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BMC Biol
2021 Dec 04;191:257. doi: 10.1186/s12915-021-01194-y.
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Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation.
Valencia JE
,
Feuda R
,
Mellott DO
,
Burke RD
,
Peter IS
.
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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.
Fig. 1. Spatial expression of rx and opsin 3.2 in photoreceptors of sea urchin larvae. A, A’, A”, A”’ WMISH showing the expression of rx on the oral side of the apical organ at 72 h. B, B’, B”, B”’ WMISH for opsin3.2 expression. C, C’, C” Double-fluorescent WMISH for rx (magenta, C) and opsin3.2 (green, C’), overlay shown in C”. Arrowhead indicates photoreceptors. M, mouth; AO, apical organ; OV, oral view; RLV, right lateral view; LLV, left lateral view; AV, apical view
Fig. 2. Immunostaining showing the expression of opsin 3.2 in neuronal ciliary photoreceptors. Confocal laser scanning images of whole-mount S. purpuratus larvae showing immunostaining A of opsin 3.2 and synaptotagmin B at 72 h and B of opsin3.2 and α-tubulin at 96 h. C Confocal images of co-immunostaining for opsin3.2 (green, C) and synaptotagmin B (magenta, C’), showing co-expression (C”). D Confocal images of co-immunostaining for opsin3.2 with α-tubulin (D’) showing co-localization in cell surface cilia of photoreceptors (D”). E Co-immunostaining of opsin3.2 (green) and pigment cell-specific SP1 (red) showing pigment cells located in proximity to photoreceptors. Arrowheads indicate photoreceptors (A, B, E) and cilia on photoreceptors (D, D’, D”). M, mouth; AO, apical organ; CB, ciliated band
Fig. 3. Expression of photoreceptor regulatory state and PSED genes in sea urchin larvae. A WMISH in 72-h larvae showing the expression of selected regulatory genes in ciliary photoreceptors (arrowheads). Additional regulatory genes expressed in photoreceptors are shown in Fig. 4. B WMISH in 72-h larvae showing the expression of pax6, six1/2, dach, and eya in the hydropore canal (HC). OV, oral view; LLV, left lateral view
Fig. 4. Time course of regulatory gene expression during photoreceptor development. Embryos were stained by WMISH with probes detecting the expression of regulatory genes for which expression was observed in larval photoreceptor cells at 60 and/or 72 h. Developmental stages from pregastrula (24 h) to pluteus larva (72 h) are indicated. OV, oral view; RLV, right lateral view. Scale bars 20 μm
Fig. 5. Developmental spatial expression of PSED regulatory genes. Images of embryos stained by WMISH for expression of four members of the retinal determination network at indicated developmental stages. Co-expression was observed in the hydropore canal but not in photoreceptor cells. HC, hydropore canal; LLV, left lateral view; OV, oral view. Scale bars 20 μm
Fig. 6. Summary diagram showing sea urchin photoreceptors and phylogenetic distribution of photoreceptor-specific regulatory states. A Summary diagram of sea urchin larva showing the expression of regulatory genes in photoreceptors and expression of indicated PSED genes in the hydropore canal (HC). Pigment cells (PC) are associated with photoreceptors and distributed throughout the aboral ectoderm. B Diagram showing the expression of a common set of regulatory genes in ciliary photoreceptors in animals representing specific positions within the phylogenetic tree. DA, deuterostome ancestor; CA, chordate ancestor; VA, vertebrate ancestor