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Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation

BACKGROUND: The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution. Photoreceptor cell types are particularly broadly distributed throughout Bilateria; however, their evolutionary relationship is so far unresolved. Prev...

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Autores principales: Valencia, Jonathan E., Feuda, Roberto, Mellott, Dan O., Burke, Robert D., Peter, Isabelle S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8642985/
https://www.ncbi.nlm.nih.gov/pubmed/34863182
http://dx.doi.org/10.1186/s12915-021-01194-y
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author Valencia, Jonathan E.
Feuda, Roberto
Mellott, Dan O.
Burke, Robert D.
Peter, Isabelle S.
author_facet Valencia, Jonathan E.
Feuda, Roberto
Mellott, Dan O.
Burke, Robert D.
Peter, Isabelle S.
author_sort Valencia, Jonathan E.
collection PubMed
description BACKGROUND: The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution. Photoreceptor cell types are particularly broadly distributed throughout Bilateria; however, their evolutionary relationship is so far unresolved. Previous studies indicate that ciliary photoreceptors are homologous at least within chordates, and here, we present evidence that a related form of this cell type is also present in echinoderm larvae. RESULTS: Larvae of the purple sea urchin Strongylocentrotus purpuratus have photoreceptors that are positioned bilaterally in the oral/anterior apical neurogenic ectoderm. Here, we show that these photoreceptors express the transcription factor Rx, which is commonly expressed in ciliary photoreceptors, together with an atypical opsin of the G(O) family, opsin3.2, which localizes in particular to the cilia on the cell surface of photoreceptors. We show that these ciliary photoreceptors express the neuronal marker synaptotagmin and are located in proximity to pigment cells. Furthermore, we systematically identified additional transcription factors expressed in these larval photoreceptors and found that a majority are orthologous to transcription factors expressed in vertebrate ciliary photoreceptors, including Otx, Six3, Tbx2/3, and Rx. Based on the developmental expression of rx, these photoreceptors derive from the anterior apical neurogenic ectoderm. However, genes typically involved in eye development in bilateria, including pax6, six1/2, eya, and dac, are not expressed in sea urchin larval photoreceptors but are instead co-expressed in the hydropore canal. CONCLUSIONS: Based on transcription factor expression, location, and developmental origin, we conclude that the sea urchin larval photoreceptors constitute a cell type that is likely homologous to the ciliary photoreceptors present in chordates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01194-y.
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spelling pubmed-86429852021-12-06 Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation Valencia, Jonathan E. Feuda, Roberto Mellott, Dan O. Burke, Robert D. Peter, Isabelle S. BMC Biol Research Article BACKGROUND: The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution. Photoreceptor cell types are particularly broadly distributed throughout Bilateria; however, their evolutionary relationship is so far unresolved. Previous studies indicate that ciliary photoreceptors are homologous at least within chordates, and here, we present evidence that a related form of this cell type is also present in echinoderm larvae. RESULTS: Larvae of the purple sea urchin Strongylocentrotus purpuratus have photoreceptors that are positioned bilaterally in the oral/anterior apical neurogenic ectoderm. Here, we show that these photoreceptors express the transcription factor Rx, which is commonly expressed in ciliary photoreceptors, together with an atypical opsin of the G(O) family, opsin3.2, which localizes in particular to the cilia on the cell surface of photoreceptors. We show that these ciliary photoreceptors express the neuronal marker synaptotagmin and are located in proximity to pigment cells. Furthermore, we systematically identified additional transcription factors expressed in these larval photoreceptors and found that a majority are orthologous to transcription factors expressed in vertebrate ciliary photoreceptors, including Otx, Six3, Tbx2/3, and Rx. Based on the developmental expression of rx, these photoreceptors derive from the anterior apical neurogenic ectoderm. However, genes typically involved in eye development in bilateria, including pax6, six1/2, eya, and dac, are not expressed in sea urchin larval photoreceptors but are instead co-expressed in the hydropore canal. CONCLUSIONS: Based on transcription factor expression, location, and developmental origin, we conclude that the sea urchin larval photoreceptors constitute a cell type that is likely homologous to the ciliary photoreceptors present in chordates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01194-y. BioMed Central 2021-12-04 /pmc/articles/PMC8642985/ /pubmed/34863182 http://dx.doi.org/10.1186/s12915-021-01194-y 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
Valencia, Jonathan E.
Feuda, Roberto
Mellott, Dan O.
Burke, Robert D.
Peter, Isabelle S.
Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
title Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
title_full Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
title_fullStr Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
title_full_unstemmed Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
title_short Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
title_sort ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8642985/
https://www.ncbi.nlm.nih.gov/pubmed/34863182
http://dx.doi.org/10.1186/s12915-021-01194-y
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