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Home / Equine Research Bank / BMC Genomics / Genetic diversity, evolution and selection in the major hist...
BMC genomics2020; 21(1); 677; doi: 10.1186/s12864-020-07089-6

Genetic diversity, evolution and selection in the major histocompatibility complex DRB and DQB loci in the family Equidae.

Abstract: The mammalian Major Histocompatibility Complex (MHC) is a genetic region containing highly polymorphic genes with immunological functions. MHC class I and class II genes encode antigen-presenting molecules expressed on the cell surface. The MHC class II sub-region contains genes expressed in antigen presenting cells. The antigen binding site is encoded by the second exon of genes encoding antigen presenting molecules. The exon 2 sequences of these MHC genes have evolved under the selective pressure of pathogens. Interspecific differences can be observed in the class II sub-region. The family Equidae includes a variety of domesticated, and free-ranging species inhabiting a range of habitats exposed to different pathogens and represents a model for studying this important part of the immunogenome. While equine MHC class II DRA and DQA loci have received attention, the genetic diversity and effects of selection on DRB and DQB loci have been largely overlooked. This study aimed to provide the first in-depth analysis of the MHC class II DRB and DQB loci in the Equidae family. Results: Three DRB and two DQB genes were identified in the genomes of all equids. The genes DRB2, DRB3 and DQB3 showed high sequence conservation, while polymorphisms were more frequent at DRB1 and DQB1 across all species analyzed. DQB2 was not found in the genome of the Asiatic asses Equus hemionus kulan and E. h. onager. The bioinformatic analysis of non-zero-coverage-bases of DRB and DQB genes in 14 equine individual genomes revealed differences among individual genes. Evidence for recombination was found for DRB1, DRB2, DQB1 and DQB2 genes. Trans-species allele sharing was identified in all genes except DRB1. Site-specific selection analysis predicted genes evolving under positive selection both at DRB and DQB loci. No selected amino acid sites were identified in DQB3. Conclusions: The organization of the MHC class II sub-region of equids is similar across all species of the family. Genomic sequences, along with phylogenetic trees suggesting effects of selection as well as trans-species polymorphism support the contention that pathogen-driven positive selection has shaped the MHC class II DRB/DQB sub-regions in the Equidae.
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Publication Date: 2020-09-30 PubMed ID: 32998693PubMed Central: PMC7525986DOI: 10.1186/s12864-020-07089-6Google Scholar: Lookup
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Summary

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The research article investigates the genetic diversity, evolution and selection in the Major Histocompatibility Complex (MHC) class II DRB and DQB genes in the Equidae family, including various domesticated and free-ranging species. Understanding these genetic elements can provide insights into their immunological functions.

Understanding MHC class II sub-region

  • In mammals, the Major Histocompatibility Complex (MHC) is a group of genes with high levels of polymorphism, or variations, and are of critical importance in immune function. They produce molecules that present antigens, or foreign substances in the body, on cell surfaces.
  • The class II sub-region of the MHC consists of genes expressed in antigen presenting cells. The second exon of these genes, which encodes the antigen binding site, has evolved under the selective pressure of pathogens.
  • Between different species, there are visible differences in the class II sub-region of the MHC.

Role of Equidae in the Study

  • The Equidae family, which includes various domesticated and wild species, live in diverse environments and hence are exposed to different pathogens. This makes them a good model to study the MHC Class II Immunogenome.
  • While prior attention has been given to the equine MHC class II DRA and DQA loci, this study focuses on investigating the genetic diversity and impact of selection on the DRB and DQB loci.

Key Findings

  • Three DRB and two DQB genes were identified in the genomes of all equids. There was high sequence conservation in the genes DRB2, DRB3, and DQB3, while the genes DRB1 and DQB1 showed more frequent polymorphism across different species.
  • There were notable differences among individual genes when the non-zero-coverage-bases of the DRB and DQB genes in 14 equine individual genomes were analyzed.
  • Evolution under positive selection was detected at both DRB and DQB loci. However, no selected amino acid sites were identified in the DQB3 gene.
  • Overall, the MHC class II sub-region in equids is organized similarly across all species in the family, and this consistency, besides genomic sequences and phylogenetic trees, supports the claim that the evolution of MHC class II DRB/DQB sub-regions in the Equidae has been influenced by pathogen-driven positive selection.

