Abstract
The chicken major histocompatibility complex (MHC) is located on the microchromosome 16 and is described as the most variable region in the genome. The genes of the MHC play a central role in the immune system. Particularly, genes encoding proteins involved in the antigen presentation to T cells. Therefore, describing the genetic polymorphism of this region is crucial in understanding host–pathogen interactions. The tandem repeat LEI0258 is located within the core area of the B region of the chicken MHC (MHC-B region) and its genotypes correlate with serology. This marker was used to provide a picture of the worldwide diversity of the chicken MHC-B region and to categorize chicken MHC haplotypes. More than 1,600 animals from 80 different populations or lines of chickens from Africa, Asia, and Europe, including wild fowl species, were genotyped at the LEI0258 locus. Fifty novel alleles were described after sequencing. The resulting 79 alleles were classified into 12 clusters, based on the SNPs and indels found within the sequences flanking the repeats. Furthermore, hypotheses were formulated on the evolutionary dynamics of the region. This study constitutes the largest variability report for the chicken MHC and establishes a framework for future diversity or association studies.
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References
Bacon LD, Witter RL, Crittenden LB, Fadly A, Motta J (1981) B Haplotype influence on Marek's disease, Rous sarcoma, and lymphoid leucosis virus-induced tumors in chickens. Poult Sci 60:1132–1139
Bader SR, Kothlow S, Trapp S, Schwarz SC, Philipp HC, Weigend S, Sharifi AR, Preisinger R, Schmahl W, Kaspers B, Matiasek K (2010) Acute paretic syndrome in juvenile White Leghorn chickens resembles late stages of acute inflammatory demyelinating polyneuropathies in humans. J Neuroinflammation 28:7–7
Banat GR, Tkalcic S, Dzielawa JA, Jackwood MW, Saggese MD, Yates L, Kopulos R, Briles WE, Collisson EW (2012) Association of the chicken MHC B haplotypes with resistance to avian coronavirus. Dev Comp Immunol (Epub ahead of print)
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Belkhir K, Borsa P, Goudet J, Chikhi L, Raufasate N, Bonhomme F (2000) GENETIX, logiciel sous Windows TM pour la génétique des populations In Laboratoire Génome, Populations, Interactions: CNRS UMR5117 Université Montpellier II. CNRS UMR5117 Université Montpellier II, Montpellier
Berthouly C, Bed’Hom B, Tixier-Boichard M, Chen CF, Lee YP, Laloë D, Legros H, Verrier E, Rognon X (2008) Using molecular markers and multivariate methods to study the genetic diversity on local European and Asian chickens breeds. Anim Genet 39:121–129
Berthouly C, Leroy G, Van TN, Thanh HH, Bed’Hom B, Nguyen BT, Vu CC, Monicat F, Tixier-Boichard M, Verrier E, Maillard JC, Rognon X (2009) Genetic analysis of local Vietnamese chickens provides evidence of gene flow from wild to domestic populations. BMC Genet 10:1
Chang CM, Coville JL, Coquerelle G, Gourichon D, Oulmouden A, Tixier-Boichard M (2006) Complete association between a retroviral insertion in the tyrosinase gene and the recessive white mutation in chickens. BMC Genomics 7:19
Chang CS, Chen CF, Berthouly-Salazar C, Chazara O, Lee YP, Chang CM, Chang KH, Bed’hom B, Tixier-Boichard M (2012) A global analysis of molecular markers and phenotypic traits in local chicken breeds in Taiwan. Anim Genet 43:172–182
Chazara O, Pinard-van Der Laan MH, Tixier-Boichard M, Bed’hom B (2008) Molecular genotype investigation of the Gallus gallus major histocompatibility complex. Dev Biol (Basel) 132:271–278
Chazara O, Juul-Madsen HR, Chang CS, Tixier-Boichard M, Bed’hom B (2011) Correlation in chicken between the marker LEI0258 alleles and Major Histocompatibility Complex sequences. BMC Proc Suppl4:S29 doi:10.1186/1753-6561-5-S4-S29
Delany ME, Robinson CM, Goto RM, Miller MM (2009) Architecture and organization of chicken microchromosome 16: order of the NOR, MHC-Y, and MHC-B subregions. J Hered 100:507–514
