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Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)

BACKGROUND: Insects depend on their olfactory sense as a vital system. Olfactory cues are processed by a rather complex system and translated into various types of behavior. In holometabolous insects like the red flour beetle Tribolium castaneum, the nervous system typically undergoes considerable r...

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Autores principales: Trebels, Björn, Dippel, Stefan, Goetz, Brigitte, Graebner, Maria, Hofmann, Carolin, Hofmann, Florian, Schmid, Freya-Rebecca, Uhl, Mara, Vuong, Minh-Phung, Weber, Vanessa, Schachtner, Joachim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8323255/
https://www.ncbi.nlm.nih.gov/pubmed/34330268
http://dx.doi.org/10.1186/s12915-021-01055-8
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author Trebels, Björn
Dippel, Stefan
Goetz, Brigitte
Graebner, Maria
Hofmann, Carolin
Hofmann, Florian
Schmid, Freya-Rebecca
Uhl, Mara
Vuong, Minh-Phung
Weber, Vanessa
Schachtner, Joachim
author_facet Trebels, Björn
Dippel, Stefan
Goetz, Brigitte
Graebner, Maria
Hofmann, Carolin
Hofmann, Florian
Schmid, Freya-Rebecca
Uhl, Mara
Vuong, Minh-Phung
Weber, Vanessa
Schachtner, Joachim
author_sort Trebels, Björn
collection PubMed
description BACKGROUND: Insects depend on their olfactory sense as a vital system. Olfactory cues are processed by a rather complex system and translated into various types of behavior. In holometabolous insects like the red flour beetle Tribolium castaneum, the nervous system typically undergoes considerable remodeling during metamorphosis. This process includes the integration of new neurons, as well as remodeling and elimination of larval neurons. RESULTS: We find that the sensory neurons of the larval antennae are reused in the adult antennae. Further, the larval antennal lobe gets transformed into its adult version. The beetle’s larval antennal lobe is already glomerularly structured, but its glomeruli dissolve in the last larval stage. However, the axons of the olfactory sensory neurons remain within the antennal lobe volume. The glomeruli of the adult antennal lobe then form from mid-metamorphosis independently of the presence of a functional OR/Orco complex but mature dependent on the latter during a postmetamorphic phase. CONCLUSIONS: We provide insights into the metamorphic development of the red flour beetle’s olfactory system and compared it to data on Drosophila melanogaster, Manduca sexta, and Apis mellifera. The comparison revealed that some aspects, such as the formation of the antennal lobe’s adult glomeruli at mid-metamorphosis, are common, while others like the development of sensory appendages or the role of Orco seemingly differ. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01055-8.
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spelling pubmed-83232552021-07-30 Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst) Trebels, Björn Dippel, Stefan Goetz, Brigitte Graebner, Maria Hofmann, Carolin Hofmann, Florian Schmid, Freya-Rebecca Uhl, Mara Vuong, Minh-Phung Weber, Vanessa Schachtner, Joachim BMC Biol Research Article BACKGROUND: Insects depend on their olfactory sense as a vital system. Olfactory cues are processed by a rather complex system and translated into various types of behavior. In holometabolous insects like the red flour beetle Tribolium castaneum, the nervous system typically undergoes considerable remodeling during metamorphosis. This process includes the integration of new neurons, as well as remodeling and elimination of larval neurons. RESULTS: We find that the sensory neurons of the larval antennae are reused in the adult antennae. Further, the larval antennal lobe gets transformed into its adult version. The beetle’s larval antennal lobe is already glomerularly structured, but its glomeruli dissolve in the last larval stage. However, the axons of the olfactory sensory neurons remain within the antennal lobe volume. The glomeruli of the adult antennal lobe then form from mid-metamorphosis independently of the presence of a functional OR/Orco complex but mature dependent on the latter during a postmetamorphic phase. CONCLUSIONS: We provide insights into the metamorphic development of the red flour beetle’s olfactory system and compared it to data on Drosophila melanogaster, Manduca sexta, and Apis mellifera. The comparison revealed that some aspects, such as the formation of the antennal lobe’s adult glomeruli at mid-metamorphosis, are common, while others like the development of sensory appendages or the role of Orco seemingly differ. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01055-8. BioMed Central 2021-07-30 /pmc/articles/PMC8323255/ /pubmed/34330268 http://dx.doi.org/10.1186/s12915-021-01055-8 Text en © The Author(s) 2021 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
Trebels, Björn
Dippel, Stefan
Goetz, Brigitte
Graebner, Maria
Hofmann, Carolin
Hofmann, Florian
Schmid, Freya-Rebecca
Uhl, Mara
Vuong, Minh-Phung
Weber, Vanessa
Schachtner, Joachim
Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)
title Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)
title_full Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)
title_fullStr Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)
title_full_unstemmed Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)
title_short Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, Herbst)
title_sort metamorphic development of the olfactory system in the red flour beetle (tribolium castaneum, herbst)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8323255/
https://www.ncbi.nlm.nih.gov/pubmed/34330268
http://dx.doi.org/10.1186/s12915-021-01055-8
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