Cite This Article

APA
Klumplerova M, Splichalova P, Oppelt J, Futas J, Kohutova A, Musilova P, Kubickova S, Vodicka R, Orlando L, Horin P. (2020). Genetic diversity, evolution and selection in the major histocompatibility complex DRB and DQB loci in the family Equidae. BMC Genomics, 21(1), 677. https://doi.org/10.1186/s12864-020-07089-6

Publication

BMC genomics
ISSN: 1471-2164
NlmUniqueID: 100965258
Country: England
Language: English
Volume: 21
Issue: 1
Pages: 677
PII: 677

Researcher Affiliations

Klumplerova, Marie
  • Department of Animal Genetics, Veterinary and Pharmaceutical University, Brno, Czech Republic.
  • Ceitec VFU, RG Animal Immunogenomics, Brno, Czech Republic.
Splichalova, Petra
  • Department of Animal Genetics, Veterinary and Pharmaceutical University, Brno, Czech Republic.
  • Ceitec VFU, RG Animal Immunogenomics, Brno, Czech Republic.
Oppelt, Jan
  • Ceitec VFU, RG Animal Immunogenomics, Brno, Czech Republic.
  • Ceitec MU, Masaryk University, Kamenice 753/5, 625 00, Brno, Czech Republic.
  • National Centre for Biomolecular research, Faculty of Science, Masaryk University, Kamenice 753/5, 625 00, Brno, Czech Republic.
Futas, Jan
  • Department of Animal Genetics, Veterinary and Pharmaceutical University, Brno, Czech Republic.
  • Ceitec VFU, RG Animal Immunogenomics, Brno, Czech Republic.
Kohutova, Aneta
  • Department of Animal Genetics, Veterinary and Pharmaceutical University, Brno, Czech Republic.
  • Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 753/5, 625 00, Brno, Czech Republic.
Musilova, Petra
  • Department of Genetics and Reproductive Biotechnologies, Veterinary Research Institute, Brno, Czech Republic.
  • Ceitec VRI, RG Animal Cytogenomics, Brno, Czech Republic.
Kubickova, Svatava
  • Department of Genetics and Reproductive Biotechnologies, Veterinary Research Institute, Brno, Czech Republic.
  • Ceitec VRI, RG Animal Cytogenomics, Brno, Czech Republic.
Vodicka, Roman
  • Zoo Prague, U Trojského zámku 120/3, 171 00, Praha 7, Czech Republic.
Orlando, Ludovic
  • Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, 31000, Toulouse, France.
  • Centre for GeoGenetics, Natural History Museum of Denmark, Øster Voldgade 5-7, 1350K, Copenhagen, Denmark.
Horin, Petr
  • Department of Animal Genetics, Veterinary and Pharmaceutical University, Brno, Czech Republic. horin@dior.ics.muni.cz.
  • Ceitec VFU, RG Animal Immunogenomics, Brno, Czech Republic. horin@dior.ics.muni.cz.

MeSH Terms

  • Animals
  • Equidae / classification
  • Equidae / genetics
  • Evolution, Molecular
  • Genetic Speciation
  • Major Histocompatibility Complex / genetics
  • Phylogeny
  • Polymorphism, Genetic
  • Recombination, Genetic
  • Selection, Genetic

Grant Funding

  • CZ.1.05/1.1.00/02.0068 / Central European Institute of Technology CEITEC
  • NPU LQ1601 / Czech National Sustainability Programme

