Revealing new candidate genes for reproductive traits in pigs: Combining Bayesian GWAS and functional pathways

Genetics Selection Evolution

Volumn 48, Issue 1, 2016, Pages

  Verardo, Lucas L ^a,b   Silva, Fabyano F ^a   Lopes, Marcos S ^b,c   Madsen, Ole ^b   Bastiaansen, John W M ^b   Knol, Egbert F ^c   Kelly, Mathew ^d   Varona, Luis ^e   Lopes, Paulo S ^a   Guimarães, Simone E F ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c TOPIGS Research Center IPG   (Netherlands)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY; CARDIOVASCULAR DISEASE; DEVELOPMENTAL BIOLOGY; DIABETES; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC MARKER; PIG; REPRODUCTIVE STRATEGY; SURVIVAL;

SUIDAE;

ANIMAL; BAYES THEOREM; FEMALE; GENE REGULATORY NETWORK; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; NORMAL DISTRIBUTION; PHENOTYPE; PIG; POISSON DISTRIBUTION; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BAYES THEOREM; FEMALE; GENE REGULATORY NETWORKS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; NORMAL DISTRIBUTION; PHENOTYPE; POISSON DISTRIBUTION; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; REPRODUCTION; SUS SCROFA;

EID: 84958119834     PISSN: 0999193X     EISSN: 12979686     Source Type: Journal    
DOI: 10.1186/s12711-016-0189-x     Document Type: Article

References (81)

