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

Valencia, Jonathan E. and Feuda, Roberto and Mellott, Dan O. and Burke, Robert D. and Peter, Isabelle S. (2019) Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation. . (Unpublished) http://resolver.caltech.edu/CaltechAUTHORS:20190628-103435076

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Abstract

One of the signatures of evolutionarily related cell types is the expression of similar combinations of transcription factors in distantly related animals. Here we present evidence that sea urchin larvae possess bilateral clusters of ciliary photoreceptors that are positioned in the oral/anterior apical neurogenic domain and associated with pigment cells. The expression of synaptotagmin indicates that the photoreceptors are neurons. Immunostaining shows that the sea urchin photoreceptors express an RGR/GO-opsin, opsin3.2, which co-localizes with tubulin on immotile cilia on the cell surface. Furthermore, orthologs of several transcription factors expressed in vertebrate photoreceptors are expressed in sea urchin ciliary photoreceptors, including Otx, Six3, Tbx2/3, and Rx, a transcription factor typically associated with ciliary photoreceptors. Analysis of gene expression during sea urchin development indicates that the photoreceptors derive from the anterior apical neurogenic domain. Thus, based on location, developmental origin, and transcription factor expression, sea urchin ciliary photoreceptors are likely homologous to vertebrate rods and cones. However, we found that genes typically involved in eye development in many animals, including pax6, six1/2, eya, and dac, are not expressed in sea urchin ciliary photoreceptors. Instead, all four genes are co-expressed in the hydropore canal, indicating that these genes operate as a module in an unrelated developmental context. Thus, based on current evidence, we conclude that at least within deuterostomes, ciliary photoreceptors share a common evolutionary origin and express a shared regulatory state that includes Rx, Otx, and Six3, but not transcription factors that are commonly associated with the retinal determination circuit.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/683318DOIDiscussion Paper
ORCID:
AuthorORCID
Peter, Isabelle S.0000-0003-3685-3147
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. We thank Drs. Markus Meister and Daniel Wagenaar for helpful discussions on earlier versions of the manuscript. This work was supported by National Institutes of Health Grants HD 037105 and HD 094047 (to I.S.P.), and by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (2016-03737), awarded to R.D.B. Author contributions: The project was initially conceived by J.V., R.F., and I.S.P; J.V. and R.F. performed WMISH analysis; D.O.M. and R.D.B. contributed antibodies and performed immunostaining; J.V., R.F. and I.S.P. contributed analysis of PSED circuit in the context of GRN evolution; R.F., R.D.B., and I.S.P. wrote the manuscript.
Funders:
Funding AgencyGrant Number
NIHHD 037105
NIHHD 094047
Natural Sciences and Engineering Research Council of Canada (NSERC)2016-03737
Record Number:CaltechAUTHORS:20190628-103435076
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190628-103435076
Official Citation:Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation Jonathan E. Valencia, Roberto Feuda, Dan O Mellott, Robert Burke, Isabelle S Peter bioRxiv 683318; doi: https://doi.org/10.1101/683318
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:96819
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:28 Jun 2019 17:57
Last Modified:28 Jun 2019 17:57

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