Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-30T19:57:22.542Z Has data issue: false hasContentIssue false

A genome-wide association analysis for susceptibility of pigs to enterotoxigenic Escherichia coli F41

Published online by Cambridge University Press:  03 March 2016

H. Y. Ji
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China Institute of Animal Husbandry and Veterinary, Jiangxi Academy of Agricultural Science, 330200 Nanchang, China
B. Yang
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
Z. Y. Zhang
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
J. Ouyang
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China Department of Biology, Nanchang University of Science and Technology, 330038 Nanchang, China
M. Yang
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
X. F. Zhang
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
W. C. Zhang
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
Y. Su
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
K. W. Zhao
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
S. J. Xiao
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
X. M. Yan
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China Department of Biology, Nanchang University of Science and Technology, 330038 Nanchang, China
J. Ren*
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
L. S. Huang*
Affiliation:
State Key Laboratory for Pig Genetic Improvement and Production Science, Jiangxi Agricultural University, 330045 Nanchang, China
Get access

Abstract

Enterotoxigenic Escherichia coli (ETEC) is a type of pathogenic bacteria that cause diarrhea in piglets through colonizing pig small intestine epithelial cells by their surface fimbriae. Different fimbriae type of ETEC including F4, F18, K99 and F41 have been isolated from diarrheal pigs. In this study, we performed a genome-wide association study to map the loci associated with the susceptibility of pigs to ETEC F41 using 39454 single nucleotide polymorphisms (SNPs) in 667 F2 pigs from a White Duroc×Erhualian F2 cross. The most significant SNP (ALGA0022658, P=5.59×10−13) located at 6.95 Mb on chromosome 4. ALGA0022658 was in high linkage disequilibrium (r2>0.5) with surrounding SNPs that span a 1.21 Mb interval. Within this 1.21 Mb region, we investigated ZFAT as a positional candidate gene. We re-sequenced cDNA of ZFAT in four pigs with different susceptibility phenotypes, and identified seven coding variants. We genotyped these seven variants in 287 unrelated pigs from 15 diverse breeds that were measured with ETEC F41 susceptibility phenotype. Five variants showed nominal significant association (P<0.05) with ETEC F41 susceptibility phenotype in International commercial pigs. This study provided refined region associated with susceptibility of pigs to ETEC F41 than that reported previously. Further works are needed to uncover the underlying causal mutation(s).

Type
Research Article
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Both authors contributed equally to this study and should be considered as co-first authors.