1. Blasco A, Bidanel JP, Haley CS. Genetics and neonatal survival. In: Varley MA, editor. The neonatal pig: development and survival. Wallingford: CABI; 1995. p. 17-38.
2. Onteru SK, Fan B, Du ZQ, Garrick DJ, Stalder KJ, Rothschild MF. A whole-genome association study for pig reproductive traits. Anim Genet. 2012;43:18-26.
3. Nevis IF, Reitsma A, Dominic A, McDonald S, Thabane L, Akl EA, et al. Pregnancy outcomes in women with chronic kidney disease: a systematic review. Clin J Am Soc Nephrol. 2011;6:2587-98.
4. Mathiesen ER, Ringholm L, Damm P. Stillbirth in diabetic pregnancies. Best Pract Res Clin Obstet Gynaecol. 2011;25:105-11.
5. Lee K, Khoshnood B, Chen L, Stephen NW, Cromie JW, Mittendorf RL. Infant mortality from congenital malformations in the United States, 1970-1997. Obstet Gynecol. 2001;98:620-7.
6. Hirooka H, de Koning DJ, Harlizius B, van Arendonk JA, Rattink AP, Groenen MA, et al. A whole-genome scan for quantitative trait loci affecting teat number in pigs. J Anim Sci. 2001;79:2320-6.
7. Hens JR, Wysolmerski JJ. Key stages of mammary gland development: molecular mechanisms involved in the formation of the embryonic mammary gland. Breast Cancer Res. 2005;7:220-4.
8. Ren DR, Ren J, Ruan GF, Guo YM, Wu LH, Yang GC, et al. Mapping and fine mapping of quantitative trait loci for the number of vertebrae in a White Duroc × Chinese Erhualian intercross resource population. Anim Genet. 2012;43:545-51.
9. Uimari P, Sironen A, Sevón-Aimonen ML. Whole-genome SNP association analysis of reproduction traits in the Finnish Landrace pig breed. Genet Sel Evol. 2011;43:42.
10. Schneider JF, Rempel LA, Rohrer GA. Genome-wide association study of swine farrowing traits. Part I: genetic and genomic parameter estimates. J Anim Sci. 2012;90:3353-9.
11. Perez-Enciso M, Tempelman RJ, Gianola D. A comparison between linear and Poisson mixed models for litter size in Iberian pigs. Livest Prod Sci. 1993;35:303-16.
12. Ayres DR, Pereira RJ, Boligon AA, Silva FF, Schenkel FS, Roso VM, et al. Linear and Poisson models for genetic evaluation of tick resistance in cross-bred Hereford x Nellore cattle. J Anim Breed Genet. 2013;130:417-24.
13. Cui Y, Kim DY, Zhu J. On the generalized Poisson regression mixture model for mapping quantitative trait loci with count data. Genetics. 2006;174:2159-72.
14. Silva KM, Bastiaansen JWM, Knol EF, Merks JWM, Lopes PS, Guimarães SEF, et al. Meta-analysis of results from quantitative trait loci mapping studies on pig chromosome 4. Anim Genet. 2011;42:280-92.
15. Hadfield JD, Nakagawa S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol. 2010;23:494-508.
16. Van Raden PM. Efficient methods to compute genomic predictions. J Dairy Sci. 2008;91:4414-23.
17. Stranden I, Garrick DJ. Derivation of equivalent computing algorithms for genomic predictions and reliabilities of animal merit. J Dairy Sci. 2009;92:2971-5.
18. Wang H, Misztal I, Aguilar I, Legarra A, Muir WM. Genome-wide association mapping including phenotypes from relatives without genotypes. Genet Res (Camb). 2012;94:73-83.
19. Li Z, Gopal V, Li X, Davis JM, Casella G. Simultaneous SNP identification in association studies with missing data. Ann Appl Stat. 2012;6:432-56.
20. Ramírez O, Quintanilla R, Varona L, Gallardo D, Díaz I, Pena RN, Amills M. DECR1 and ME1 genotypes are associated with lipid composition traits in Duroc pigs. J Anim Breed Genet. 2014;131:46-52.
21. Cecchinato A, Ribeca C, Chessa S, Cipolat-Gotet C, Maretto F, Casellas J, et al. Candidate gene association analysis for milk yield, composition, urea nitrogen and somatic cell scores in Brown Swiss cows. Animal. 2014;7:1062-70.
22. Mirina A, Atzmon G, Ye K, Bergman A. Gene size matters. PLoS One. 2012;7:e49093.
23. Yu TP, Tuggle CK, Schmitz CB, Rothschild MF. Association of PIT1 polymorphisms with growth and carcass traits in pigs. J Anim Sci. 1995;73:1282-8.
24. Chen J, Yang XJ, Xia D, Chen J, Wegner J, Jiang Z, et al. Sterol regulatory element binding transcription factor 1 expression and genetic polymorphism significantly affect intramuscular fat deposition in the longissimus muscle of Erhualian and Sutai pigs. J Anim Sci. 2008;86:57-63.
25. Fortes MR, Reverter T, Nagaraj SH, Zhang Y, Jonsson NN, Barris W, et al. A SNP-derived regulatory gene network underlying puberty in two tropical breeds of beef cattle. J Anim Sci. 2011;89:1669-83.
26. Reverter A, Fortes MRS. Building single nucleotide polymorphism-derived gene regulatory networks: towards functional genomewide association studies. J Anim Sci. 2013;91:530-6.