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 82 references
  1. Abi Rached L, McDermott MF, Pontarotti P. The MHC big bang.. Immunol Rev 1999 Feb;167:33-44.
    doi: 10.1111/j.1600-065X.1999.tb01380.xpubmed: 10319249google scholar: lookup
  2. Chowdhary BP. Equine Genomics. 1st Edition. Ames: Wiley-Blackwell; 2013.
  3. Flajnik MF, Kasahara M. Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system.. Immunity 2001 Sep;15(3):351-62.
    doi: 10.1016/S1074-7613(01)00198-4pubmed: 11567626google scholar: lookup
  4. Klein J. Natural history of the major Histocompatability complex. 99t. New York: Wiley; 1986.
  5. Sommer S. The importance of immune gene variability (MHC) in evolutionary ecology and conservation.. Front Zool 2005 Oct 20;2:16.
    doi: 10.1186/1742-9994-2-16pmc: PMC1282567pubmed: 16242022google scholar: lookup
  6. Takahashi K, Rooney AP, Nei M. Origins and divergence times of mammalian class II MHC gene clusters.. J Hered 2000 May-Jun;91(3):198-204.
    doi: 10.1093/jhered/91.3.198pubmed: 10833044google scholar: lookup
  7. Yuhki N, Beck T, Stephens R, Neelam B, O'Brien SJ. Comparative genomic structure of human, dog, and cat MHC: HLA, DLA, and FLA.. J Hered 2007;98(5):390-9.
    doi: 10.1093/jhered/esm056pubmed: 17675392google scholar: lookup
  8. Beck S, Trowsdale J. Sequence organisation of the class II region of the human MHC.. Immunol Rev 1999 Feb;167:201-10.
    doi: 10.1111/j.1600-065X.1999.tb01393.xpubmed: 10319262google scholar: lookup
  9. Hughes AL, Nei M. Evolutionary relationships of class II major-histocompatibility-complex genes in mammals.. Mol Biol Evol 1990 Nov;7(6):491-514.
    pubmed: 2126590doi: 10.1093/oxfordjournals.molbev.a040622google scholar: lookup
  10. Futas J, Horin P. Natural killer cell receptor genes in the family Equidae: not only Ly49.. PLoS One 2013;8(5):e64736.
    doi: 10.1371/journal.pone.0064736pmc: PMC3665701pubmed: 23724088google scholar: lookup
  11. Janova E, Matiasovic J, Vahala J, Vodicka R, Van Dyk E, Horin P. Polymorphism and selection in the major histocompatibility complex DRA and DQA genes in the family Equidae.. Immunogenetics 2009 Jul;61(7):513-27.
    doi: 10.1007/s00251-009-0380-0pubmed: 19557406google scholar: lookup
  12. Kamath PL, Getz WM. Adaptive molecular evolution of the Major Histocompatibility Complex genes, DRA and DQA, in the genus Equus.. BMC Evol Biol 2011 May 18;11:128.
    doi: 10.1186/1471-2148-11-128pmc: PMC3126738pubmed: 21592397google scholar: lookup
  13. Krüger K, Gaillard C, Stranzinger G, Rieder S. Phylogenetic analysis and species allocation of individual equids using microsatellite data.. J Anim Breed Genet 2005 Apr;122 Suppl 1:78-86.
    doi: 10.1111/j.1439-0388.2005.00505.xpubmed: 16130461google scholar: lookup
  14. Vilstrup JT, Seguin-Orlando A, Stiller M, Ginolhac A, Raghavan M, Nielsen SC, Weinstock J, Froese D, Vasiliev SK, Ovodov ND, Clary J, Helgen KM, Fleischer RC, Cooper A, Shapiro B, Orlando L. Mitochondrial phylogenomics of modern and ancient equids.. PLoS One 2013;8(2):e55950.
    doi: 10.1371/journal.pone.0055950pmc: PMC3577844pubmed: 23437078google scholar: lookup
  15. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
    doi: 10.1038/nature12323pubmed: 23803765google scholar: lookup