Downing T, Lynn DJ, Connell S, Lloyd AT, Bhuiyan AK, Silva P, Naqvi AN, Sanfo R, Sow RS, Podisi B, O’Farrelly C, Hanotte O, Bradley DG (2009) Contrasting evolution of diversity at two disease-associated chicken genes. Immunogenetics 61:303–314
Eriksson J, Larson G, Gunnarsson U, Bed’hom B, Tixier-Boichard M, Strömstedt L, Wright D, Jungerius A, Vereijken A, Randi E, Jensen P, Andersson L (2008) Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet 4:e1000010
Fillon V, Zoorob R, Yerle M, Auffray C, Vignal A (1996) Mapping of the genetically independent chicken major histocompatibility complexes B@ and RFP-Y@ to the same microchromosome by two-color fluorescent in situ hybridization. Cytogenet Cell Genet 75:7–9
Fulton JE, Juul-Madsen HR, Ashwell CM, McCarron AM, Arthur JA, O’Sullivan NP, Taylor RL Jr (2006) Molecular genotype identification of the Gallus gallus major histocompatibility complex. Immunogenetics 58:407–421
Gärke C, Ytournel F, Bed’hom B, Gut I, Lathrop M, Weigend S, Simianer H (2012) Comparison of SNPs and microsatellites for assessing the genetic structure of chicken populations. Anim Genet 43:419–428
Goto RM, Wang Y, Taylor RL Jr, Wakenell PS, Hosomichi K, Shiina T, Blackmore CS, Briles WE, Miller MM (2009) BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken. Proc Natl Acad Sci U S A 106:16740–16745
Granevitze Z, Hillel J, Chen GH, Cuc NTK, Feldam M, Eding H, Weigend S (2007) Genetic diversity within chicken populations from different continents and management histories. Anim Genet 38:576–583
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hillel J, Groenen MA, Tixier-Boichard M, Korol AB, David L, Kirzhner VM, Burke T, Barre-Dirie A, Crooijmans RP, Elo K, Feldman MW, Freidlin PJ, Mäki-Tanila A, Oortwijn M, Thomson P, Vignal A, Wimmers K, Weigend S (2003) Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet Sel Evol 35:533–557
Hoque MR, Lee SH, Jung KC, Kang BS, Park MN, Lim HK, Choi KD, Lee JH (2011) Discrimination of Korean native chicken populations usings SNPs from mtDNA and MHC polymorphisms. Asian-Aust J Anim Sci 24:1637–1643
Huson DH, Bryant D (2006) Application of phylogenetics networks in evolutionary studies. Mol Biol Evol 23:254–267
Izadi F, Ritland C, Cheng KM (2011) Genetic diversity of the major histocompatibility complex region in commercial and noncommercial chicken flocks using the LEI0258 microsatellite marker. Poult Sci 90:2711–2717
Kaufman J, Milne S, Göbel TW, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 28:923–925
Lee LF, Bacon LD, Yoshida S, Yanagida N, Zhang HM, Witter RL (2004) The efficacy of recombinant fowlpox vaccine protection against Marek’s disease: its dependence on chicken line and B haplotype. Avian Dis 48:129–137
Leroy G, Kayang BB, Youssao IAK, Yapi-Gnaoré CV, Osei-Amponsah R, Loukou NE, Fotsa JC, Benabdeljelil K, Bed’hom B, Tixier-Boichard M, Rognon X (2012) Gene diversity, agroecological structure and introgression patterns among village chicken populations across North. West and Central Africa. BMC Genet 13:34
Lima-Rosa CA, Canal CW, Fallavena PRV, Freitas LB, Salzano FM (2005) LEI0258 microsatellite variability and its relationship to B-F haplotypes in Brazilian (blue-egg Caipira) chickens. Genet Mol Biol 28:386–389
Liu YP, Wu GS, Yao YG, Miao YW, Luikart G, Baig M, Beja-Pereira A, Ding ZL, Palanichamy MG, Zhang YP (2006) Multiple maternal origins of chickens: out of the Asian jungles. Mol Phylogenet Evol 38:12–19
Loywyck V, Bed’Hom B, Pinard-van der Laan M-H, Pitel F, Verrier E, Bijma P (2008) Evolution of polymorphisms at molecular markers in QTL and non-QTL regions in selected lines of chicken. Genet Sel Evol 40:639–661
McConnell SK, Dawson DA, Wardle A, Burke T (1999) The isolation and mapping of 19 tetranucleotide microsatellite markers in the chicken. Anim Genet 30:183–189
Miller MM, Goto RM, Taylor RL Jr, Zoorob R, Auffray C, Briles RW, Briles WE, Bloom SE (1996) Assignment of Rfp-Y to the chicken major histocompatibility complex/NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region. Proc Natl Acad Sci U S A 93:3958–3962