References

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.CrossRefGoogle ScholarPubMed
Aulchenko, YS, Ripke, S, Isaacs, A and van Duijn, CM 2007. GenABEL: an R library for genome-wide association analysis. Bioinformatics 23, 12941296.CrossRefGoogle Scholar
Baker, DR, Billey, LO and Francis, DH 1997. Distribution of K88 Escherichia coli-adhesive and nonadhesive phenotypes among pigs of four breeds. Veterinary Microbiology 54, 123132.CrossRefGoogle ScholarPubMed
Chen, X, Gao, S, Jiao, X and Liu, XF 2004. Prevalence of serogroups and virulence factors of Escherichia coli strains isolated from pigs with postweaning diarrhoea in eastern China. Veterinary Microbiology 103, 1320.Google Scholar
Fan, B, Onteru, SK, Du, ZQ, Garrick, DJ, Stalder, KJ and Rothschild, MF 2011. Genome-wide association study identifies Loci for body composition and structural soundness traits in pigs. PLoS One 6, e14726.Google Scholar
Fan, Y, Xing, Y, Zhang, Z, Ai, H, Ouyang, Z, Ouyang, J, Yang, M, Li, P, Chen, Y, Gao, J, Li, L, Huang, L and Ren, J 2013. A further look at porcine chromosome 7 reveals VRTN variants associated with vertebral number in Chinese and western pigs. PLoS One 8, e62534.Google Scholar
Grindflek, E, Lien, S, Hamland, H, Hansen, MH, Kent, M, van Son, M and Meuwissen, TH 2011. Large scale genome-wide association and LDLA mapping study identifies QTLs for boar taint and related sex steroids. BMC Genomics 12, 362.Google Scholar
Groenen, MA, Archibald, AL, Uenishi, H, Tuggle, CK, Takeuchi, Y, Rothschild, MF, Rogel-Gaillard, C, Park, C, Milan, D, Megens, HJ, Li, S, Larkin, DM, Kim, H, Frantz, LA, Caccamo, M, Ahn, H, Aken, BL, Anselmo, A, Anthon, C, Auvil, L, Badaoui, B, Beattie, CW, Bendixen, C, Berman, D, Blecha, F, Blomberg, J, Bolund, L, Bosse, M, Botti, S, Bujie, Z, Bystrom, M, Capitanu, B, Carvalho-Silva, D, Chardon, P, Chen, C, Cheng, R, Choi, SH, Chow, W, Clark, RC, Clee, C, Crooijmans, RP, Dawson, HD, Dehais, P, De Sapio, F, Dibbits, B, Drou, N, Du, ZQ, Eversole, K, Fadista, J, Fairley, S, Faraut, T, Faulkner, GJ, Fowler, KE, Fredholm, M, Fritz, E, Gilbert, JG, Giuffra, E, Gorodkin, J, Griffin, DK, Harrow, JL, Hayward, A, Howe, K, Hu, ZL, Humphray, SJ, Hunt, T, Hornshoj, H, Jeon, JT, Jern, P, Jones, M, Jurka, J, Kanamori, H, Kapetanovic, R, Kim, J, Kim, JH, Kim, KW, Kim, TH, Larson, G, Lee, K, Lee, KT, Leggett, R, Lewin, HA, Li, Y, Liu, W, Loveland, JE, Lu, Y, Lunney, JK, Ma, J, Madsen, O, Mann, K, Matthews, L, McLaren, S, Morozumi, T, Murtaugh, MP, Narayan, J, Nguyen, DT, Ni, P, Oh, SJ, Onteru, S, Panitz, F, Park, EW, Park, HS, Pascal, G, Paudel, Y, Perez-Enciso, M, Ramirez-Gonzalez, R, Reecy, JM, Rodriguez-Zas, S, Rohrer, GA, Rund, L, Sang, Y, Schachtschneider, K, Schraiber, JG, Schwartz, J, Scobie, L, Scott, C, Searle, S, Servin, B, Southey, BR, Sperber, G, Stadler, P, Sweedler, JV, Tafer, H, Thomsen, B, Wali, R, Wang, J, Wang, J, White, S, Xu, X, Yerle, M, Zhang, G, Zhang, J, Zhang, J, Zhao, S, Rogers, J, Churcher, C and Schook, LB 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491, 393398.Google Scholar
Guo, Y, Mao, H, Ren, J, Yan, X, Duan, Y, Yang, G, Ren, D, Zhang, Z, Yang, B, Ouyang, J, Brenig, B, Haley, C and Huang, L 2009. A linkage map of the porcine genome from a large-scale White Duroc×Erhualian resource population and evaluation of factors affecting recombination rates. Animal Genetics 40, 4752.Google Scholar
