Abstract
Newcastle disease (ND) and avian infectious bronchitis (IB) are contagious diseases of chickens. To identify genes associated with antibody levels against ND and IB, a genome-wide association study was performed using specific-locus amplified fragment sequencing (SLAF-seq) technology in Jinghai yellow chickens. This determined six single-nucleotide polymorphisms (SNPs) that were associated with antibody levels against Newcastle disease virus (NDV): rsZ2494661, rsZ2494710, rs1211307701, rs1211307711, rs1218289310 and rs420701988. Of these, rsZ2494661 and rsZ2494710 reached the 5 % Bonferroni genome-wide significance level (5.5E-07) and they were both 134.7 kb downstream of the SETBP1 gene. The remaining four SNPs had ‘suggestive’ genome-wide significance levels (1.1E-05) and they were within or near the Plexin B1, LRRN1 and PDGFC genes. IB had two SNPs associated with antibody levels: rs149988433 and rs16170823; both reached chromosome-wide significance levels and they were near the USP7 and TRIM27 genes, respectively. Bioinformatics, GO annotation and pathway analysis indicated that five of these genes (Plexin B1, TRIM27, PDGFC, SETBP1 and USP7) may be important for the generation of protective antibodies against NDV and infectious bronchitis virus (IBV). This paves the way for further research on host immune responses against NDV.
Similar content being viewed by others
References
Aldous EW, Alexander DJ (2001) Detection and differentiation of Newcastle disease virus (avian paramyxovirus type 1). Avian Pathol 30(2):117–128
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19(9):1655–1664
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402
Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh LS (2004) UniProt: the Universal Protein knowledgebase. Nucleic Acids Res 32(Database issue):D115–D119
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25(1):25–29
Barbezange C, Jestin V (2005) Molecular study of the quasispecies evolution of a typical pigeon paramyxovirus type 1 after serial passages in pigeons by contact. Avian Pathol 34(2):111–122
Biscarini F, Bovenhuis H, van Arendonk JAM, Parmentier HK, Jungerius AP, van der Poel JJ (2010) Across‐line SNP association study of innate and adaptive immune response in laying hens. Anim Genet 41(1):26–38
Cavanagh D (2001) A nomenclature for avian coronavirus isolates and the question of species status. Avian Pathol 30(2):109–115
Cavanagh D (2007) Coronavirus avian infectious bronchitis virus. Vet Res 38(2):281–297
Cavanagh D, Naqi S (2003) Infectious bronchitis. Dis Poult 11:101–119
Cheng C, Niu C, Yang Y, Wang Y, Lu M (2013) Expression of HAUSP in gliomas correlates with disease progression and survival of patients. Oncol Rep 29(5):1730–1736
Damola A, Legendre A, Ball S, Masters JR, Williamson M (2013) Function of mutant and wild-type plexinb1 in prostate cancer cells. Prostate 73(12):1326–1335
Deng Y, Li J, Wu S, Zhu Y, Chen Y, He F (2006) Integrated nr Database in Protein Annotation System and Its Localization. Comput Eng 32(5):71–74
Fernandez-Mercado M, Pellagatti A, Di Genua C, Larrayoz MJ, Winkelmann N, Aranaz P, Burns A, Schuh A, Calasanz MJ, Cross NC, Boultwood J (2013) Mutations in SETBP1 are recurrent in myelodysplastic syndromes and often coexist with cytogenetic markers associated with disease progression. Br J Haematol 163(2):235–239
Gu X, Feng C, Ma L, Song C, Wang Y, Da Y, Li H, Chen K, Ye S, Ge C, Hu X, Li N (2011) Genome-wide association study of body weight in chicken F2 resource population. PLoS One 6(7):e21872
Hou HA, Kuo YY, Tang JL, Chou WC, Yao M, Lai YJ, Lin CC, Chen CY, Liu CY, Tseng MH, Huang CF, Chiang YC, Lee FY, Liu MC, Liu CW, Huang SY, Ko BS, Wu SJ, Tsay W, Chen YC, Tien HF (2014) Clinical implications of the SETBP1 mutation in patients with primary myelodysplastic syndrome and its stability during disease progression. Am J Hematol 89(2):181–186
Ignjatović J, Sapats S (2000) Avian infectious bronchitis virus. Rev Sci Tech 19(2):493–508
Ioannidis JP, Thomas G, Daly MJ (2009) Validating, augmenting and refining genome-wide association signals. Nat Rev Genet 10(5):318–329
Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25(15):1966–1967
Li DF, Lian L, Qu LJ, Chen YM, Liu WB, Chen SR, Zheng JX, Xu GY, Yang N (2013) A genome-wide SNP scan reveals two loci associated with the chicken resistance to Marek’s disease. Anim Genet 44(2):217–222
Liu W, Li D, Liu J, Chen S, Qu L, Zheng J, Xu G, Yang N (2011) A genome-wide SNP scan reveals novel loci for egg production and quality traits in white leghorn and brown-egg dwarf layers. PLoS One 6(12):e28600
