID, Irano N, Dias MM, Carvalheiro R, Albuquerque LG (2015) Genome-wide association study of reproductive traits in Nellore heifers using Bayesian inference. Genet Sel Evol 47:67. https://doi.org/10.1186/s12711-015-0146-0
Couldrey C, Johnson T, Lopdell T et al (2017) Bovine mammary gland X chromosome inactivation. J Dairy Sci 100:5491–5500. https://doi.org/10.3168/jds.2016-12490
de Camargo GMF, Porto-Neto LR, Kelly MJ et al (2015) Non-synonymous mutations mapped to chromosome X associated with andrological and growth traits in beef cattle. BMC Genomics 16:384. https://doi.org/10.1186/s12864-015-1595-0
Formigoni IB, Ferraz JBS, Silva J, AIi V et al (2005) Valores econômicos para habilidade de permanência e probabilidade de prenhez aos 14 meses em bovinos de corte. Arq Bras Med Vet Zootec 57:220–226. https://doi.org/10.1590/S0102-09352005000800013
Fortes MRS, Reverter A, Hawken RJ, et al (2012) Candidate genes associated with testicular development, sperm quality, and hormone levels of inhibin, luteinizing hormone, and insulin-like growth factor 1 in Brahman bulls. Biol Reprod 87. https://doi.org/10.1095/biolreprod.112.101089
Irano N, de Camargo GMF, Costa RB et al (2016) Genome-wide association study for indicator traits of sexual precocity in Nellore cattle. PLoS ONE 11:e0159502. https://doi.org/10.1371/journal.pone.0159502
Johnson T, Keehan M, Harland C et al (2019) Short communication: identification of the pseudoautosomal region in the Hereford bovine reference genome assembly ARS-UCD1.2. J Dairy Sci 102:3254–3258. https://doi.org/10.3168/jds.2018-15638
Legarra A, Aguilar I, Misztal I (2009) A relationship matrix including full pedigree and genomic information. J Dairy Sci 92:4656–4663. https://doi.org/10.3168/jds.2009-2061
Legarra A, Christensen OF, Aguilar I, Misztal I (2014) Single Step, a general approach for genomic selection. Livest Sci 166:54–65. https://doi.org/10.1016/j.livsci.2014.04.029
Lyons RE, Loan NT, Dierens L et al (2014) Evidence for positive selection of taurine genes within a QTL region on chromosome X associated with testicular size in Australian Brahman cattle. BMC Genet 15:6. https://doi.org/10.1186/1471-2156-15-6
Misztal I (2020) Fev 20. BLUPF90 - a flexible mixed model program in Fortran 90. University of Georgia Retrieved from. http://nce.ads.uga.edu/wiki/lib/exe/fetch.php?media=blupf90.pdf.
Nilsson E, Zhang B, Skinner MK (2013) Gene bionetworks that regulate ovarian primordial follicle assembly. BMC Genomics 14:496. https://doi.org/10.1186/1471-2164-14-496
Pravia MI, Ravagnolo O, Urioste JI, Garrick DJ (2014) Identification of breeding objectives using a bioeconomic model for a beef cattle production system in Uruguay. Livest Sci 160:21–28. https://doi.org/10.1016/j.livsci.2013.12.006
Sanchez M-P, Ramayo-Caldas Y, Wolf V et al (2019) Sequence-based GWAS, network and pathway analyses reveal genes co-associated with milk cheese-making properties and milk composition in Montbéliarde cows. Genet Sel Evol 51:34. https://doi.org/10.1186/s12711-019-0473-7
Santana ML, Eler JP, Bignardi AB, Ferraz JBS (2015) Two-trait random regression model to estimate the genetic association of scrotal circumference with female reproductive performance in Nelore cattle. Theriogenology 83:1534–1540. https://doi.org/10.1016/j.theriogenology.2015.02.003
Sidorenko J, Kassam I, Kemper KE et al (2019) The effect of X-linked dosage compensation on complex trait variation. Nat Commun 10:3009. https://doi.org/10.1038/s41467-019-10598-y
Van Melis MH, Eler JP, Rosa GJM et al (2010) Additive genetic relationships between scrotal circumference, heifer pregnancy, and stayability in Nellore cattle. J Anim Sci 88:3809–3813. https://doi.org/10.2527/jas.2009-2127
Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. Am J of Human Gen 88(1):76–82. https://doi.org/10.1016/j.ajhg.2010.11.011
Wang H, Misztal I, Aguilar I et al (2012) Genome-wide association mapping including phenotypes from relatives without genotypes. Genetics Research 94:73–83. https://doi.org/10.1017/S0016672312000274
Funding
This project was supported by Bahia Research Support Foundation (FAPESB grant number BOL0543/2016), and by National Council for Scientific and Technological [CNPq grant numbers 422799/2016–5]; São Paulo Research Foundation [FAPESP grant numbers 2009/16118–5].
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ICH, IDPSD, and RBC conceived and designed the experiment. ICH, IDPSD, GMCF, and RBC analyzed the data. ICH, IDPSD, and RBC wrote the manuscript. LGA provided the phenotypes along with genotypes, and revised the manuscript. The authors have read and agreed with the content of the manuscript.
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Communicated by Maciej Szydlowski
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Hermisdorff, I.d., Diaz, I.D., de Camargo, G.M.F. et al. Effect of genomic X-chromosome regions on Nelore bull fertility. J Appl Genetics 62, 655–659 (2021). https://doi.org/10.1007/s13353-021-00645-0
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DOI: https://doi.org/10.1007/s13353-021-00645-0