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Genome-wide association analysis reveals genomic regions on Chromosome 13 affecting litter size and candidate genes for uterine horn length in Erhualian pigs

Published online by Cambridge University Press:  14 March 2018

X. Ma ,
P. H. Li ,
M. X. Zhu ,
L. C. He ,
S. P. Sui ,
S. Gao ,
G. S. Su ,
N. S. Ding ,
Y. Huang  and
Z. Q. Lu
...Show all authors
X. Ma
Affiliation:
Institute of Swine Science, Nanjing Agricultural University, Nanjing 210095, China
P. H. Li*
Affiliation:
Institute of Swine Science, Nanjing Agricultural University, Nanjing 210095, China
M. X. Zhu
Affiliation:
Jiangsu Animal Husbandry Station, Nanjing 210036, China
L. C. He
Affiliation:
Institute of Swine Science, Nanjing Agricultural University, Nanjing 210095, China
S. P. Sui
Affiliation:
Institute of Swine Science, Nanjing Agricultural University, Nanjing 210095, China
S. Gao
Affiliation:
Institute of Swine Science, Nanjing Agricultural University, Nanjing 210095, China
G. S. Su
Affiliation:
Department of Molecular Biology and Genetics, Center for Quantitative Genetics and Genomics, Aarhus University, Tjele 8830, Denmark
N. S. Ding
Affiliation:
College of Animal Science and Veterinary Medicine, Jiangxi Agricultural University, Nanchang 330045, China
Y. Huang
Affiliation:
Changzhou Jiaoxi Cooperatives of Erhualian Pigs, Changzhou 213116, China
Z. Q. Lu
Affiliation:
Changshu Animal Husbandry and Veterinary Station, Suzhou 215500, China
X. G. Huang
Affiliation:
Sutai Enterprise Co., Ltd, Suzhou 215000, China
R. H. Huang*
Affiliation:
Institute of Swine Science, Nanjing Agricultural University, Nanjing 210095, China
*
†E-mail: lipinghua718@njau.edu.cn; rhhuang@njau.edu.cn
†E-mail: lipinghua718@njau.edu.cn; rhhuang@njau.edu.cn
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Abstract

Litter size has a great impact on the profit of swine producers. Uterine development is an important determinant of reproduction efficiency and could hence affect litter size. Chinese Erhualian pig is one of the most prolific breeds in the world, even though large phenotypic variation in litter size was observed within Erhualian sows. To dissect the genetic basis of the phenotypic variation, we herein conducted genome-wide association studies for total number born and number born alive (NBA) of Erhualian sows. In total, one significant single nucleotide polymorphism (SNP) (P<1.78e−06) and 11 suggestive SNPs (P<3.57e−05) were identified on 10 chromosomes, confirming seven previously reported quantitative trait loci (QTL) and uncovering six QTL for litter size or uterus length. One locus on Sus scrofa chromosome (SSC) 13 (79.28 to 90.43 Mb) harbored a cluster of suggestive SNPs associated with multiparous NBA. The SNP (rs81447100) within this region was confirmed to be significantly (P<0.05) associated with litter size in Erhualian (n=313), Sutai (n=173) and Yorkshire (n=488) populations. Retinol binding protein 2 and retinol binding protein 1 functionally related to the development of uterus were located in a region of 2 Mb around rs81447100. Moreover, four genes related to embryo implantation and development were also detected around other significant SNPs. Taken together, our findings provide a potential marker (rs81447100) for the genetic improvement of litter size not only in Chinese Erhualian pigs but also in European commercial pig breeds like Yorkshire, and would facilitate the final identification of causative variant(s) underlying the effect of SSC13 QTL on litter size.

Keywords

pigfertility phenotypic variationrs81447100potential marker
Type
Research Article
Information
animal , Volume 12 , Issue 12 , December 2018 , pp. 2453 - 2461
Copyright
© The Animal Consortium 2018 

