Open Access Research article

The Xenopus FcR family demonstrates continually high diversification of paired receptors in vertebrate evolution

Sergey V Guselnikov1, Thaminda Ramanayake2, Aleksandra Y Erilova1, Ludmila V Mechetina1, Alexander M Najakshin1, Jacques Robert2 and Alexander V Taranin1*

Author Affiliations

1 Institute of Cytology and Genetics, Novosibirsk, Russia

2 University of Rochester Medical Centre, Rochester, NY, USA

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BMC Evolutionary Biology 2008, 8:148  doi:10.1186/1471-2148-8-148

Published: 16 May 2008

Abstract

Background

Recent studies have revealed an unexpected diversity of domain architecture among FcR-like receptors that presumably fulfill regulatory functions in the immune system. Different species of mammals, as well as chicken and catfish have been found to possess strikingly different sets of these receptors. To better understand the evolutionary history of paired receptors, we extended the study of FcR-like genes in amphibian representatives Xenopus tropicalis and Xenopus laevis.

Results

The diploid genome of X. tropicalis contains at least 75 genes encoding paired FcR-related receptors designated XFLs. The allotetraploid X. laevis displays many similar genes primarily expressed in lymphoid tissues. Up to 35 domain architectures generated by combinatorial joining of six Ig-domain subtypes and two subtypes of the transmembrane regions were found in XFLs. None of these variants are shared by FcR-related proteins from other studied species. Putative activating XFLs associate with the FcRγ subunit, and their transmembrane domains are highly similar to those of activating mammalian KIR-related receptors. This argues in favor of a common origin for the FcR and the KIR families. Phylogenetic analysis shows that the entire repertoires of the Xenopus and mammalian FcR-related proteins have emerged after the amphibian-amniotes split.

Conclusion

FcR- and KIR-related receptors evolved through continual species-specific diversification, most likely by extensive domain shuffling and birth-and-death processes. This mode of evolution raises the possibility that the ancestral function of these paired receptors was a direct interaction with pathogens and that many physiological functions found in the mammalian receptors were secondary acquisitions or specializations.