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Identification of pleiotropic genes and gene sets underlying growth and immunity traits: a case study on Meishan pigs

Published online by Cambridge University Press:  22 December 2015

Z. Zhang
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
Z. Wang
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
Y. Yang
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
J. Zhao
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
Q. Chen
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
R. Liao
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
Z. Chen
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
X. Zhang
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
M. Xue
Affiliation:
National Station of Animal Husbandry, Beijing 100125, PR China
H. Yang
Affiliation:
National Station of Animal Husbandry, Beijing 100125, PR China
Y. Zheng
Affiliation:
National Station of Animal Husbandry, Beijing 100125, PR China
Q. Wang*
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
Y. Pan*
Affiliation:
Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, PR China Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai 200240, PR China
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Abstract

Both growth and immune capacity are important traits in animal breeding. The animal quantitative trait loci (QTL) database is a valuable resource and can be used for interpreting the genetic mechanisms that underlie growth and immune traits. However, QTL intervals often involve too many candidate genes to find the true causal genes. Therefore, the aim of this study was to provide an effective annotation pipeline that can make full use of the information of Gene Ontology terms annotation, linkage gene blocks and pathways to further identify pleiotropic genes and gene sets in the overlapping intervals of growth-related and immunity-related QTLs. In total, 55 non-redundant QTL overlapping intervals were identified, 1893 growth-related genes and 713 immunity-related genes were further classified into overlapping intervals and 405 pleiotropic genes shared by the two gene sets were determined. In addition, 19 pleiotropic gene linkage blocks and 67 pathways related to immunity and growth traits were discovered. A total of 343 growth-related genes and 144 immunity-related genes involved in pleiotropic pathways were also identified, respectively. We also sequenced and genotyped 284 individuals from Chinese Meishan pigs and European pigs and mapped the single nucleotide polymorphisms (SNPs) to the pleiotropic genes and gene sets that we identified. A total of 971 high-confidence SNPs were mapped to the pleiotropic genes and gene sets that we identified, and among them 743 SNPs were statistically significant in allele frequency between Meishan and European pigs. This study explores the relationship between growth and immunity traits from the view of QTL overlapping intervals and can be generalized to explore the relationships between other traits.

