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.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
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:R43
Cui L, Wall PK, Leebens-Mack JH et al (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749
Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3:e314
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 167:275–304
Force A, Lynch M, Bryan FB, Pickett M, Yan Y, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814
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 6:198
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 15:1696–1705
Hillier LW, Miller W, Birney E et al (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716
Horton R, Wilming L, Rand V et al (2004) Gene map of the extended human MHC. Nat Rev Genet 5:889–899
Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci 86:958–962
Hughes AL, Yeager M, Elshof AET, Chorney MJ (1999) A new taxonomy of mammalian MHC class I molecules. Immunol 20:22–26
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 39:1361–1368
Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617–624
Kim Y, Stephan W (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765–777
Krautwurst D, Yau KW, Reed R (1998) Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95:917–926
Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920
Lundin LG (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16:1–19
Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genomics 3:35–44
Lynch M, O’Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804
Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10:882–891
McLysaght A, Hokamp K, Wolfe KH (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31:204–205
Otto SP, Yong P (2002) The evolution of gene duplicates. Adv Genet 46:451–483
Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197
Reed RR (2000) Regulating olfactory receptor expression: controlling globally, acting locally. Nat Neurosci 7:638–639
Rubin GM, Yandell MD, Wortman JR et al (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215
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 47:55–63
Yap MW, Nisole S, Lynch C, Stoye JP (2004) Trim5 protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci 101:10786–10791
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.
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Darbo, E., Danchin, E.G.J., Mc Dermott, M.F.P. et al. Evolution of major histocompatibility complex by “en bloc” duplication before mammalian radiation. Immunogenetics 60, 423–438 (2008). https://doi.org/10.1007/s00251-008-0301-7
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DOI: https://doi.org/10.1007/s00251-008-0301-7