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References

Ai, H, Fang, X, Yang, B, Huang, Z, Chen, H, Mao, L, Zhang, F, Zhang, L, Cui, L, He, W, Yang, J, Yao, X, Zhou, L, Han, L, Li, J, Sun, S, Xie, X, Lai, B, Su, Y, Lu, Y, Yang, H, Huang, T, Deng, W, Nielsen, R, Ren, J and Huang, L 2015. Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing. Nature Genetics 47, 217–225.Google Scholar
Bartlett, A, Pain, SJ, Hughes, PE, Stott, P and van Wettere, WH 2009. The effects of PG600 and boar exposure on oestrus detection and potential litter size following mating at either the induced (pubertal) or second oestrus. Animal Reproduction Science 114, 219–227.Google Scholar
Blaner, WS 1989. Retinol-binding protein: the serum transport protein for vitamin A*. Endocrine Reviews 10, 308–316.Google Scholar
Darvasi, A and Soller, M 1992. Selective genotyping for determination of linkage between a marker locus and a quantitative trait locus. Theoretical and Applied Genetics 85, 353–359.Google Scholar
Dulioust, E, Toyama, K, Busnel, MC, Moutier, R, Carlier, M, Marchaland, C, Ducot, B, Roubertoux, P and Auroux, M 1995. Long-term effects of embryo freezing in mice. Proceedings of the National Academy of Sciences of the United States of America 92, 589–593.Google Scholar
Dyck, GW and Swierstra, EE 1983. Growth of the reproductive tract of the gilt from birth to puberty. Canadian Journal of Animal Science 63, 81–87.Google Scholar
Fernandez-Rodriguez, A, Rodriguez, C, Varona, L, Balcells, I, Noguera, JL, Ovilo, C and Fernandez, AI 2010. Analysis of candidate genes underlying two epistatic quantitative trait loci on SSC12 affecting litter size in pig. Animal Genetics 41, 73–80.Google Scholar
Harney, JP, Ali, M, Vedeckis, WV and Bazer, FW 1994. Porcine conceptus and endometrial retinoid-binding proteins. Reproduction, Fertility and Development 6, 211–219.Google Scholar
Harney, JP, Ott, TL, Geisert, RD and Bazer, FW 1993. Retinol-binding protein gene expression in cyclic and pregnant endometrium of pigs, sheep, and cattle. Biology of Reproduction 49, 1066–1073.Google Scholar
He, LC, Li, PH, Ma, X, Sui, SP, Gao, S, Kim, SW, Gu, YQ, Huang, Y, Ding, NS and Huang, RH 2017. Identification of new single nucleotide polymorphisms affecting total number born and candidate genes related to ovulation rate in Chinese Erhualian pigs. Animal Genetics 48, 48–54.Google Scholar
Hu, SJ, Ren, G, Liu, JL, Zhao, ZA, Yu, YS, Su, RW, Ma, XH, Ni, H, Lei, W and Yang, ZM 2008. MicroRNA expression and regulation in mouse uterus during embryo implantation. Journal of Biological Chemistry 283, 23473–23484.Google Scholar
Johansson, S, Dencker, L and Dantzer, V 2001. Immunohistochemical localization of retinoid binding proteins at the materno-fetal interface of the porcine epitheliochorial placenta. Biology of Reproduction 64, 60–68.Google Scholar
Liu, KH, Dore, JJ Jr, Roberts, MP, Krishnan, R, Hopkins, FM and Godkin, JD 1993. Expression and cellular localization of retinol-binding protein messenger ribonucleic acid in bovine blastocysts and extraembryonic membranes. Biology of Reproduction 49, 393–400.Google Scholar
Liu, KH and Godkin, JD 1992. Characterization and immunolocalization of bovine uterine retinol-binding protein. Biology of Reproduction 47, 1099–1104.Google Scholar
Madsen, P, Sørensen, P, Su, G, Damgaard, LH, Thomsen, H and Labouriau, R 2006. DMU-a package for analyzing multivariate mixed models. In 8th World Congress on Genetics Applied to Livestock Production, 13–18 August, Belo Horizonte, Minas Gerais, Brazil, pp. 27–11.Google Scholar
Noguera, JL, Rodriguez, C, Varona, L, Tomas, A, Munoz, G, Ramirez, O, Barragan, C, Arque, M, Bidanel, JP, Amills, M, Ovilo, C and Sanchez, A 2009. A bi-dimensional genome scan for prolificacy traits in pigs shows the existence of multiple epistatic QTL. BMC Genomics 10, 636.Google Scholar
Onteru, SK, Fan, B, Du, ZQ, Garrick, DJ, Stalder, KJ and Rothschild, MF 2012. A whole-genome association study for pig reproductive traits. Animal Genetics 43, 18–26.Google Scholar
Orlandi, A, Ferlosio, A, Ciucci, A, Francesconi, A, Lifschitz-Mercer, B, Gabbiani, G, Spagnoli, LG and Czernobilsky, B 2006. Cellular retinol binding protein-1 expression in endometrial hyperplasia and carcinoma: diagnostic and possible therapeutic implications. Modern Pathology 19, 797–803.Google Scholar