  16. Jónsson H, Schubert M, Seguin-Orlando A, Ginolhac A, Petersen L, Fumagalli M, Albrechtsen A, Petersen B, Korneliussen TS, Vilstrup JT, Lear T, Myka JL, Lundquist J, Miller DC, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, Stagegaard J, Strauss G, Bertelsen MF, Sicheritz-Ponten T, Antczak DF, Bailey E, Nielsen R, Willerslev E, Orlando L. Speciation with gene flow in equids despite extensive chromosomal plasticity.. Proc Natl Acad Sci U S A 2014 Dec 30;111(52):18655-60.
    doi: 10.1073/pnas.1412627111pmc: PMC4284605pubmed: 25453089google scholar: lookup
  17. Nergadze SG, Lupotto M, Pellanda P, Santagostino M, Vitelli V, Giulotto E. Mitochondrial DNA insertions in the nuclear horse genome.. Anim Genet 2010 Dec;41 Suppl 2:176-85.
    doi: 10.1111/j.1365-2052.2010.02130.xpubmed: 21070293google scholar: lookup
  18. Trifonov VA, Musilova P, Kulemsina AI. Chromosome evolution in Perissodactyla.. Cytogenet Genome Res 2012;137(2-4):208-17.
    doi: 10.1159/000339900pubmed: 22813844google scholar: lookup
  19. Bailey E. Identification and genetics of horse lymphocyte alloantigens.. Immunogenetics 1980;11(5):499-506.
    doi: 10.1007/BF01567818pubmed: 6242885google scholar: lookup
  20. Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI. Nomenclature for the major histocompatibility complexes of different species: a proposal.. Immunogenetics 1990;31(4):217-9.
    pubmed: 2329006doi: 10.1007/bf00204890google scholar: lookup
  21. Gustafson AL, Tallmadge RL, Ramlachan N, Miller D, Bird H, Antczak DF, Raudsepp T, Chowdhary BP, Skow LC. An ordered BAC contig map of the equine major histocompatibility complex.. Cytogenet Genome Res 2003;102(1-4):189-95.
    doi: 10.1159/000075747pubmed: 14970701google scholar: lookup
  22. Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
    doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
  23. Raudsepp T, Finno CJ, Bellone RR, Petersen JL. Ten years of the horse reference genome: insights into equine biology, domestication and population dynamics in the post-genome era.. Anim Genet 2019 Dec;50(6):569-597.
    doi: 10.1111/age.12857pmc: PMC6825885pubmed: 31568563google scholar: lookup
  24. Viļuma A, Mikko S, Hahn D, Skow L, Andersson G, Bergström TF. Genomic structure of the horse major histocompatibility complex class II region resolved using PacBio long-read sequencing technology.. Sci Rep 2017 Mar 31;7:45518.
    pmc: PMC5374520pubmed: 28361880doi: 10.1038/srep45518google scholar: lookup
  25. Miller D, Tallmadge RL, Binns M, Zhu B, Mohamoud YA, Ahmed A, Brooks SA, Antczak DF. Polymorphism at expressed DQ and DR loci in five common equine MHC haplotypes.. Immunogenetics 2017 Mar;69(3):145-156.
    doi: 10.1007/s00251-016-0964-4pmc: PMC5316504pubmed: 27889800google scholar: lookup
  26. Arbanasić H, Galov A, Ambriović-Ristov A, Grizelj J, Arsenos G, Marković B, Dovenski T, Vince S, Curik I. Extensive polymorphism of the major histocompatibility complex DRA gene in Balkan donkeys: perspectives on selection and genealogy.. Anim Genet 2013 Dec;44(6):711-6.
    doi: 10.1111/age.12054pubmed: 23621397google scholar: lookup
  27. Díaz S, Echeverría MG, It V, Posik DM, Rogberg-Muñoz A, Pena NL, Peral-García P, Vega-Pla JL, Giovambattista G. Development of an ELA-DRA gene typing method based on pyrosequencing technology.. Tissue Antigens 2008 Nov;72(5):464-8.
