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

Abstract 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 unresolv...

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Autores principales:	Jonathan E. Valencia, Roberto Feuda, Dan O. Mellott, Robert D. Burke, Isabelle S. Peter
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Cell type evolution Photoreceptors Regulatory state GRN evolution Echinoderms Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/de94693b5b364593a5d2cdbcc9b1c7f2
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spelling	oai:doaj.org-article:de94693b5b364593a5d2cdbcc9b1c7f22021-12-05T12:25:54ZCiliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation10.1186/s12915-021-01194-y1741-7007https://doaj.org/article/de94693b5b364593a5d2cdbcc9b1c7f22021-12-01T00:00:00Zhttps://doi.org/10.1186/s12915-021-01194-yhttps://doaj.org/toc/1741-7007Abstract 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 GO 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.Jonathan E. ValenciaRoberto FeudaDan O. MellottRobert D. BurkeIsabelle S. PeterBMCarticleCell type evolutionPhotoreceptorsRegulatory stateGRN evolutionEchinodermsBiology (General)QH301-705.5ENBMC Biology, Vol 19, Iss 1, Pp 1-15 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Cell type evolution Photoreceptors Regulatory state GRN evolution Echinoderms Biology (General) QH301-705.5
spellingShingle	Cell type evolution Photoreceptors Regulatory state GRN evolution Echinoderms Biology (General) QH301-705.5 Jonathan E. Valencia Roberto Feuda Dan O. Mellott Robert D. Burke Isabelle S. Peter Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
description	Abstract 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 GO 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.
format	article
author	Jonathan E. Valencia Roberto Feuda Dan O. Mellott Robert D. Burke Isabelle S. Peter
author_facet	Jonathan E. Valencia Roberto Feuda Dan O. Mellott Robert D. Burke Isabelle S. Peter
author_sort	Jonathan E. Valencia
title	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_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_sort	ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
publisher	BMC
publishDate	2021
url	https://doaj.org/article/de94693b5b364593a5d2cdbcc9b1c7f2
work_keys_str_mv	AT jonathanevalencia ciliaryphotoreceptorsinseaurchinlarvaeindicatepandeuterostomecelltypeconservation AT robertofeuda ciliaryphotoreceptorsinseaurchinlarvaeindicatepandeuterostomecelltypeconservation AT danomellott ciliaryphotoreceptorsinseaurchinlarvaeindicatepandeuterostomecelltypeconservation AT robertdburke ciliaryphotoreceptorsinseaurchinlarvaeindicatepandeuterostomecelltypeconservation AT isabellespeter ciliaryphotoreceptorsinseaurchinlarvaeindicatepandeuterostomecelltypeconservation
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Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation

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