Type
Research Article
Copyright
© The Animal Consortium 2015 

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References

Adelman, DM, Maltepe, E and Simon, MC 1999. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes & Development 13, 24782483.CrossRefGoogle ScholarPubMed
Aerts, J, Megens, H, Veenendaal, T, Ovcharenko, I, Crooijmans, R, Gordon, L, Stubbs, L and Groenen, M 2006. Extent of linkage disequilibrium in chicken. Cytogenetic and Genome Research 117, 338345.Google Scholar
Ai, H, Fang, X, Yang, B, Huang, Z, Chen, H, Mao, L, Zhang, F, Zhang, L, Cui, L and He, W 2015. Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing. Nature Genetics 47, 217225.Google Scholar
Ai, H, Huang, L and Ren, J 2013. Genetic diversity, linkage disequilibrium and selection signatures in Chinese and Western pigs revealed by genome-wide SNP markers. PLoS One 8, e56001.Google Scholar
Amaral, AJ, Megens, H-J, Crooijmans, RP, Heuven, HC and Groenen, MA 2008. Linkage disequilibrium decay and haplotype block structure in the pig. Genetics 179, 569579.CrossRefGoogle ScholarPubMed
Benjamini, Y and Hochberg, Y 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289300.Google Scholar
Bolormaa, S, Pryce, JE, Reverter, A, Zhang, Y, Barendse, W, Kemper, K, Tier, B, Savin, K, Hayes, BJ and Goddard, ME 2014. A multi-trait, meta-analysis for detecting pleiotropic polymorphisms for stature, fatness and reproduction in beef cattle. PLoS Genetics 10, e1004198.Google Scholar
Borghetti, P, De Angelis, E, Saleri, R, Cavalli, V, Cacchioli, A, Corradi, A, Mocchegiani, E and Martelli, P 2006. Peripheral T lymphocyte changes in neonatal piglets: relationship with growth hormone (GH), prolactin (PRL) and cortisol changes. Veterinary Immunology and Immunopathology 110, 1725.Google Scholar
Chen, Q, Ma, Y, Yang, Y, Chen, Z, Liao, R, Xie, X, Wang, Z, He, P, Tu, Y and Zhang, X 2013. Genotyping by genome reducing and sequencing for outbred animals. PLoS One 8, e67500.Google Scholar
Clapperton, M, Bishop, S and Glass, E 2005. Innate immune traits differ between Meishan and Large White pigs. Veterinary Immunology and Immunopathology 104, 131144.Google Scholar
Clapperton, M, Diack, AB, Matika, O, Glass, EJ, Gladney, CD, Mellencamp, MA, Hoste, A and Bishop, SC 2009. Traits associated with innate and adaptive immunity in pigs: heritability and associations with performance under different health status conditions. Genetics Selection Evolution 41, 54.CrossRefGoogle ScholarPubMed
Deverman, BE and Patterson, PH 2009. Cytokines and CNS development. Neuron 64, 6178.Google Scholar
Durinck, S, Moreau, Y, Kasprzyk, A, Davis, S, De Moor, B, Brazma, A and Huber, W 2005. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21, 34393440.Google Scholar
Fröhlich, H, Speer, N, Poustka, A and Beissbarth, T 2007. GOSim – an R-package for computation of information theoretic GO similarities between terms and gene products. BMC Bioinformatics 8, 166.Google Scholar
Galina-Pantoja, L, Mellencamp, MA, Bastiaansen, J, Cabrera, R, Solano-Aguilar, G and Lunney, JK 2006. Relationship between immune cell phenotypes and pig growth in a commercial farm. Animal Biotechnology 17, 8198.Google Scholar
Hu, ZL, Park, CA, Wu, XL and Reecy, JM 2013. Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic Acids Research 41, D871D879.Google Scholar
Kanehisa, M and Goto, S 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28, 2730.Google Scholar
Klasing, KC 1988. Nutritional aspects of leukocytic cytokines. The Journal of Nutrition 118, 14361446.Google Scholar
Klein, J and Nikolaidis, N 2005. The descent of the antibody-based immune system by gradual evolution. Proceedings of the National Academy of Sciences of the United States of America 102, 169174.Google Scholar
Le, Y, Zhou, Y, Iribarren, P and Wang, J 2004. Chemokines and chemokine receptors: their manifold roles in homeostasis and disease. Cellular & Molecular Immunology 1, 95104.Google Scholar
Liu, G, Jennen, DG, Tholen, E, Juengst, H, Kleinwachter, T, Holker, M, Tesfaye, D, Un, G, Schreinemachers, HJ, Murani, E, Ponsuksili, S, Kim, JJ, Schellander, K and Wimmers, K 2007. A genome scan reveals QTL for growth, fatness, leanness and meat quality in a Duroc-Pietrain resource population. Animal Genetics 38, 241252.Google Scholar
Lowe, HJ and Barnett, GO 1994. Understanding and using the medical subject headings (MeSH) vocabulary to perform literature searches. The Journal of the American Medical Association 271, 11031108.Google Scholar
Mao, X, Cai, T, Olyarchuk, JG and Wei, L 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21, 37873793.Google Scholar
Müller, E, Moser, G, Bartenschilager, H and Geldermann, H 2000. Trait values of growth, carcass and meat quality in Wild Boar, Meishan and Pietrain pigs as well as their crossbred generations. Journal of Animal Breeding and Genetics 117, 189202.Google Scholar
Rauw, W, Kanis, E, Noordhuizen-Stassen, E and Grommers, F 1998. Undesirable side effects of selection for high production efficiency in farm animals: a review. Livestock Production Science 56, 1533.Google Scholar
Reiner, G, Fischer, R, Hepp, S, Berge, T, Kohler, F and Willems, H 2008. Quantitative trait loci for white blood cell numbers in swine. Animal Genetics 39, 163168.Google Scholar
Rothschild, MF, Hu, Z-l and Jiang, Z 2007. Advances in QTL mapping in pigs. International Journal of Biological Sciences 3, 192197.Google Scholar
Solovieff, N, Cotsapas, C, Lee, PH, Purcell, SM and Smoller, JW 2013. Pleiotropy in complex traits: challenges and strategies. Nature Reviews Genetics 14, 483495.Google Scholar
Upton, GJ 1992. Fisher’s exact test. Journal of the Royal Statistical Society. Series A (Statistics in Society) 155, 395402.Google Scholar
van der Most, PJ, de Jong, B, Parmentier, HK and Verhulst, S 2011. Trade-off between growth and immune function: a meta-analysis of selection experiments. Functional Ecology 25, 7480.Google Scholar
Vereecke, L, Beyaert, R and van Loo, G 2009. The ubiquitin-editing enzyme A20 (TNFAIP3) is a central regulator of immunopathology. Trends in Immunology 30, 383391.Google Scholar
Wang, Z, Chen, Q, Yang, Y, Liao, R, Zhao, J, Zhang, Z, Chen, Z, Zhang, X, Xue, M and Yang, H 2015. Genetic diversity and population structure of six Chinese indigenous pig breeds in the Taihu Lake region revealed by sequencing data. Animal Genetics 46, 697701.Google Scholar
Wong, MM and Fish, EN 2003. Chemokines: attractive mediators of the immune response. Seminars in Immunology 15, 514.Google Scholar
Zhang, X, Li, N, Li, X, Zhao, W, Qiao, Y, Liang, L and Ding, Y 2012. Low expression of DAB2IP contributes to malignant development and poor prognosis in hepatocellular carcinoma. Journal of Gastroenterology and Hepatology 27, 11171125.Google Scholar
Zhao, S, Zhu, M and Chen, H 2012. Immunogenomics for identification of disease resistance genes in pigs: a review focusing on gram-negative bacilli. Journal of Animal Science and Biotechnology 3, 113.Google Scholar
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