Abstract
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.
Highlights
The lack of introns is typical for most members of the giant G protein-coupled receptor (GPCR) gene family and it has been proposed that many G-protein-coupled receptors are derived and amplified from a single intron-less common progenitor that was encoded by a retrogene[36,37]
Most of the cnidarian opsins far annotated are intron-less genes, at least one opsin in anthozoan Acropora digitifera, CNOP2, has been characterized with two introns[39]. The first of these intron matches, in position and phase, with the first intron of bovine rhodopsin (Fig. S12). Such examples of the first introns to be located in cnidarian opsins are moderately short and have conventional GT-AG donor and acceptor splice sites and it appears that this intron was already present in an opsin gene present in the last common ancestor of eumetazoa
Intron-less opsin genes appear to be a Cnidarian feature, with the original variant of the gene most probably being lost in medusozoans
Summary
The chromophore undergoes a photoisomerization event to form all-trans retinal, that in turn drives the activation of the photopigment Aside from this universally conserved lysine, other important amino acid residues can be found in opsin primary structures. It is well known that light affects many behavioral activities of cnidarians, including diel vertical migration, responses to rapid changes in light intensity and reproduction[13] Their phylogenetic position, simple nervous system and elaborate set of eyes[14] make their visual system of key importance for understanding the early evolution of vision, and for understanding the biology of box jellyfish[15,16,17,18]. 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 both visual and extraocular photoreception in cubozoans
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