Abstract

BackgroundThe draft mouse (Mus musculus) genome sequence revealed an unexpected proliferation of gene duplicates encoding a family of secretoglobin proteins including the androgen-binding protein (ABP) α, β and γ subunits. Further investigation of 14 α-like (Abpa) and 13 β- or γ-like (Abpbg) undisrupted gene sequences revealed a rich diversity of developmental stage-, sex- and tissue-specific expression. Despite these studies, our understanding of the evolution of this gene family remains incomplete. Questions arise from imperfections in the initial mouse genome assembly and a dearth of information about the gene family structure in other rodents and mammals.ResultsHere, we interrogate the latest 'finished' mouse (Mus musculus) genome sequence assembly to show that the Abp gene repertoire is, in fact, twice as large as reported previously, with 30 Abpa and 34 Abpbg genes and pseudogenes. All of these have arisen since the last common ancestor with rat (Rattus norvegicus). We then demonstrate, by sequencing homologs from species within the Mus genus, that this burst of gene duplication occurred very recently, within the past seven million years. Finally, we survey Abp orthologs in genomes from across the mammalian clade and show that bursts of Abp gene duplications are not specific to the murid rodents; they also occurred recently in the lagomorph (rabbit, Oryctolagus cuniculus) and ruminant (cattle, Bos taurus) lineages, although not in other mammalian taxa.ConclusionWe conclude that Abp genes have undergone repeated bursts of gene duplication and adaptive sequence diversification driven by these genes' participation in chemosensation and/or sexual identification.

Highlights

  • The draft mouse (Mus musculus) genome sequence revealed an unexpected proliferation of gene duplicates encoding a family of secretoglobin proteins including the androgenbinding protein (ABP) α, β and γ subunits

  • Rodent gene predictions and nomenclature We revisited the Abp region of the mouse (C57BL/6J strain) genome sequence considering that a recent assembly might contain genes that had been hidden within the gaps of the 2002 initial draft assembly

  • Neither of the two paralogues that we found in Apodemus nor any of the three Abpa genes found in the rat genome shows this property, suggesting that the impressive gene family expansion seen in Mus musculus began in an ancestor common to M. pahari and the subgenus Mus

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Summary

Introduction

The draft mouse (Mus musculus) genome sequence revealed an unexpected proliferation of gene duplicates encoding a family of secretoglobin proteins including the androgenbinding protein (ABP) α, β and γ subunits. The remaining ~10% of genes, representing the volatile portion of the mammalian gene complement, in general possess functions that are very different from those of the conserved gene set: they are substantially enriched in functions contributing to chemosensation, reproduction, immunity, host defense and toxin degradation [3] Gene families, such as those containing olfactory or vomeronasal receptors, immunoglobulin domain-containing proteins, or cytochromes P450 that are expanded in one lineage are often expanded in another. Some among us contributed to initial analyses of the draft mouse genome assembly [2] by identifying mouse-specific gene duplications that remained unduplicated in the human genome We argued that such genes contribute disproportionately to biology that is specific to the rodent lineage [3]. In common with all other members of the secretoglobin family to which they belong, ABP subunits have not unequivocally been assigned molecular functions [12,13,14,15]

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