Miller MM, Bacon LD, Hala K, Hunt HD, Ewald SJ, Kaufman J, Zoorob R, Briles WE (2004) 2004 Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56:261–279
Minozzi G, Parmentier HK, Mignon-Grasteau S, Nieuwland MG, Bed’hom B, Gourichon D, Minvielle F, der Laan MH P-v (2008) Correlated effects of selection for immunity in White Leghorn chicken lines on natural antibodies and specific antibody responses to KLH and M. butyricum. BMC Genet 9:5
Muir WM, Wong GK, Zhang Y, Wang J, Groenen MA, Crooijmans RP, Megens HJ, Zhang H, Okimoto R, Vereijken A, Jungerius A, Albers GA, Lawley CT, Delany ME, MacEachern S, Cheng HH (2008) Genome-wide assessment of worldwide chicken SNP genetic diversity indicates significant absence of rare alleles in commercial breeds. Proc Natl Acad Sci U S A 105:17312–17317
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218
O’Neill AM, Livant EJ, Ewald SJ (2009) The chicken BF1 (classical MHC class I) gene shows evidence of selection for diversity in expression and in promoter and signal peptide regions. Immunogenetics 61:289–302
Owen JP, Delany ME, Mullens BA (2008) MHC haplotype involvement in avian resistance to an ectoparasite. Immunogenetics 60:621–631
Petersen A, Chadfield MS, Christensen JP, Christensen H, Bisgaard M (2008) Characterization of small-colony variants of Enterococcus faecalis isolated from chickens with amyloid arthropathy. J Clin Microbiol 46:2686–2691
Pinard MH, Hepkema BG (1993) Biochemical and serological identification of major histocompatibility complex antigens in outbred chickens. Vet Immunol Immunopathol 39:407–419
Pinard-van der Laan MH (2002) Immune modulation: the genetic approach. Vet Immunol Immunopathol 87:199–205
Pinard-van der Laan M-H, Siegel PB, Lamont SJ (1998) Lessons from selection experiments on immune response in the chicken. Avian Poult Biol Rev 9:125–141
Rogers SL, Kaufman J (2008) High allelic polymorphism, moderate sequence diversity and diversifying selection for B-NK but not B-lec, the pair of lectin-like receptor genes in the chicken MHC. Immunogenetics 60:461–475
Rosenberg NA, Burke T, Elo K, Feldman MW, Freidlin PJ, Groenen MA, Hillel J, Mäki-Tanila A, Tixier-Boichard M, Vignal A, Wimmers K, Weigend S (2001) Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds. Genetics 159:699–713
Schou TW, Labouriau R, Permin A, Christensen JP, Sørensen P, Cu HP, Nguyen VK, Juul-Madsen HR (2010) MHC haplotype and susceptibility to experimental infections (Salmonella enteritidis, Pasteurella multocida or Ascaridia galli) in a commercial and an indigenous chicken breed. Vet Immunol Immunopathol 135:52–63
Solinhac R, Leroux S, Galkina S, Chazara O, Feve K, Vignoles F, Morisson M, Derjusheva S, Bed’hom B, Vignal A, Fillon V, Pitel F (2010) Integrative mapping analysis of chicken microchromosome 16 organization. BMC Genomics 11:616
Suzuki K, Kobayashi E, Yamashita H, Uenishi H, Churkina I, Plastow G, Hamasima N, Mitsuhashi T (2012) Structural analysis of MHC alleles in an RSV tumour regression chicken using a BAC library. Anim Genet 43:348–351
Twito T, Weigend S, Blum S, Granevitze Z, Feldman MW, Perl-Treves R, Lavi U, Hillel J (2007) Biodiversity of 20 chicken breeds assessed by SNPs located in gene regions. Cytogenet Genome Res 117:319–326
Acknowledgments
The authors thank Anne-Marie Chaussé (INRA, Nouzilly, France), Xavier Rognon (INRA, Jouy en Josas, France), Yannick Roman (Zoo de Clères, Clères, France), and Cheng Yu-Shin (Livestock Research Institute, Sinhua, Taiwan) for their help collecting DNA samples. They also thank Janet Fulton (Hy-Line International, Dallas Center, USA) for the helpful comments and discussion. This work was supported by a studentship awarded by the French ministry of Higher Education and Research.
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Chazara, O., Chang, CS., Bruneau, N. et al. Diversity and evolution of the highly polymorphic tandem repeat LEI0258 in the chicken MHC-B region. Immunogenetics 65, 447–459 (2013). https://doi.org/10.1007/s00251-013-0697-6
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DOI: https://doi.org/10.1007/s00251-013-0697-6