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Published December 4, 2021 | Supplemental Material + Submitted + Published
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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. 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.

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© The Author(s) 2021. 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/. The Creative Commons Public Domain Dedication waiver (http://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. Received 15 April 2021. Accepted 12 November 2021. Published 04 December 2021. We are grateful to Drs. Markus Meister and Daniel Wagenaar and to the Caltech Neurotechnology Center for the advice and for the helpful discussions on earlier versions of the manuscript. This work was supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (https://www.nichd.nih.gov/) grants HD 037105 and HD095982 awarded to I.S.P. and by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (http://www.nserc-crsng.gc.ca/index_eng.asp; 2016-03737), awarded to R.D.B. Analysis of regulatory gene expression by WMISHs was supported by Eunice Kennedy Shriver National Institute of Child Health and Human Development (https://www.nichd.nih.gov/) grants HD037105 and HD095982 awarded to I.S.P. Immunostaining and production of opsin antibodies were supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (http://www.nserc-crsng.gc.ca/index_eng.asp; 2016-03737), awarded to R.D.B. Jonathan E. Valencia and Roberto Feuda contributed equally to this work. Contributions. The project was initially conceived by J.V., R.F., and I.S.P. J.V., R.F., D.O.M., and R.D.B. performed the research experiments. J.V., R.F., R.D.B., and I.S.P. analyzed the data and wrote the manuscript drafts. I.S.P. edited and wrote the final version of the manuscript. All authors read and approved the final manuscript. Availability of data and materials. All data generated during this study are included in this published article [and its supplementary information files]. Alignments of opsins are available at https://github.com/RobertoFeu/Opsins_phylogeny_Valencia_et_al. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. The authors declare that they have no competing interests.

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August 20, 2023
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