    doi: 10.1111/j.1399-0039.2008.01113.xpubmed: 18764814google scholar: lookup
  28. Díaz S, Giovambattista G, Dulout FN, Peral-García P. Genetic variation of the second exon of ELA-DRB genes in Argentine Creole horses.. Anim Genet 2001 Oct;32(5):257-63.
    doi: 10.1046/j.1365-2052.2001.00779.xpubmed: 11683711google scholar: lookup
  29. Hedrick PW, Parker KM, Miller EL, Miller PS. Major histocompatibility complex variation in the endangered Przewalski's horse.. Genetics 1999 Aug;152(4):1701-10.
    pmc: PMC1460696pubmed: 10430594doi: 10.1093/genetics/152.4.1701google scholar: lookup
  30. Kamath PL, Getz WM. Unraveling the effects of selection and demography on immune gene variation in free-ranging plains zebra (Equus quagga) populations.. PLoS One 2012;7(12):e50971.
    doi: 10.1371/journal.pone.0050971pmc: PMC3522668pubmed: 23251409google scholar: lookup
  31. Villegas-Castagnasso EE, Díaz S, Giovambattista G, Dulout FN, Peral-García P. Analysis of ELA-DQB exon 2 polymorphism in Argentine Creole horses by PCR-RFLP and PCR-SSCP.. J Vet Med A Physiol Pathol Clin Med 2003 Aug;50(6):280-5.
    doi: 10.1046/j.1439-0442.2003.00543.xpubmed: 12887619google scholar: lookup
  32. Vranova M, Alloggio I, Qablan M, Vyskocil M, Baumeisterova A, Sloboda M, Putnova L, Vrtkova I, Modry D, Horin P. Genetic diversity of the class II major histocompatibility DRA locus in European, Asiatic and African domestic donkeys.. Infect Genet Evol 2011 Jul;11(5):1136-41.
    pubmed: 21515411doi: 10.1016/j.meegid.2011.04.010google scholar: lookup
  33. Spurgin LG, Richardson DS. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings.. Proc Biol Sci 2010 Apr 7;277(1684):979-88.
    doi: 10.1098/rspb.2009.2084pmc: PMC2842774pubmed: 20071384google scholar: lookup
  34. Borghans JA, Beltman JB, De Boer RJ. MHC polymorphism under host-pathogen coevolution.. Immunogenetics 2004 Feb;55(11):732-9.
    doi: 10.1007/s00251-003-0630-5pubmed: 14722687google scholar: lookup
  35. Hedrick PW. Balancing selection and MHC.. Genetica 1998-1999;104(3):207-14.
    doi: 10.1023/A:1026494212540pubmed: 10386384google scholar: lookup
  36. Nikolich-Zugich J, Fremont DH, Miley MJ, Messaoudi I. The role of mhc polymorphism in anti-microbial resistance.. Microbes Infect 2004 Apr;6(5):501-12.
    doi: 10.1016/j.micinf.2004.01.006pubmed: 15109966google scholar: lookup
  37. Stear MJ, Innocent GT, Buitkamp J. The evolution and maintenance of polymorphism in the major histocompatibility complex.. Vet Immunol Immunopathol 2005 Oct 18;108(1-2):53-7.
    doi: 10.1016/j.vetimm.2005.07.005pubmed: 16099055google scholar: lookup
  38. Hughes AL, Yeager M. Natural selection at major histocompatibility complex loci of vertebrates.. Annu Rev Genet 1998;32:415-35.
    doi: 10.1146/annurev.genet.32.1.415pubmed: 9928486google scholar: lookup
  39. Meyer D, C Aguiar VR, Bitarello BD, C Brandt DY, Nunes K. A genomic perspective on HLA evolution.. Immunogenetics 2018 Jan;70(1):5-27.
    pmc: PMC5748415pubmed: 28687858doi: 10.1007/s00251-017-1017-3google scholar: lookup
  40. Meyer D, Thomson G. How selection shapes variation of the human major histocompatibility complex: a review.. Ann Hum Genet 2001 Jan;65(Pt 1):1-26.
    doi: 10.1046/j.1469-1809.2001.6510001.xpubmed: 11415519google scholar: lookup
