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Genomic architecture of MHC-linked odorant receptor gene repertoires among 16 vertebrate species

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Abstract

The recent sequencing and assembly of the genomes of different organisms have shown that almost all vertebrates studied in detail so far have one or more clusters of genes encoding odorant receptors (OR) in close physical linkage to the major histocompatibility complex (MHC). It has been postulated that MHC-linked OR genes could be involved in MHC-influenced mate choice, comprising both pre- as well as post-copulatory mechanisms. We have therefore carried out a systematic comparison of protein sequences of these receptors from the genomes of man, chimpanzee, gorilla, orangutan, rhesus macaque, mouse, rat, dog, cat, cow, pig, horse, elephant, opossum, frog and zebra fish (amounting to a total of 559 protein sequences) in order to identify OR families exhibiting evolutionarily conserved MHC linkage. In addition, we compared the genomic structure of this region within these 16 species, accounting for presence or absence of OR gene families, gene order, transcriptional orientation and linkage to the MHC or framework genes. The results are presented in the form of gene maps and phylogenetic analyses that reveal largely concordant repertoires of gene families, at least among tetrapods, although each of the eight taxa studied (primates, rodents, ungulates, carnivores, proboscids, marsupials, amphibians and teleosts) exhibits a typical architecture of MHC (or MHC framework loci)-linked OR genes. Furthermore, the comparison of the genomic organization of this region has implications for phylogenetic relationships between closely related taxa, especially in disputed cases such as the evolutionary history of even- and odd-toed ungulates and carnivores. Finally, the largely conserved linkage between distinct OR genes and the MHC supports the concept that particular alleles within a given haplotype function in a concerted fashion during self-/non-self-discrimination processes in reproduction.

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Acknowledgements

This work was supported by the Berliner Krebsgesellschaft (Ernst-von-Leyden fellowship to P.S.C.S.), the Monika Kutzner-Stiftung, Berlin (fellowship to T.K.). We are grateful to the VolkswagenStiftung, Hannover, for supporting our research on genes and their products from the human MHC and its vicinity (I/72 740, I/75 196, I/79 989). The authors declare that no competing interests exist.

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Authors and Affiliations

  1. Institut für Immungenetik, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Berlin, Germany

    Pablo Sandro Carvalho Santos, Thomas Kellermann, Barbara Uchanska-Ziegler & Andreas Ziegler

  2. Leibniz Institute for Zoo and Wildlife Research (IZW), Evolutionary Genetics, Berlin, Germany

    Pablo Sandro Carvalho Santos

  3. Institut für Immungenetik, Charité-Universitätsmedizin Berlin, Campus Benjamin Franklin, Freie Universität Berlin, Thielallee 73, 14195, Berlin, Germany

    Pablo Sandro Carvalho Santos & Andreas Ziegler

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  1. Pablo Sandro Carvalho Santos
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  2. Thomas Kellermann
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  3. Barbara Uchanska-Ziegler
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  4. Andreas Ziegler
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Correspondence to Pablo Sandro Carvalho Santos or Andreas Ziegler.

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Santos, P.S.C., Kellermann, T., Uchanska-Ziegler, B. et al. Genomic architecture of MHC-linked odorant receptor gene repertoires among 16 vertebrate species. Immunogenetics 62, 569–584 (2010). https://doi.org/10.1007/s00251-010-0468-6

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  • DOI: https://doi.org/10.1007/s00251-010-0468-6

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