Abstract

BackgroundThe sense of smell is unrivaled in terms of molecular complexity of its input channels. Even zebrafish, a model vertebrate system in many research fields including olfaction, possesses several hundred different olfactory receptor genes, organized in four different gene families. For one of these families, the initially discovered odorant receptors proper, segregation of expression into distinct spatial subdomains within a common sensory surface has been observed both in teleost fish and in mammals. However, for the remaining three families, little to nothing was known about their spatial coding logic. Here we wished to investigate, whether the principle of spatial segregation observed for odorant receptors extends to another olfactory receptor family, the V2R-related OlfC genes. Furthermore we thought to examine, how expression of OlfC genes is integrated into expression zones of odorant receptor genes, which in fish share a single sensory surface with OlfC genes.ResultsTo select representative genes, we performed a comprehensive phylogenetic study of the zebrafish OlfC family, which identified a novel OlfC gene, reduced the number of pseudogenes to 1, and brought the total family size to 60 intact OlfC receptors. We analyzed the spatial pattern of OlfC-expressing cells for seven representative receptors in three dimensions (height within the epithelial layer, horizontal distance from the center of the olfactory organ, and height within the olfactory organ). We report non-random distributions of labeled neurons for all OlfC genes analysed. Distributions for sparsely expressed OlfC genes are significantly different from each other in nearly all cases, broad overlap notwithstanding. For two of the three coordinates analyzed, OlfC expression zones are intercalated with those of odorant receptor zones, whereas in the third dimension some segregation is observed.ConclusionOur results show that V2R-related OlfC genes follow the same spatial logic of expression as odorant receptors and their expression zones intermingle with those of odorant receptor genes. Thus, distinctly different expression zones for individual receptor genes constitute a general feature shared by teleost and tetrapod V2R/OlfC and odorant receptor families alike.

Highlights

  • The sense of smell is unrivaled in terms of molecular complexity of its input channels

  • Qualitative as well as quantitative analysis of expression patterns of rodent and zebrafish odorant receptors has shown that this scattering is not completely random, but that different Olfactory receptors (ORs) segregate into distinct spatial subdomains within a common sensory surface [8, 10, 11]

  • Zebrafish ORs belonging to class C GPCRs (OlfC) family consists of 60 intact genes and 1 pseudogene In previous studies the size of the zebrafish OlfC gene family was given as 46 [22] or 54 intact genes [23], several incomplete and pseudogenes were reported

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Summary

Introduction

The sense of smell is unrivaled in terms of molecular complexity of its input channels. A model vertebrate system in many research fields including olfaction, possesses several hundred different olfactory receptor genes, organized in four different gene families For one of these families, the initially discovered odorant receptors proper, segregation of expression into distinct spatial subdomains within a common sensory surface has been observed both in teleost fish and in mammals. Several hundred to over two thousand different receptor genes convey olfactory signals in mammals [1,2,3] Most of these olfactory receptors belong to one of four different gene families, the initially discovered odorant receptors proper (ORs, [4]), two types of vomeronasal receptors (V1Rs and V2R, respectively), and the trace amine-associated receptors (TAARs), all of which have counterparts in the teleost olfactory system Qualitative as well as quantitative analysis of expression patterns of rodent and zebrafish odorant receptors has shown that this scattering is not completely random, but that different ORs segregate into distinct spatial subdomains within a common sensory surface [8, 10, 11]

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