  41. Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation.. Trends Ecol Evol 2000 Dec 1;15(12):496-503.
    doi: 10.1016/S0169-5347(00)01994-7pmc: PMC7134603pubmed: 11114436google scholar: lookup
  42. Kamath PL, Turner WC, Küsters M, Getz WM. Parasite-mediated selection drives an immunogenetic trade-off in plains zebras (Equus quagga).. Proc Biol Sci 2014 May 22;281(1783):20140077.
    pmc: PMC3996612pubmed: 24718761doi: 10.1098/rspb.2014.0077google scholar: lookup
  43. Soller JT, Murua-Escobar H, Willenbrock S, Janssen M, Eberle N, Bullerdiek J, Nolte I. Comparison of the human and canine cytokines IL-1(alpha/beta) and TNF-alpha to orthologous other mammalians.. J Hered 2007;98(5):485-90.
    doi: 10.1093/jhered/esm025pubmed: 17573384google scholar: lookup
  44. Huang J, Zhao Y, Shiraigol W, Li B, Bai D, Ye W, Daidiikhuu D, Yang L, Jin B, Zhao Q, Gao Y, Wu J, Bao W, Li A, Zhang Y, Han H, Bai H, Bao Y, Zhao L, Zhai Z, Zhao W, Sun Z, Zhang Y, Meng H, Dugarjaviin M. Analysis of horse genomes provides insight into the diversification and adaptive evolution of karyotype.. Sci Rep 2014 May 14;4:4958.
    doi: 10.1038/srep04958pmc: PMC4021364pubmed: 24828444google scholar: lookup
  45. Huang J, Zhao Y, Bai D, Shiraigol W, Li B, Yang L, Wu J, Bao W, Ren X, Jin B, Zhao Q, Li A, Bao S, Bao W, Xing Z, An A, Gao Y, Wei R, Bao Y, Bao T, Han H, Bai H, Bao Y, Zhang Y, Daidiikhuu D, Zhao W, Liu S, Ding J, Ye W, Ding F, Sun Z, Shi Y, Zhang Y, Meng H, Dugarjaviin M. Donkey genome and insight into the imprinting of fast karyotype evolution.. Sci Rep 2015 Sep 16;5:14106.
    doi: 10.1038/srep14106pmc: PMC4571621pubmed: 26373886google scholar: lookup
  46. Mashima S. Comparative sequence analysis of equine and human MHC class II DQB genes.. Cytogenet Genome Res 2003;102(1-4):196-200.
    doi: 10.1159/000075748pubmed: 14970702google scholar: lookup
  47. GenBank. https://www.ncbi.nlm.nih.gov/genbank/. Accessed 11 Dec 2017.
  48. IPD-MHC Database. https://www.ebi.ac.uk/ipd/mhc/. Accessed 11 Dec 2017.
  49. Horín P, Matiasovic J. A second locus and new alleles in the major histocompatibility complex class II (ELA-DQB) region in the horse.. Anim Genet 2002 Jun;33(3):196-200.
    doi: 10.1046/j.1365-2052.2002.00839.xpubmed: 12030922google scholar: lookup
  50. Renaud G, Petersen B, Seguin-Orlando A, Bertelsen MF, Waller A, Newton R, Paillot R, Bryant N, Vaudin M, Librado P, Orlando L. Improved de novo genomic assembly for the domestic donkey.. Sci Adv 2018 Apr;4(4):eaaq0392.
    pmc: PMC5938232pubmed: 29740610doi: 10.1126/sciadv.aaq0392google scholar: lookup
  51. Hashimoto K, Hirai M, Kurosawa Y. A gene outside the human MHC related to classical HLA class I genes.. Science 1995 Aug 4;269(5224):693-5.
    doi: 10.1126/science.7624800pubmed: 7624800google scholar: lookup
  52. Ghosh S, Qu Z, Das PJ, Fang E, Juras R, Cothran EG, McDonell S, Kenney DG, Lear TL, Adelson DL, Chowdhary BP, Raudsepp T. Copy number variation in the horse genome.. PLoS Genet 2014 Oct;10(10):e1004712.
    doi: 10.1371/journal.pgen.1004712pmc: PMC4207638pubmed: 25340504google scholar: lookup
  53. Wang W, Wang S, Hou C, Xing Y, Cao J, Wu K, Liu C, Zhang D, Zhang L, Zhang Y, Zhou H. Genome-wide detection of copy number variations among diverse horse breeds by array CGH.. PLoS One 2014;9(1):e86860.