Liu R, Sun Y, Zhao G, Wang F, Wu D, Zheng M, Chen J, Zhang L, Hu Y, Wen J (2013) Genome-wide association study identifies loci and candidate genes for body composition and meat quality traits in Beijing-You chickens. PLoS One 8(4):e61172
Luo C, Qu H, Ma J, Wang J, Li C, Yang C, Hu X, Li N, Shu D (2013) Genome-wide association study of antibody response to Newcastle disease virus in chicken. BMC Genet 14(1):42
Makishima H, Yoshida K, Nguyen N, Przychodzen B, Sanada M, Okuno Y, Ng KP, Gudmundsson KO, Vishwakarma BA, Jerez A, Gomez-Segui I, Takahashi M, Shiraishi Y, Nagata Y, Guinta K, Mori H, Sekeres MA, Chiba K, Tanaka H, Muramatsu H, Sakaguchi H, Paquette RL, McDevitt MA, Kojima S, Saunthararajah Y, Miyano S, Shih LY, Du Y, Ogawa S, Maciejewski JP (2013) Somatic SETBP1 mutations in myeloid malignancies. Nat Genet 45(8):942–946
Noorai RE, Freese NH, Wright LM, Chapman SC, Clark LA (2012) Genome-wide association mapping and identification of candidate genes for the rumpless and ear-tufted traits of the Araucana chicken. PLoS One 7(7):e40974
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81(3):559–575
Saridakis V, Sheng Y, Sarkari F, Holowaty MN, Shire K, Nguyen T, Zhang RG, Liao J, Lee W, Edwards AM, Arrowsmith CH, Frappier L (2005) Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein–Barr nuclear antigen 1: implications for EBV-mediated immortalization. Mol Cell 18(1):25–36
Shiina T, Briles WE, Goto RM, Hosomichi K, Yanagiya K, Shimizu S, Inoko H, Miller MM (2007) Extended gene map reveals tripartite motif, C-type lectin, and Ig superfamily type genes within a subregion of the chicken MHC-B affecting infectious disease. J Immunol 178(11):7162–7172
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8(3):e58700
Tang Y, Zhang T, Zhang G, Wang J, Fan Q, Chen X, Wei Y, Han K, Wang Y (2014) Eight SNPs of the Myf5 gene and diplotypes associated with growth and reproductive traits in Jinghai yellow chicken. Mol Biol Rep 41(10):6837–6844
van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, Colland F, Maurice MM, Burgering BM (2006) FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol 8(10):1064–1073
Wolc A, Arango J, Settar P, Fulton JE, O’Sullivan NP, Preisinger R, Habier D, Fernando R, Garrick DJ, Hill WG, Dekkers JC (2012) Genome-wide association analysis and genetic architecture of egg weight and egg uniformity in layer chickens. Anim Genet 43(Suppl 1):87–96
Worzfeld T, Swiercz JM, Looso M, Straub BK, Sivaraj KK, Offermanns S (2012) ErbB-2 signals through Plexin-B1 to promote breast cancer metastasis. J Clin Invest 122(4):1296–1305
Xie L, Luo C, Zhang C, Zhang R, Tang J, Nie Q, Ma L, Hu X, Li N, Da Y, Zhang X (2012) Genome-wide association study identified a narrow chromosome 1 region associated with chicken growth traits. PLoS One 7(2):e30910
Yonash N, Cheng HH, Hillel J, Heller DE, Cahaner A (2001) DNA microsatellites linked to quantitative trait loci affecting antibody response and survival rate in meat-type chickens. Poult Sci 80(1):22–28
Zhang Z, Ersoz E, Lai C-Q, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355–360
Zhou C, Wong OGW, Masters JR, Williamson M (2012) Effect of cancer-associated mutations in the PlexinB1 gene. Mol Cancer 11:11
Zoumpoulidou G, Broceño C, Li H, Bird D, Thomas G, Mittnacht S (2012) Role of the tripartite motif protein 27 in cancer development. J Natl Cancer Inst 104(12):941–952
Zurek B, Schoultz I, Neerincx A, Napolitano LM, Birkner K, Bennek E, Sellge G, Lerm M, Meroni G, Söderholm JD, Kufer TA (2012) TRIM27 negatively regulates NOD2 by ubiquitination and proteasomal degradation. PLoS One 7(7):e41255
Acknowledgements
This work was supported by the Natural Science Foundation of Colleges and Universities in Jiang Su Province, China (12KJB230003), the Natural Science Foundation of China (31201793), the National Poultry Industry Technology System of China (nycytx-42-G1-05), the University Preponderant Discipline Construction Project of Jiang Su Province, China, and the Animal Genetic Breeding and Molecular Design Key Laboratory of Jiang Su Province, China.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Maciej Szydlowski
Wenhao Wang and Tao Zhang contributed equally to this study.
Rights and permissions
About this article
Cite this article
Wang, W., Zhang, T., Zhang, G. et al. Genome-wide association study of antibody level response to NDV and IBV in Jinghai yellow chicken based on SLAF-seq technology. J Appl Genetics 56, 365–373 (2015). https://doi.org/10.1007/s13353-014-0269-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13353-014-0269-y