27. Verardo LL, Silva FF, Varona L, Resende MDV, Bastiaansen JWM, Lopes PS, et al. Bayesian GWAS and network analysis revealed new candidate genes for number of teats in pigs. J Appl Genet. 2015;56:123-32.
28. Ramos AM, Crooijmans RPMA, Affara NA, Amaral AJ, Archibald AL, Beever JE, et al. Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS One. 2009;4:e6524.
29. Oliphant A, Barker DL, Stuelpnagel JR, Chee MS. BeadArray technology: enabling an accurate, cost-effective approach to high-throughput genotyping. Biotechniques. 2002;Suppl56-8, 60-1.
30. Groenen MA, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, et al. Analyses of pig genomes provide insight into porcine demography and evolution. Nature. 2012;491:393-8.
31. Lopes MS, Bastiaansen JW, Harlizius B, Knol EF, Bovenhuis H. A genome-wide association study reveals dominance effects on number of teats in pigs. PLoS One. 2014;9:e105867.
32. Foulley JL, Gianola D, Im S. Genetic evaluation of traits distributed as Poisson-binomial with reference to reproductive traits. Theor Appl Genet. 1987;73:870-7.
33. Tempelman RJ, Gianola D. A mixed effects model for overdispersed count data in animal breeding. Biometrics. 1996;52:265-79.
34. Sun D, Speckman PL, Tsutakawa RK. Random effects in generalized linear mixed models (GLMMs). In: Dey DK, Ghosh SK, Mallick BK, editors. Generalized linear models: A Bayesian perspective. New York: Marcel Dekker Inc.; 2000.
35. Sorensen D, Gianola D. Uncertainty about functions of random variables. In: likelihood, Bayesian, and MCMC methods in quantitative genetics. New York: Springer-Verlarg; 2002.
36. Rashidi H, Mulder HA, Mathur P, van Arendonk JAM, Knol EF. Variation among sows in response to porcine reproductive and respiratory syndrome. Anim Sci. 2014;92:95-105.
37. Herrero-Medrano JM, Mathur PK, ten Napel J, Rashidi H, Alexandri P, Knol EF, et al. Estimation of genetic parameters and breeding values across challenged environments to select for robust pigs. J Anim Sci. 2015;93:1494-502.
38. Duijvesteijn N, Veltmaat JM, Knol EF, Harlizius B. High-resolution association mapping of number of teats in pigs reveals regions controlling vertebral development. BMC Genomics. 2014;15:542.
39. Hadfield JD. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw. 2010;33:1-22.
40. Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A. Bayesian measures of model complexity and fit. J R Statist Soc B. 2002;64:583-639.
41. Plummer M, Best N, Cowles K, Vines K. CODA: convergence diagnosis and output analysis for MCMC. R News. 2006;6:7-11.
42. Aguilar I, Misztal I, Legarra A, Tsuruta S. Efficient computation of the genomic relationship matrix and other matrices used in single-step evaluation. J Anim Breed Genet. 2011;128:422-8.
43. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21:263-5.
44. Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, et al. The structure of haplotype blocks in the human genome. Science. 2002;296:2225-9.
45. Lewontin RC. The interaction of selection and linkage. I. General considerations; heterotic models. Genetics. 1964;49:49-67.
46. Veroneze R, Bastiaansen JW, Knol EF, Guimarães SE, Silva FF, Harlizius B, et al. Linkage disequilibrium patterns and persistence of phase in purebred and crossbred pig (Sus scrofa) populations. BMC Genet. 2014;15:126.
47. Meuwissen TH, Hayes BJ, Goddard ME. Prediction of total genetic value using genome-wide dense marker maps. Genetics. 2001;157:1819-29.
48. Sandelin A, Alkema W, Engström P, Wasserman WW, Lenhard B. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 2004;32:D91-4 (Database issue).
49. Touzet H, Varré JS. Efficient and accurate P-value computation for Position Weight Matrices. Algorithms Mol Biol. 2007;2:15.
50. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498-504.
51. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics. 2005;21:3448-9.
52. Canario L, Cantoni E, Le Bihan E, Caritez JC, Billon Y, Bidanel JP, et al. Between-breed variability of stillbirth and its relationship with sow and piglet characteristics. J Anim Sci. 2006;84:3185-96.
53. Varona L, Sorensen D. A genetic analysis of mortality in pigs. Genetics. 2010;184:277-84.
54. Guo YM, Lee GJ, Archibald AL, Haley CS. Quantitative trait loci for production traits in pigs: a combined analysis of two Meishan x Large White populations. Anim Genet. 2008;39:486-95.
55. Lee SS, Chen Y, Moran C, Cepica S, Reiner G, Bartenschlager H, et al. Linkage and QTL mapping for Sus scrofa chromosome 2. J Anim Breed Genet. 2003;120:11-9.
56. King AH, Jiang Z, Gibson JP, Haley CS, Archibald AL. Mapping quantitative trait loci affecting female reproductive traits on porcine chromosome 8. Biol Reprod. 2003;68:2172-9.