    doi: 10.1371/journal.pone.0086860pmc: PMC3907382pubmed: 24497987google scholar: lookup
  54. Ellis SA, Ballingall KT. Cattle MHC: evolution in action?. Immunol Rev 1999 Feb;167:159-68.
    doi: 10.1111/j.1600-065X.1999.tb01389.xpubmed: 10319258google scholar: lookup
  55. He Y, Xi D, Leng J, Qian T, Jin D, Chen T, Yang C, Hao T, Yang Z, Deng W. Genetic variability of MHC class II DQB exon 2 alleles in yak (Bos grunniens).. Mol Biol Rep 2014;41(4):2199-206.
    doi: 10.1007/s11033-014-3071-3pubmed: 24430299google scholar: lookup
  56. Villanueva-Noriega MJ, Baker CS, Medrano-González L. Evolution of the MHC-DQB exon 2 in marine and terrestrial mammals.. Immunogenetics 2013 Jan;65(1):47-61.
    doi: 10.1007/s00251-012-0647-8pubmed: 23064401google scholar: lookup
  57. Schierup MH, Mikkelsen AM, Hein J. Recombination, balancing selection and phylogenies in MHC and self-incompatibility genes.. Genetics 2001 Dec;159(4):1833-44.
    pmc: PMC1461893pubmed: 11779818doi: 10.1093/genetics/159.4.1833google scholar: lookup
  58. Collette Y, Gilles A, Pontarotti P, Olive D. A co-evolution perspective of the TNFSF and TNFRSF families in the immune system.. Trends Immunol 2003 Jul;24(7):387-94.
    doi: 10.1016/S1471-4906(03)00166-2pubmed: 12860530google scholar: lookup
  59. Těšický M, Vinkler M. Trans-Species Polymorphism in Immune Genes: General Pattern or MHC-Restricted Phenomenon?. J Immunol Res 2015;2015:838035.
    doi: 10.1155/2015/838035pmc: PMC4458282pubmed: 26090501google scholar: lookup
  60. Takahata N, Nei M. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci.. Genetics 1990 Apr;124(4):967-78.
    pmc: PMC1203987pubmed: 2323559doi: 10.1093/genetics/124.4.967google scholar: lookup
  61. Arbanasić H, Huber Đ, Kusak J, Gomerčić T, Hrenović J, Galov A. Extensive polymorphism and evidence of selection pressure on major histocompatibility complex DLA-DRB1, DQA1 and DQB1 class II genes in Croatian grey wolves.. Tissue Antigens 2013 Jan;81(1):19-27.
    doi: 10.1111/tan.12029pubmed: 23134500google scholar: lookup
  62. Chen YY, Zhang YY, Zhang HM, Ge YF, Wan QH, Fang SG. Natural selection coupled with intragenic recombination shapes diversity patterns in the major histocompatibility complex class II genes of the giant panda.. J Exp Zool B Mol Dev Evol 2010 May 15;314(3):208-23.
    pubmed: 19950128doi: 10.1002/jez.b.21327google scholar: lookup
  63. Schubert M, Ermini L, Der Sarkissian C, Jónsson H, Ginolhac A, Schaefer R, Martin MD, Fernández R, Kircher M, McCue M, Willerslev E, Orlando L. Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX.. Nat Protoc 2014 May;9(5):1056-82.
    doi: 10.1038/nprot.2014.063pubmed: 24722405google scholar: lookup
  64. Schubert M, Ginolhac A, Lindgreen S, Thompson JF, Al-Rasheid KA, Willerslev E, Krogh A, Orlando L. Improving ancient DNA read mapping against modern reference genomes.. BMC Genomics 2012 May 10;13:178.
    doi: 10.1186/1471-2164-13-178pmc: PMC3468387pubmed: 22574660google scholar: lookup
  65. Song K, Li L, Zhang G. Coverage recommendation for genotyping analysis of highly heterologous species using next-generation sequencing technology.. Sci Rep 2016 Oct 20;6:35736.
    doi: 10.1038/srep35736pmc: PMC5071758pubmed: 27760996google scholar: lookup
  66. NCBI clone database. https://www.ncbi.nlm.nih.gov/clone/library/genomic/197/. Accessed 11 Dec 2017.
