Cargando…

Exploring the molecular makeup of support cells in insect camera eyes

Animals typically have either compound eyes, or camera-type eyes, both of which have evolved repeatedly in the animal kingdom. Both eye types include two important kinds of cells: photoreceptor cells, which can be excited by light, and non-neuronal support cells (SupCs), which provide essential supp...

Descripción completa

Detalles Bibliográficos
Autores principales: Rathore, Shubham, Stahl, Aaron, Benoit, Joshua B., Buschbeck, Elke K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10664524/
https://www.ncbi.nlm.nih.gov/pubmed/37993800
http://dx.doi.org/10.1186/s12864-023-09804-5
_version_ 1785148750377779200
author Rathore, Shubham
Stahl, Aaron
Benoit, Joshua B.
Buschbeck, Elke K.
author_facet Rathore, Shubham
Stahl, Aaron
Benoit, Joshua B.
Buschbeck, Elke K.
author_sort Rathore, Shubham
collection PubMed
description Animals typically have either compound eyes, or camera-type eyes, both of which have evolved repeatedly in the animal kingdom. Both eye types include two important kinds of cells: photoreceptor cells, which can be excited by light, and non-neuronal support cells (SupCs), which provide essential support to photoreceptors. At the molecular level deeply conserved genes that relate to the differentiation of photoreceptor cells have fueled a discussion on whether or not a shared evolutionary origin might be considered for this cell type. In contrast, only a handful of studies, primarily on the compound eyes of Drosophila melanogaster, have demonstrated molecular similarities in SupCs. D. melanogaster SupCs (Semper cells and primary pigment cells) are specialized eye glia that share several molecular similarities with certain vertebrate eye glia, including Müller glia. This led us to question if there could be conserved molecular signatures of SupCs, even in functionally different eyes such as the image-forming larval camera eyes of the sunburst diving beetle Thermonectus marmoratus. To investigate this possibility, we used an in-depth comparative whole-tissue transcriptomics approach. Specifically, we dissected the larval principal camera eyes into SupC- and retina-containing regions and generated the respective transcriptomes. Our analysis revealed several common features of SupCs including enrichment of genes that are important for glial function (e.g. gap junction proteins such as innexin 3), glycogen production (glycogenin), and energy metabolism (glutamine synthetase 1 and 2). To evaluate similarities, we compared our transcriptomes with those of fly (Semper cells) and vertebrate (Müller glia) eye glia as well as respective retinas. T. marmoratus SupCs were found to have distinct genetic overlap with both fly and vertebrate eye glia. These results suggest that T. marmoratus SupCs are a form of glia, and like photoreceptors, may be deeply conserved. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09804-5.
format Online
Article
Text
id pubmed-10664524
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-106645242023-11-22 Exploring the molecular makeup of support cells in insect camera eyes Rathore, Shubham Stahl, Aaron Benoit, Joshua B. Buschbeck, Elke K. BMC Genomics Research Animals typically have either compound eyes, or camera-type eyes, both of which have evolved repeatedly in the animal kingdom. Both eye types include two important kinds of cells: photoreceptor cells, which can be excited by light, and non-neuronal support cells (SupCs), which provide essential support to photoreceptors. At the molecular level deeply conserved genes that relate to the differentiation of photoreceptor cells have fueled a discussion on whether or not a shared evolutionary origin might be considered for this cell type. In contrast, only a handful of studies, primarily on the compound eyes of Drosophila melanogaster, have demonstrated molecular similarities in SupCs. D. melanogaster SupCs (Semper cells and primary pigment cells) are specialized eye glia that share several molecular similarities with certain vertebrate eye glia, including Müller glia. This led us to question if there could be conserved molecular signatures of SupCs, even in functionally different eyes such as the image-forming larval camera eyes of the sunburst diving beetle Thermonectus marmoratus. To investigate this possibility, we used an in-depth comparative whole-tissue transcriptomics approach. Specifically, we dissected the larval principal camera eyes into SupC- and retina-containing regions and generated the respective transcriptomes. Our analysis revealed several common features of SupCs including enrichment of genes that are important for glial function (e.g. gap junction proteins such as innexin 3), glycogen production (glycogenin), and energy metabolism (glutamine synthetase 1 and 2). To evaluate similarities, we compared our transcriptomes with those of fly (Semper cells) and vertebrate (Müller glia) eye glia as well as respective retinas. T. marmoratus SupCs were found to have distinct genetic overlap with both fly and vertebrate eye glia. These results suggest that T. marmoratus SupCs are a form of glia, and like photoreceptors, may be deeply conserved. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09804-5. BioMed Central 2023-11-22 /pmc/articles/PMC10664524/ /pubmed/37993800 http://dx.doi.org/10.1186/s12864-023-09804-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Rathore, Shubham
Stahl, Aaron
Benoit, Joshua B.
Buschbeck, Elke K.
Exploring the molecular makeup of support cells in insect camera eyes
title Exploring the molecular makeup of support cells in insect camera eyes
title_full Exploring the molecular makeup of support cells in insect camera eyes
title_fullStr Exploring the molecular makeup of support cells in insect camera eyes
title_full_unstemmed Exploring the molecular makeup of support cells in insect camera eyes
title_short Exploring the molecular makeup of support cells in insect camera eyes
title_sort exploring the molecular makeup of support cells in insect camera eyes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10664524/
https://www.ncbi.nlm.nih.gov/pubmed/37993800
http://dx.doi.org/10.1186/s12864-023-09804-5
work_keys_str_mv AT rathoreshubham exploringthemolecularmakeupofsupportcellsininsectcameraeyes
AT stahlaaron exploringthemolecularmakeupofsupportcellsininsectcameraeyes
AT benoitjoshuab exploringthemolecularmakeupofsupportcellsininsectcameraeyes
AT buschbeckelkek exploringthemolecularmakeupofsupportcellsininsectcameraeyes