Skip to main content Accessibility help
×
×
Home

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

  • Z. Zhang (a1) (a2), Z. Wang (a1) (a2), Y. Yang (a1) (a2), J. Zhao (a1) (a2), Q. Chen (a1) (a2), R. Liao (a1) (a2), Z. Chen (a1) (a2), X. Zhang (a1) (a2), M. Xue (a3), H. Yang (a3), Y. Zheng (a3), Q. Wang (a1) (a2) and Y. Pan (a1) (a2)...

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.

Copyright

Corresponding author

References

Hide All
Adelman, DM, Maltepe, E and Simon, MC 1999. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes & Development 13, 24782483.
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.
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.
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.
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.
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.
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.
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.
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.
Clapperton, M, Bishop, S and Glass, E 2005. Innate immune traits differ between Meishan and Large White pigs. Veterinary Immunology and Immunopathology 104, 131144.
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.
Deverman, BE and Patterson, PH 2009. Cytokines and CNS development. Neuron 64, 6178.
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.
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.
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.
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.
Kanehisa, M and Goto, S 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28, 2730.
Klasing, KC 1988. Nutritional aspects of leukocytic cytokines. The Journal of Nutrition 118, 14361446.
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.
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.
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.
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.
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.
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.
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.
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.
Rothschild, MF, Hu, Z-l and Jiang, Z 2007. Advances in QTL mapping in pigs. International Journal of Biological Sciences 3, 192197.
Solovieff, N, Cotsapas, C, Lee, PH, Purcell, SM and Smoller, JW 2013. Pleiotropy in complex traits: challenges and strategies. Nature Reviews Genetics 14, 483495.
Upton, GJ 1992. Fisher’s exact test. Journal of the Royal Statistical Society. Series A (Statistics in Society) 155, 395402.
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.
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.
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.
Wong, MM and Fish, EN 2003. Chemokines: attractive mediators of the immune response. Seminars in Immunology 15, 514.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

animal
  • ISSN: 1751-7311
  • EISSN: 1751-732X
  • URL: /core/journals/animal
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
UNKNOWN
Supplementary materials

Zhang supplementary material
Table S1

 Unknown (12 KB)
12 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed