Immunogenetics

, 60:423 | Cite as

Evolution of major histocompatibility complex by “en bloc” duplication before mammalian radiation

  • Elodie Darbo
  • Etienne G. J. Danchin
  • Michael F. P. Mc Dermott
  • Pierre Pontarotti
Original Paper

Abstract

Duplications are an important mechanism for the emergence of genetic novelties. Reports on duplicated genes are numerous, and mechanisms for polyploidization or local gene duplication are beginning to be understood. When a local duplication is studied, searches are usually done gene-by-gene, and the size of duplicated segments is not often investigated. Therefore, we do not know if the gene in question has duplicated alone or with other genes, implying that “en bloc” duplications are poorly studied. We propose a method for identification of “en bloc” duplication using mapping, phylogenetic and statistical analyses. We show that two segments present in the major histocompatibility complex (MHC) region of human chromosome 6 have resulted from an “en bloc” duplication that took place between divergence of amniotes and methaterian/eutherian separation. These segments contain members of the same multigenic families, namely olfactory receptors genes, genes encoding proteins containing B30.2 domain, genes encoding proteins containing immunoglobulin V domain and MHC class I genes. We will discuss the fact that olfactory receptors and MHC genes have undergone positive selection, which could have helped in fixation of the surrounding genes.

Keywords

Evolution “En bloc” duplication MHC Phylogeny Hitchhiking effect 

Notes

Acknowledgements

We thank Philippe Monget for discussion, Olivier Chabrol for his help with bioinformatics, Anne Grimaldi and Sophie Roetynck for having initiated this work. This work was supported by the ANR program no. ANR-07-BLAN-0054-01.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Blomme T, Vandepoele K, De Bodt S, Simillion C, Maere S, Van de Peer Y (2006) The gain and loss of genes during 600 million years of vertebrate evolution. Genome Biol 7:R43PubMedCrossRefGoogle Scholar
  3. Cui L, Wall PK, Leebens-Mack JH et al (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749PubMedCrossRefGoogle Scholar
  4. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3:e314PubMedCrossRefGoogle Scholar
  5. Dawkins R, Leelayuwat C, Gaudieri S, Tay G, Hui J, Cattley S, Martinez P, Kulski J (1999) Genomics of the major histocompatibility complex: haplotypes, duplication, retroviruses and disease. Immunol Rev 167:275–304PubMedCrossRefGoogle Scholar
  6. Force A, Lynch M, Bryan FB, Pickett M, Yan Y, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  7. Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814PubMedCrossRefGoogle Scholar
  8. Gouret P, Vitiello V, Balandraud N, Gilles A, Pontarotti P, Danchin EG (2005) FIGENIX: intelligent automation of genomic annotation: expertise integration in a new software platform. BMC Bioinformatics 6:198PubMedCrossRefGoogle Scholar
  9. Henry J, Mather IH, McDermott MF, Pontarotti P (1998) B30.2-like domain proteins: update and new insights into a rapidly expanding family of proteins. Mol Biol Evol 15:1696–1705PubMedGoogle Scholar
  10. Hillier LW, Miller W, Birney E et al (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716CrossRefGoogle Scholar
  11. Horton R, Wilming L, Rand V et al (2004) Gene map of the extended human MHC. Nat Rev Genet 5:889–899PubMedCrossRefGoogle Scholar
  12. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci 86:958–962PubMedCrossRefGoogle Scholar
  13. Hughes AL, Yeager M, Elshof AET, Chorney MJ (1999) A new taxonomy of mammalian MHC class I molecules. Immunol 20:22–26Google Scholar
  14. Jiang Z, Tang H, Ventura M, Cardone MF, Marques-Bonet T, She X, Pevzner PA, Eichler EE (2007) Ancestral reconstruction of segmental duplications reveals punctuated cores of human genome evolution. Nat Genet 39:1361–1368PubMedCrossRefGoogle Scholar
  15. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617–624PubMedCrossRefGoogle Scholar
  16. Kim Y, Stephan W (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765–777PubMedGoogle Scholar
  17. Krautwurst D, Yau KW, Reed R (1998) Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95:917–926PubMedCrossRefGoogle Scholar
  18. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920PubMedCrossRefGoogle Scholar
  19. Lundin LG (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16:1–19PubMedCrossRefGoogle Scholar
  20. Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genomics 3:35–44PubMedCrossRefGoogle Scholar
  21. Lynch M, O’Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804PubMedGoogle Scholar
  22. Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10:882–891PubMedCrossRefGoogle Scholar
  23. McLysaght A, Hokamp K, Wolfe KH (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31:204–205CrossRefGoogle Scholar
  24. Otto SP, Yong P (2002) The evolution of gene duplicates. Adv Genet 46:451–483PubMedCrossRefGoogle Scholar
  25. Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197PubMedCrossRefGoogle Scholar
  26. Reed RR (2000) Regulating olfactory receptor expression: controlling globally, acting locally. Nat Neurosci 7:638–639CrossRefGoogle Scholar
  27. Rubin GM, Yandell MD, Wortman JR et al (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215PubMedCrossRefGoogle Scholar
  28. Tazi-Ahnini R, Henry J, Offer C, Bouissou-Bouchouata C, Mather IH, Pontarotti P (1997) Cloning, localization, and structure of new members of the butyrophilin gene family in the juxta-telomeric region of the major histocompatibility complex. Immunogenetics 47:55–63PubMedCrossRefGoogle Scholar
  29. Yap MW, Nisole S, Lynch C, Stoye JP (2004) Trim5 protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci 101:10786–10791PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Elodie Darbo
    • 1
  • Etienne G. J. Danchin
    • 2
  • Michael F. P. Mc Dermott
    • 3
  • Pierre Pontarotti
    • 1
  1. 1.LATP UMR 6632 CNRS Evolution biologique et ModélisationUniversité de ProvenceMarseille Cedex 03France
  2. 2.UMR IBSV, INRA, UNSA, CNRSCentre de recherche de Sophia-AntipolisSophia-Antipolis CedexFrance
  3. 3.Leeds Institute of Molecular Medicine (LIMM), Wellcome Trust Brenner BuildingSt. James’s University HospitalLeedsUK

Personalised recommendations