Kathiresan, S, Willer, CJ, Peloso, GM, Demissie, S, Musunuru, K, Schadt, EE, Kaplan, L, Bennett, D, Li, Y, Tanaka, T, Voight, BF, Bonnycastle, LL, Jackson, AU, Crawford, G, Surti, A, Guiducci, C, Burtt, NP, Parish, S, Clarke, R, Zelenika, D, Kubalanza, KA, Morken, MA, Scott, LJ, Stringham, HM, Galan, P, Swift, AJ, Kuusisto, J, Bergman, RN, Sundvall, J, Laakso, M, Ferrucci, L, Scheet, P, Sanna, S, Uda, M, Yang, Q, Lunetta, KL, Dupuis, J, de Bakker, PI, O’Donnell, CJ, Chambers, JC, Kooner, JS, Hercberg, S, Meneton, P, Lakatta, EG, Scuteri, A, Schlessinger, D, Tuomilehto, J, Collins, FS, Groop, L, Altshuler, D, Collins, R, Lathrop, GM, Melander, O, Salomaa, V, Peltonen, L, Orho-Melander, M, Ordovas, JM, Boehnke, M, Abecasis, GR, Mohlke, KL and Cupples, LA 2009. Common variants at 30 loci contribute to polygenic dyslipidemia. Nature Genetics 41, 5665.Google Scholar
Margolin, AA, Wang, K, Lim, WK, Kustagi, M, Nemenman, I and Califano, A 2006. Reverse engineering cellular networks. Nature Protocol 1, 662671.CrossRefGoogle ScholarPubMed
Meijerink, E, Neuenschwander, S, Fries, R, Dinter, A, Bertschinger, HU, Stranzinger, G and Vogeli, P 2000. A DNA polymorphism influencing alpha(1,2)fucosyltransferase activity of the pig FUT1 enzyme determines susceptibility of small intestinal epithelium to Escherichia coli F18 adhesion. Immunogenetics 52, 129136.CrossRefGoogle ScholarPubMed
Moon, HW, Hoffman, LJ, Cornick, NA, Booher, SL and Bosworth, BT 1999. Prevalences of some virulence genes among Escherichia coli isolates from swine presented to a diagnostic laboratory in lowa. Journal of Veterinary Diagnostic Investigation 6, 557560.CrossRefGoogle 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, 1826.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. The American Journal of Human Genetics 81, 559575.Google Scholar
Ren, J, Duan, Y, Qiao, R, Yao, F, Zhang, Z, Yang, B, Guo, Y, Xiao, S, Wei, R, Ouyang, Z, Ding, N, Ai, H and Huang, L 2011. A missense mutation in PPARD causes a major QTL effect on ear size in pigs. PLoS Genetics 7, e1002043.Google Scholar
Ren, J, Yan, X, Ai, H, Zhang, Z, Huang, X, Ouyang, J, Yang, M, Yang, H, Han, P, Zeng, W, Chen, Y, Guo, Y, Xiao, S, Ding, N and Huang, L 2012. Susceptibility towards enterotoxigenic Escherichia coli F4ac diarrhea is governed by the MUC13 gene in pigs. PLoS One 7, e44573.Google Scholar
Shi, YY and He, L 2005. SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Research 15, 9798.Google Scholar
Stephens, M, Smith, NJ and Donnelly, P 2001. A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics 68, 978989.CrossRefGoogle ScholarPubMed
Thornton, T and McPeek, MS 2010. ROADTRIPS: case-control association testing with partially or completely unknown population and pedigree structure. American Journal of Human Genetics 86, 172184.Google Scholar
Yan, X, Huang, X, Ren, J, Ouyang, J, Yang, M, Han, P and Huang, L 2011. Adhesion phenotypes of pigs of Chinese and western breeds and a White Duroc-Erhualian crossbreed with regard to susceptibility to enterotoxigenic Escherichia coli with fimbrial adhesins K99, 987P, and F41. American Journal of Veterinary Research 72, 8084.Google Scholar
Yang, B, Huang, X, Yan, X, Ren, J, Yang, S, Zou, Z, Zeng, W, Ou, Y, Huang, W and Huang, L 2009. Detection of quantitative trait loci for porcine susceptibility to enterotoxigenic Escherichia coli F41 in a White Duroc×Chinese Erhualian resource population. Animal 3, 946950.CrossRefGoogle Scholar
Yang, B, Zhang, W, Zhang, Z, Fan, Y, Xie, X, Ai, H, Ma, J, Xiao, S, Huang, L and Ren, J 2013. Genome-wide association analyses for fatty acid composition in porcine muscle and abdominal fat tissues. PLoS One 8, e65554.Google Scholar
Zhang, B, Ren, J, Yan, X, Huang, X, Ji, H, Peng, Q, Zhang, Z and Huang, L 2008. Investigation of the porcine MUC13 gene: isolation, expression, polymorphisms and strong association with susceptibility to enterotoxigenic Escherichia coli F4ab/ac. Animal Genetics 39, 258266.CrossRefGoogle ScholarPubMed
Supplementary material: File

Ji supplementary material

Tables S1-S4 and Figure S1

Download Ji supplementary material(File)
File 41.4 KB