Padmanabhan, N, Jia, D, Geary-Joo, C, Wu, X, Ferguson-Smith, AC, Fung, E, Bieda, MC, Snyder, FF, Gravel, RA, Cross, JC and Watson, ED 2013. Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell 155, 81–93.Google Scholar
Pasini, D, Cloos, PA, Walfridsson, J, Olsson, L, Bukowski, JP, Johansen, JV, Bak, M, Tommerup, N, Rappsilber, J and Helin, K 2010. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306–310.Google Scholar
Purcell, S, Neale, B, Todd-Brown, K, Thomas, L, Ferreira, MA, Bender, D, Maller, J, Sklar, P, de Bakker, PI, Daly, MJ and Sham, PC 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81, 559–575.Google Scholar
Rosendo, A, Iannuccelli, N, Gilbert, H, Riquet, J, Billon, Y, Amigues, Y, Milan, D and Bidanel, JP 2012. Microsatellite mapping of quantitative trait loci affecting female reproductive tract characteristics in Meishan x Large White F(2) pigs. Journal of Animal Science 90, 37–44.Google Scholar
Rothschild, MF, Messer, L, Day, A, Wales, R, Short, T, Southwood, O and Plastow, G 2000. Investigation of the retinol-binding protein 4 (RBP4) gene as a candidate gene for increased litter size in pigs. Mammalian Genome 11, 75–77.Google Scholar
Sandholm, N, Salem, RM, McKnight, AJ, Brennan, EP, Forsblom, C, Isakova, T, McKay, GJ, Williams, WW, Sadlier, DM, Makinen, VP, Swan, EJ, Palmer, C, Boright, AP, Ahlqvist, E, Deshmukh, HA, Keller, BJ, Huang, H, Ahola, AJ, Fagerholm, E, Gordin, D, Harjutsalo, V, He, B, Heikkila, O, Hietala, K, Kyto, J, Lahermo, P, Lehto, M, Lithovius, R, Osterholm, AM, Parkkonen, M, Pitkaniemi, J, Rosengard-Barlund, M, Saraheimo, M, Sarti, C, Soderlund, J, Soro-Paavonen, A, Syreeni, A, Thorn, LM, Tikkanen, H, Tolonen, N, Tryggvason, K, Tuomilehto, J, Waden, J, Gill, GV, Prior, S, Guiducci, C, Mirel, DB, Taylor, A, Hosseini, SM, Group, DER, Parving, HH, Rossing, P, Tarnow, L, Ladenvall, C, Alhenc-Gelas, F, Lefebvre, P, Rigalleau, V, Roussel, R, Tregouet, DA, Maestroni, A, Maestroni, S, Falhammar, H, Gu, T, Mollsten, A, Cimponeriu, D, Ioana, M, Mota, M, Mota, E, Serafinceanu, C, Stavarachi, M, Hanson, RL, Nelson, RG, Kretzler, M, Colhoun, HM, Panduru, NM, Gu, HF, Brismar, K, Zerbini, G, Hadjadj, S, Marre, M, Groop, L, Lajer, M, Bull, SB, Waggott, D, Paterson, AD, Savage, DA, Bain, SC, Martin, F, Hirschhorn, JN, Godson, C, Florez, JC, Groop, PH and Maxwell, AP 2012. New susceptibility loci associated with kidney disease in type 1 diabetes. PLoS Genetics 8, e1002921.Google Scholar
Schneider, JF, Rempel, LA, Snelling, WM, Wiedmann, RT, Nonneman, DJ and Rohrer, GA 2012. Genome-wide association study of swine farrowing traits. Part II: Bayesian analysis of marker data. Journal of Animal Science 90, 3360–3367.Google Scholar
Seo, H, Kim, M, Choi, Y and Ka, H 2011. Salivary lipocalin is uniquely expressed in the uterine endometrial glands at the time of conceptus implantation and induced by interleukin 1beta in pigs. Biology of Reproduction 84, 279–287.Google Scholar
Wilkie, PJ, Paszek, AA, Beattie, CW, Alexander, LJ, Wheeler, MB and Schook, LB 1999. A genomic scan of porcine reproductive traits reveals possible quantitative trait loci (QTLs) for number of corpora lutea. Mammalian Genome 10, 573–578.Google Scholar
Wilson, ME, Biensen, NJ and Ford, SP 1999. Novel insight into the control of litter size in pigs, using placental efficiency as a selection tool. Journal of Animal Science 77, 1654–1658.Google Scholar
Wolf, G 1983. Multiple functions of vitamin A. Physiological Reviews 64, 873–937.Google Scholar
Wu, MC and Dziuk, PJ 1988. Procedures for measuring length of the pig uterus. Journal of Animal Science 66, 1712–1720.Google Scholar
Zhang, F, Zhang, Z, Yan, X, Chen, H, Zhang, W, Hong, Y and Huang, L 2014. Genome-wide association studies for hematological traits in Chinese Sutai pigs. BMC Genetics 15, 41.Google Scholar
Zhou, X and Stephens, M 2012. Genome-wide efficient mixed-model analysis for association studies. Nature Genetics 44, 821–824.Google Scholar
Zhou, ZW, Liu, C, Li, TL, Bruhn, C, Krueger, A, Min, W, Wang, ZQ and Carr, AM 2013. An essential function for the ATR-activation-domain (AAD) of TopBP1 in mouse development and cellular senescence. PLoS Genetics 9, e1003702.Google Scholar
Ziegel, ER 1995. Applied multivariate statistics with SAS® software. Technometrics 38, 300.Google Scholar
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