57. Sato S, Atsuji K, Saito N, Okitsu M, Sato S, Komatsuda A, et al. Identification of quantitative trait loci affecting corpora lutea and number of teats in a Meishan × Duroc F2 resource population. J Anim Sci. 2006;84:2895-901.
58. Mezzano S, Aros C, Droguett A, Burgos ME, Ardiles L, Flores C, et al. NF-KB activation and overexpression of regulated genes in human diabetic nephropathy. Nephrol Dial Transplant. 2004;19:2505-12.
59. Behr R, Brestelli J, Fulmer JT, Miyawaki N, Kleyman TR, Kaestner KH. Mild nephrogenic diabetes insipidus caused by Foxa1 deficiency. J Biol Chem. 2004;279:41936-41.
60. Levinson RS, Batourina E, Choi C, Vorontchikhina M, Kitajewski J, Mendelsohn CL. Foxd1-dependent signals control cellularity in the renal capsule, a structure required for normal renal development. Development. 2005;132:529-39.
61. Yoshida T, Yamashita M, Horimai C, Hayashi M. Deletion of Krüppel-like factor 4 in endothelial and hematopoietic cells enhances neointimal formation following vascular injury. J Am Heart Assoc. 2014;3:e000622.
62. Fragoso MCB, Almeida MQ, Mazzuco TL, Mariani BM, Brito LP, Gonçalves TC, et al. Combined expression of BUB1B, DLGAP5, and PINK1 as predictors of poor outcome in adrenocortical tumors: validation in a Brazilian cohort of adult and pediatric patients. Eur J Endocrinol. 2012;166:61-7.
63. Arregger AL, Cardoso EM, Zucchini A, Aguirre EC, Elbert A, Contreras LN. Adrenocortical function in hypotensive patients with end stage renal disease. Steroids. 2014;84:57-63.
64. Gigante B, Bellis A, Visconti R, Marino M, Morisco C, Trimarco V, et al. Retrospective analysis of coagulation factor II receptor (F2R) sequence variation and coronary heart disease in hypertensive patients. Arterioscler Thromb Vasc Biol. 2007;27:1213-9.
65. Cho GJ, Hong SC, Oh MJ, Kim HJ. Vitamin D deficiency in gestational diabetes mellitus and the role of the placenta. Am J Obstet Gynecol. 2013;209:560.e1-8.
66. Kakoola DN, Curcio-Brint A, Lenchik NI, Gerling IC. Molecular pathway alterations in CD4 T-cells of nonobese diabetic (NOD) mice in the preinsulitis phase of autoimmune diabetes. Results Immunol. 2014;4:30-45.
67. Woroniecka KI, Park ASD, Mohtat D, Thomas DB, Pullman JM, Susztak K. Transcriptome analysis of human diabetic kidney disease. Diabetes. 2011;60:2354-69.
68. Feng X, Tang H, Leng J, Jiang Q. Suppressors of cytokine signaling (SOCS) and type 2 diabetes. Mol Biol Rep. 2014;41:2265-74.
69. Parisi MA, Bennett CL, Eckert ML, Dobyns WB, Gleeson JG, Shaw DW, et al. The NPHP1 gene deletion associated with juvenile nephronophthisis is present in a subset of individuals with Joubert syndrome. Am J Hum Genet. 2004;75:82-91.
70. Saravia JM, Baraister M. Joubert syndrome: a review. Am J Med Genet. 1992;43:726-31.
71. Wunderle VM, Critcher R, Hastie N, Goodfellow PN, Schedl A. Deletion of long-range regulatory elements upstream of SOX9 causes campomelic dysplasia. Proc Nat Acad Sci USA. 1998;95:10649-54.
72. Mansour S, Hall CM, Pembrey ME, Young ID. A clinical and genetic study of campomelic dysplasia. J Med Genet. 1995;32:415-20.
73. Jain S, Maltepe E, Lu MM, Simon C, Bradfield CA. Expression of ARNT, ARNT2, HIF1α, HIF2 α and Ah receptor mRNAs in the developing mouse. Mech Dev. 1998;73:117-23.
74. Choi YS, Chakrabarti R, Escamilla-Hernandez R, Sinha S. Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev Biol. 2009;329:227-41.
75. 3 receptor on growth-regulatory pathways in mammary gland and breast cancer. J Steroid Biochem Mol Biol. 2002;83:85-92.
76. Blalock WL, Piazzi M, Bavelloni A, Raffini M, Faenza I, D'Angelo A, et al. Identification of the PKR nuclear interactome reveals roles in ribosome biogenesis, mRNA processing and cell division. J Cell Physiol. 2014;229:1047-60.
77. Wang L, Zhang L, Yan H, Liu X, Li N, Liang J, et al. Genome-wide association studies identify the loci for 5 exterior traits in a Large White × Minzhu pig population. PLoS One. 2014;9:e103766.
78. Pistocchi A, Bartesaghi S, Cotelli F, Del Giacco L. Identification and expression pattern of zebrafish prox2 during embryonic development. Dev Dyn. 2008;237:3916-20.
79. Sato S, Hanada R, Kimura A, Abe T, Matsumoto T, Iwasaki M, et al. Central control of bone remodeling by neuromedin U. Nat Med. 2007;13:1234-40.
80. Horikoshi T, Maeda K, Kawaguchi Y, Chiba K, Mori K, Koshizuka Y, et al. A large-scale genetic association study of ossification of the posterior longitudinal ligament of the spine. Hum Genet. 2006;119:611-6.
81. 2+ ATPase (SPCA1). Biochem Biophys Res Commun. 2014;445:417-21.