A New Model Organism to Investigate Extraocular Photoreception: Opsin and Retinal Gene Expression in the Sea Urchin Paracentrotus lividus

Molecular research on the evolution of extraocular photoreception has drawn attention to photosensitive animals lacking proper eye organs. Outside of vertebrates, little is known about this type of sensory system in any other deuterostome. In this study, we investigate such an extraocular photoreceptor cell (PRC) system in developmental stages of the sea urchin Paracentrotus lividus. We provide a general overview of the cell type families present at the mature rudiment stage using single-cell transcriptomics, while emphasizing the PRCs complexity. We show that three neuronal and one muscle-like PRC type families express retinal genes prior to metamorphosis. Two of the three neuronal PRC type families express a rhabdomeric opsin as well as an echinoderm-specific opsin (echinopsin), and their genetic wiring includes sea urchin orthologs of key retinal genes such as hlf, pp2ab56e, barh, otx, ac/sc, brn3, six1/2, pax6, six3, neuroD, irxA, isl and ato. Using qPCR, in situ hybridization, and immunohistochemical analysis, we found that the expressed retinal gene composition becomes more complex from mature rudiment to juvenile stage. The majority of retinal genes are expressed dominantly in the animals’ podia, and in addition to the genes already expressed in the mature rudiment, the juvenile podia express a ciliary opsin, another echinopsin, and two Go-opsins. The expression of a core of vertebrate retinal gene orthologs indicates that sea urchins have an evolutionarily conserved gene regulatory toolkit that controls photoreceptor specification and function, and that their podia are photosensory organs.