Animals sense light primarily by an opsin-based photopigment present in a photoreceptor cell. Cnidaria are arguably the most basal phylum containing a well-developed visual system. The evolutionary history of opsins in the animal kingdom has not yet been resolved. Here, we study the evolution of animal opsins by genome-wide analysis of the cubozoan jellyfish Tripedalia cystophora, a cnidarian possessing complex lens-containing eyes and minor photoreceptors. A large number of opsin genes with distinct tissue- and stage-specific expression were identified. Our phylogenetic analysis unequivocally classifies cubozoan opsins as a sister group to c-opsins and documents lineage-specific expansion of the opsin gene repertoire in the cubozoan genome. Functional analyses provided evidence for the use of the Gs-cAMP signaling pathway in a small set of cubozoan opsins, indicating the possibility that the majority of other cubozoan opsins signal via distinct pathways. Additionally, these tests uncovered subtle differences among individual opsins, suggesting possible fine-tuning for specific photoreceptor tasks. Based on phylogenetic, expression and biochemical analysis we propose that rapid lineage- and species-specific duplications of the intron-less opsin genes and their subsequent functional diversification promoted evolution of a large repertoire of both visual and extraocular photoreceptors in cubozoans.

• MeSH
• Cyclic AMP metabolism   MeSH
• Biological Evolution * MeSH
• Cubozoa genetics   metabolism   MeSH
• Gene Expression MeSH
• Photoreceptor Cells metabolism   MeSH
• Phylogeny MeSH
• Genome * MeSH
• Genomics methods   MeSH
• Chromosome Mapping MeSH
• RNA, Messenger genetics   MeSH
• Multigene Family MeSH
• Opsins genetics   metabolism   MeSH
• GTP-Binding Proteins metabolism   MeSH
• Signal Transduction MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Cyclic AMP MeSH
• RNA, Messenger MeSH
• Opsins MeSH
• GTP-Binding Proteins MeSH

Animal eyes can vary in complexity ranging from a single photoreceptor cell shaded by a pigment cell to elaborate arrays of these basic units, which allow image formation in compound eyes of insects or camera-type eyes of vertebrates. The evolution of the eye requires involvement of several distinct components-photoreceptors, screening pigment and genes orchestrating their proper temporal and spatial organization. Analysis of particular genetic and biochemical components shows that many evolutionary processes have participated in eye evolution. Multiple examples of co-option of crystallins, Galpha protein subunits and screening pigments contrast with the conserved role of opsins and a set of transcription factors governing eye development in distantly related animal phyla. The direct regulation of essential photoreceptor genes by these factors suggests that this regulatory relationship might have been already established in the ancestral photoreceptor cell.

• MeSH
• Photoreceptor Cells, Invertebrate physiology   MeSH
• Evolution, Molecular * MeSH
• Ocular Physiological Phenomena genetics   MeSH
• Eye Proteins genetics   MeSH
• Retinal Pigments genetics   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Review MeSH
• Names of Substances
• Eye Proteins MeSH
• Retinal Pigments MeSH