Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones

Abstract Background The 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....

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Main Authors: Gaurav Ahuja, Vera Reichel, Daniel Kowatschew, Adnan S. Syed, Aswani Kumar Kotagiri, Yuichiro Oka, Franco Weth, Sigrun I. Korsching
Format: Article
Language:English
Published: BMC 2018-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-4740-8
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spelling doaj-127f15ba8a20443c94af3f2c3ccb8d622020-11-25T01:07:40ZengBMCBMC Genomics1471-21642018-05-0119111410.1186/s12864-018-4740-8Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zonesGaurav Ahuja0Vera Reichel1Daniel Kowatschew2Adnan S. Syed3Aswani Kumar Kotagiri4Yuichiro Oka5Franco Weth6Sigrun I. Korsching7Institute of Genetics, University at CologneInstitute of Genetics, University at CologneInstitute of Genetics, University at CologneInstitute of Genetics, University at CologneInstitute of Genetics, University at CologneInstitute of Genetics, University at CologneKarlsruher Institut fuer Technologie (KIT) - Campus Sued, Zoologisches Institut, Abteilung fuer Zell- und NeurobiologieInstitute of Genetics, University at CologneAbstract Background The 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. Results To 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. Conclusion Our 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.http://link.springer.com/article/10.1186/s12864-018-4740-8In situ hybridizationSpatial distributionOlfactory receptorsV2RsMicrovillous neuronsZebrafish
collection DOAJ
language English
format Article
sources DOAJ
author Gaurav Ahuja
Vera Reichel
Daniel Kowatschew
Adnan S. Syed
Aswani Kumar Kotagiri
Yuichiro Oka
Franco Weth
Sigrun I. Korsching
spellingShingle Gaurav Ahuja
Vera Reichel
Daniel Kowatschew
Adnan S. Syed
Aswani Kumar Kotagiri
Yuichiro Oka
Franco Weth
Sigrun I. Korsching
Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones
BMC Genomics
In situ hybridization
Spatial distribution
Olfactory receptors
V2Rs
Microvillous neurons
Zebrafish
author_facet Gaurav Ahuja
Vera Reichel
Daniel Kowatschew
Adnan S. Syed
Aswani Kumar Kotagiri
Yuichiro Oka
Franco Weth
Sigrun I. Korsching
author_sort Gaurav Ahuja
title Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones
title_short Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones
title_full Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones
title_fullStr Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones
title_full_unstemmed Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones
title_sort overlapping but distinct topology for zebrafish v2r-like olfactory receptors reminiscent of odorant receptor spatial expression zones
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-05-01
description Abstract Background The 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. Results To 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. Conclusion Our 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.
topic In situ hybridization
Spatial distribution
Olfactory receptors
V2Rs
Microvillous neurons
Zebrafish
url http://link.springer.com/article/10.1186/s12864-018-4740-8
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