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A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)

Fish possess one olfactory organ called the olfactory epithelium (OE), by which various chemical substances are detected. On the other hand, tetrapods possess two independent olfactory organs called the main olfactory epithelium (MOE) and vomeronasal organ (VNO), each of which mainly detects general...

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Autores principales: Sakuma, Atsuhiro, Zhang, Zicong, Suzuki, Eri, Nagasawa, Tatsuki, Nikaido, Masato
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8822828/
https://www.ncbi.nlm.nih.gov/pubmed/35135614
http://dx.doi.org/10.1186/s40851-022-00189-z
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author Sakuma, Atsuhiro
Zhang, Zicong
Suzuki, Eri
Nagasawa, Tatsuki
Nikaido, Masato
author_facet Sakuma, Atsuhiro
Zhang, Zicong
Suzuki, Eri
Nagasawa, Tatsuki
Nikaido, Masato
author_sort Sakuma, Atsuhiro
collection PubMed
description Fish possess one olfactory organ called the olfactory epithelium (OE), by which various chemical substances are detected. On the other hand, tetrapods possess two independent olfactory organs called the main olfactory epithelium (MOE) and vomeronasal organ (VNO), each of which mainly detects general odorants and pheromones, respectively. Traditionally, the VNO, so-called concentrations of vomeronasal neurons, was believed to have originated in tetrapods. However, recent studies have identified a primordial VNO in lungfish, implying that the origin of the VNO was earlier than traditionally expected. In this study, we examined the presence/absence of the VNO in the olfactory organ of bichir (Polypterus senegalus), which is the most ancestral group of extant bony vertebrates. In particular, we conducted a transcriptomic evaluation of the accessory olfactory organ (AOO), which is anatomically separated from the main olfactory organ (MOO) in bichir. As a result, several landmark genes specific to the VNO and MOE in tetrapods were both expressed in the MOO and AOO, suggesting that these organs were not functionally distinct in terms of pheromone and odorant detection. Instead, differentially expressed gene (DEG) analysis showed that DEGs in AOO were enriched in genes for cilia movement, implying its additional and specific function in efficient water uptake into the nasal cavity other than chemosensing. This transcriptomic study provides novel insight into the long-standing question of AOO function in bichir and suggests that VNO originated in the lineage of lobe-finned fish during vertebrate evolution. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40851-022-00189-z.
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spelling pubmed-88228282022-02-08 A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus) Sakuma, Atsuhiro Zhang, Zicong Suzuki, Eri Nagasawa, Tatsuki Nikaido, Masato Zoological Lett Research Article Fish possess one olfactory organ called the olfactory epithelium (OE), by which various chemical substances are detected. On the other hand, tetrapods possess two independent olfactory organs called the main olfactory epithelium (MOE) and vomeronasal organ (VNO), each of which mainly detects general odorants and pheromones, respectively. Traditionally, the VNO, so-called concentrations of vomeronasal neurons, was believed to have originated in tetrapods. However, recent studies have identified a primordial VNO in lungfish, implying that the origin of the VNO was earlier than traditionally expected. In this study, we examined the presence/absence of the VNO in the olfactory organ of bichir (Polypterus senegalus), which is the most ancestral group of extant bony vertebrates. In particular, we conducted a transcriptomic evaluation of the accessory olfactory organ (AOO), which is anatomically separated from the main olfactory organ (MOO) in bichir. As a result, several landmark genes specific to the VNO and MOE in tetrapods were both expressed in the MOO and AOO, suggesting that these organs were not functionally distinct in terms of pheromone and odorant detection. Instead, differentially expressed gene (DEG) analysis showed that DEGs in AOO were enriched in genes for cilia movement, implying its additional and specific function in efficient water uptake into the nasal cavity other than chemosensing. This transcriptomic study provides novel insight into the long-standing question of AOO function in bichir and suggests that VNO originated in the lineage of lobe-finned fish during vertebrate evolution. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40851-022-00189-z. BioMed Central 2022-02-08 /pmc/articles/PMC8822828/ /pubmed/35135614 http://dx.doi.org/10.1186/s40851-022-00189-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Sakuma, Atsuhiro
Zhang, Zicong
Suzuki, Eri
Nagasawa, Tatsuki
Nikaido, Masato
A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)
title A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)
title_full A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)
title_fullStr A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)
title_full_unstemmed A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)
title_short A transcriptomic reevaluation of the accessory olfactory organ in Bichir (Polypterus senegalus)
title_sort transcriptomic reevaluation of the accessory olfactory organ in bichir (polypterus senegalus)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8822828/
https://www.ncbi.nlm.nih.gov/pubmed/35135614
http://dx.doi.org/10.1186/s40851-022-00189-z
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