  67. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  68. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data.. Bioinformatics 2012 Dec 1;28(23):3150-2.
    doi: 10.1093/bioinformatics/bts565pmc: PMC3516142pubmed: 23060610google scholar: lookup
  69. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 2011;17:10–12.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  70. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 1999;41:95–98.
  71. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization.. Brief Bioinform 2019 Jul 19;20(4):1160-1166.
    pmc: PMC6781576pubmed: 28968734doi: 10.1093/bib/bbx108google scholar: lookup
  72. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.. Mol Biol Evol 2013 Dec;30(12):2725-9.
    doi: 10.1093/molbev/mst197pmc: PMC3840312pubmed: 24132122google scholar: lookup
  73. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology.. Bioinformatics 2010 Oct 1;26(19):2455-7.
    doi: 10.1093/bioinformatics/btq429pmc: PMC2944195pubmed: 20671151google scholar: lookup
  74. Kosakovsky Pond SL, Frost SD. Not so different after all: a comparison of methods for detecting amino acid sites under selection.. Mol Biol Evol 2005 May;22(5):1208-22.
    doi: 10.1093/molbev/msi105pubmed: 15703242google scholar: lookup
  75. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. FUBAR: a fast, unconstrained bayesian approximation for inferring selection.. Mol Biol Evol 2013 May;30(5):1196-205.
    doi: 10.1093/molbev/mst030pmc: PMC3670733pubmed: 23420840google scholar: lookup
  76. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection.. PLoS Genet 2012;8(7):e1002764.
    doi: 10.1371/journal.pgen.1002764pmc: PMC3395634pubmed: 22807683google scholar: lookup
  77. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood.. Mol Biol Evol 2007 Aug;24(8):1586-91.
    doi: 10.1093/molbev/msm088pubmed: 17483113google scholar: lookup
  78. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1.. Nature 1993 Jul 1;364(6432):33-9.
    doi: 10.1038/364033a0pubmed: 8316295google scholar: lookup
  79. Bryja J, Galan M, Charbonnel N, Cosson JF. Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae).. Immunogenetics 2006 Apr;58(2-3):191-202.
    doi: 10.1007/s00251-006-0085-6pubmed: 16467985google scholar: lookup
  80. Choi Y, Chan AP. PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels.. Bioinformatics 2015 Aug 15;31(16):2745-7.
    doi: 10.1093/bioinformatics/btv195pmc: PMC4528627pubmed: 25851949google scholar: lookup
  81. Ng PC, Henikoff S. SIFT: Predicting amino acid changes that affect protein function.. Nucleic Acids Res 2003 Jul 1;31(13):3812-4.
    doi: 10.1093/nar/gkg509pmc: PMC168916pubmed: 12824425google scholar: lookup
  82. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations.. Nat Methods 2010 Apr;7(4):248-9.
    doi: 10.1038/nmeth0410-248pmc: PMC2855889pubmed: 20354512google scholar: lookup

Citations

This article has been cited 1 times.
  1. Tozaki T, Ohnuma A, Kikuchi M, Ishige T, Kakoi H, Hirota KI, Kusano K, Nagata SI. Rare and common variant discovery by whole-genome sequencing of 101 Thoroughbred racehorses.. Sci Rep 2021 Aug 6;11(1):16057.
    doi: 10.1038/s41598-021-95669-1pubmed: 34362995google scholar: lookup
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