Abstract
BackgroundChemical senses are one of the foremost means by which organisms make sense of their environment, among them the olfactory and gustatory sense of vertebrates and arthropods. Both senses use large repertoires of receptors to achieve perception of complex chemosensory stimuli. High evolutionary dynamics of some olfactory and gustatory receptor gene families result in considerable variance of chemosensory perception between species. Interestingly, both ora/v1r genes and the closely related t2r genes constitute small and rather conserved families in teleost fish, but show rapid evolution and large species differences in tetrapods. To understand this transition, chemosensory gene repertoires of earlier diverging members of the tetrapod lineage, i.e. lobe-finned fish such as Latimeria would be of high interest.ResultsWe report here the complete T2R repertoire of Latimeria chalumnae, using thorough data mining and extensive phylogenetic analysis. Eighty t2r genes were identified, by far the largest family reported for any species so far. The genomic neighborhood of t2r genes is enriched in repeat elements, which may have facilitated the extensive gene duplication events resulting in such a large family. Examination of non-synonymous vs. synonymous substitution rates (dN/dS) suggests pronounced positive Darwinian selection in Latimeria T2Rs, conceivably ensuring efficient neo-functionalization of newly born t2r genes. Notably, both traits, positive selection and enrichment of repeat elements in the genomic neighborhood, are absent in the twenty v1r genes of Latimeria. Sequence divergence in Latimeria T2Rs and V1Rs is high, reminescent of the corresponding teleost families. Some conserved sequence motifs of Latimeria T2Rs and V1Rs are shared with the respective teleost but not tetrapod genes, consistent with a potential role of such motifs in detection of aquatic chemosensory stimuli.ConclusionsThe singularly large T2R repertoire of Latimeria may have been generated by facilitating local gene duplication via increased density of repeat elements, and efficient neofunctionalization via positive Darwinian selection.The high evolutionary dynamics of tetrapod t2r gene families precedes the emergence of tetrapods, i.e. the water-to-land transition, and thus constitutes a basal feature of the lobe-finned lineage of vertebrates.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-650) contains supplementary material, which is available to authorized users.
Highlights
Chemical senses are one of the foremost means by which organisms make sense of their environment, among them the olfactory and gustatory sense of vertebrates and arthropods
Both these features are absent in the closely related Latimeria V1Rs, which show much less negative selective pressure than their teleost counterparts. These findings indicate that high evolutionary dynamics of t2r and v1r gene families are not linked to the loss of aquatic life style in tetrapods, but appear to be an ancient evolutionary characteristic of the lobe-finned lineage
To delineate the Latimeria t2r and v1r gene repertoires we performed a recursive search of the preliminary draft of the Latimeria chalumnae genome [18] provided by the Broad Institute [21], using representative T2R and V1R/ORA protein sequences from mouse, frog (Xenopus tropicalis) and zebrafish as initial queries
Summary
Chemical senses are one of the foremost means by which organisms make sense of their environment, among them the olfactory and gustatory sense of vertebrates and arthropods. High evolutionary dynamics of some olfactory and gustatory receptor gene families result in considerable variance of chemosensory perception between species. Both ora/v1r genes and the closely related t2r genes constitute small and rather conserved families in teleost fish, but show rapid evolution and large species differences in tetrapods. Olfactory receptor genes are typically expressed in monogenic fashion, whereas coexpression of receptors shapes the response characteristics of taste cells [1,2,3] All these differences notwithstanding, closely related families do segregate between these two senses, gustatory T2Rs vs olfactory V1Rs, and T1Rs vs V2Rs, respectively. The V1R-related ora gene repertoires of teleosts consist of the same six genes, with an occasional gene loss [10], whereas mammalian v1r gene repertoires are highly species-specific [13]
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