Abstract
In comparison to complex visual systems, non-directional photoreception – the most primitive form of biological photodetection – has been poorly investigated, although it is essential to many biological processes such as circadian and seasonal rhythms. Here we describe the spatiotemporal expression pattern of the major molecular actors mediating light reception – opsins – localized in the Strongylocentrotus purpuratus larva. In contrast to other zooplanktonic larvae, the echinopluteus lacks photoreceptor cells with observable shading pigments involved in directional visual tasks. Nonetheless, the echinopluteus expresses two distinct classes of opsins: a Go-opsin and a rhabdomeric opsin. The Go-opsin, Sp-opsin3.2, is detectable at early (3 days post fertilization) and four armed pluteus stages (4 days post fertilization) in two cells that flank the apical organ. To rule out the presence of shading pigments involved in directional photoreception, we used electron microscopy to explore the expression domain of Go-opsin Sp-opsin3.2 positive cells. The rhabdomeric opsin Sp-Opsin4 expression is detectable in clusters of cells located around the primary podia at the five-fold ectoderm pentagonal disc stage (day 18-21) and thereafter, thus indicating that Sp-Opsin4 may not be involved in the photoreception mechanism of the larva, but only of the juvenile. We discuss the putative function of the relevant cells in their neural context, and propose a model for understanding simple photodetection in marine larvae.
Highlights
While the vast majority of studies on animal photoreception have so far focused on directional photoreceptors—systems comprising at least one cell with a photosensitive opsin together with shading pigments that enable it to discriminate the directionality of light, less is known about non-directional photoreception, the simplest and earliest evolving type of photoreception
In order to characterize the presence of putative photoreceptor cells in the sea urchin larva we first consulted the transcriptomic expression of S. purpuratus opsins
Various attempts in the amplification with different set of primers of the “echinopsin” Sp-opsin2 did not give any result. Both RNA fluorescence (Figures 1A–C; 3 days post fertilization: dpf larvae, early four armed larvae) and chromogenic (Figures 1D–F; 4dpf, four armed larvae) whole mount in situ hybridization (WMISH) revealed that the Go opsin Sp-opsin3.2 is expressed in two cells arranged bilaterally adjacent the apical organ—i.e., a portion of the epithelium that form the oral hood that is considered to act as central nervous system of the larva (Byrne et al, 2007)—and at the base of the left and right anterolateral arms
Summary
While the vast majority of studies on animal photoreception have so far focused on directional photoreceptors—systems comprising at least one cell with a photosensitive opsin together with shading pigments that enable it to discriminate the directionality of light—, less is known about non-directional photoreception, the simplest and earliest evolving type of photoreception. Non-directional photoreceptors, which can be difficult to detect due to a lack of visible screening pigments, allow the monitoring of absolute light intensities of the environment. They are widely used as an input to the circadian clock system and for a wide variety of other tasks. Opsins are G-protein coupled receptors involved in lightperception. Based on their amino acid sequence, they can be divided into four groups: tetraopsin, xenopsin, Gq-opsin, and c-opsin (Ramirez et al, 2016; for other classifications see: Plachetzki et al, 2007; Arendt, 2008; Koyanagi et al, 2008; Porter et al, 2011; Feuda et al, 2012). The presence of opsins provides a clear landmark for localizing putative photoreceptor cells even in the absence of shading pigments and, as a consequence, the localization of opsin-expressing cells is important for finding directional and non-directional photoreceptors
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