Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution

Abstract

Research in eye evolution has mostly focused on eyes residing in the head. In contrast, noncephalic light sensors are far less understood and rather regarded as evolutionary innovations. We established stable transgenesis in the annelid Platynereis, a reference species for evolutionary and developmental comparisons. EGFP controlled by cis-regulatory elements of r-opsin, a characteristic marker for rhabdomeric photoreceptors, faithfully recapitulates known r-opsin expression in the adult eyes, and marks a pair of pigment-associated frontolateral eyelets in the brain. Unexpectedly, transgenic animals revealed an additional series of photoreceptors in the ventral nerve cord as well as photoreceptors that are located in each pair of the segmental dorsal appendages (notopodia) and project into the ventral nerve cord. Consistent with a photosensory function of these noncephalic cells, decapitated animals display a clear photoavoidance response. Molecular analysis of the receptors suggests that they differentiate independent of pax6, a gene involved in early eye development of many metazoans, and that the ventral cells may share origins with the Hesse organs in the amphioxus neural tube. Finally, expression analysis of opn4×-2 and opn4m-2, two zebrafish orthologs of Platynereis r-opsin, reveals that these genes share expression in the neuromasts, known mechanoreceptors of the lateral line peripheral nervous system. Together, this establishes that noncephalic photoreceptors are more widespread than assumed, and may even reflect more ancient aspects of sensory systems. Our study marks significant advance for the understanding of photoreceptor cell (PRC) evolution and development and for Platynereis as a functional lophotrochozoan model system. regulation | transposon | polychaete | worm

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

“…While our work is the first description of this opsin expression pattern in mollusks, opsin-expressing mechanoreceptors have been recently described in the annelid Platynereis, zebrafish and Drosophila (Backfisch et al, 2013;Senthilan et al, 2012). From work on mechanoreception in Drosophila antennae, we now know that opsin is required for anntenal mechanoreceptors to detect vibrations, highlighting a previously unknown role for opsin in senses besides light detection (Senthilan et al, 2012).…”

“…There are at least three major groups of opsins: the r-opsins, c-opsins and Go/RGR (retinal G-protein-coupled receptor) opsins (Porter et al, 2012;Feuda et al, 2012). While c-opsins are typically thought to detect light in vertebrate eyes and r-opsins in invertebrate eyes, various opsins are expressed in the skin of many animals (Ramirez et al, 2011), and opsins have been localized to receptors dispersed across the body of animals from multiple phyla, including cnidarians, echinoderms, annelids and vertebrates (Plachetzki et al, 2012;Raible et al, 2006;Backfisch et al, 2013;Bellono et al, 2013;Fulgione et al, 2014). Because opsins are known to function as light receptors, the cells that express opsin may be dispersed light sensors that could underlie some lightmediated behaviors.…”

Systematics, evolution and phylogeny of Annelida – a morphological perspective

“…The fate of the larval eyes in ontogeny is not completely known as it is, hard to follow especially in large species. Moreover, whereas formerly a replacement by the adult eyes has generally been assumed to occur besides rare cases of persistence Purschke and Nowak, 2013), recent investigations indicate probable persistence even in species for which a replacement by the adult eyes has been assumed (Backfisch et al, 2013). A unique example of larval eyes being transformed into adult eyes occurs in Capitella teleta (Yamaguchi and Seaver, 2013).…”

“…Given the phylogenetic hypothesis of Weigert et al (2014) this means this is a plesiomorphic feature that has been lost secondarily in Sedentaria. On each side the eyes develop from a common anlage and split into two eyes each after initial formation (Dorresteijn, 2005;Backfisch et al, 2013). However, in these taxa several representatives exist which usually possess rather small eyes of unknown affiliation to either larval or adult eyes.…”

Scallop genome provides insights into evolution of bilaterian karyotype and development

“…The involvement of Pax2/5/8, Brn3 and Six4/5 in the noncephalic light sensors has been previously reported in Platynereis midventral photoreceptor cells (PRCs) 41 and amphioxus Hesse organs 42 , both of which are also Pax6-independent and have led to the hypothesis that cephalic and noncephalic PRCs may have different evolutionary origins, with the former dependent on Pax6 and the latter on Pax2/5/8 41 . However, previous investigations were all based on simple light sensors, and the possibility that these non cephalic light sensors may represent evolutionary innovations cannot be excluded 41 . Our finding of Pax2/5/8 as a key regulator in the gene network of scallop mantle eyes provides the first complex eye-based evidence supporting the hypothesis of Pax2/5/8-dependent origin of noncephalic eyes (Fig.…”