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

Jonathan E Valencia,Robert D Burke,Isabelle S Peter,Roberto Feuda,Dan O Mellott

doi:10.1186/s12915-021-01194-y

Abstract

BackgroundThe 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.ResultsLarvae 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.ConclusionsBased 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.

Highlights

The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution
Two classes of photoreceptors are commonly encountered in bilateria, ciliary photoreceptors, which are predominantly deployed in deuterostomes, and rhabdomeric photoreceptors, which are typically present in protostomes [8, 9]
When expression of rx was examined in sea urchin larvae by whole-mount in situ hybridization (WMISH), expression was found to be restricted to bilateral clusters of 1–3 cells located on the oral side of the neurogenic apical ectoderm at 72 h after fertilization (Fig. 1A)

Summary

Introduction

The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution. The remarkable similarity among certain cell types in distantly related animals suggests that some cell types have been present as a functional unit for a very long time during animal evolution [1,2,3] The similarity between these cell types is reflected in specific structural and functional properties and at the molecular level in the expression of similar gene sets. Ciliary and rhabdomeric photoreceptors are morphologically distinct by possessing different cell surface extensions that increase the photosensitive area. They are molecularly distinct by deploying different pathways for transducing the intracellular response to photo-excitement [14]. Data from different clades across the phylogeny are required to resolve the evolutionary history of photoreceptor cell types within bilateria

Methods

Results

Discussion

Conclusion