From Embryo to Adult Life: Differential Expression of Visual Opsins in the Flatfish Solea senegalensis Under Different Light Spectra and Photoperiods

Abstract

Visual photoreceptors in fish are usually adjusted to the light environment to ensure the highest efficiency and best adaptation. In the Senegalese sole, metamorphosis determines migration from pelagic to benthic habitats, with marked differences in both light intensity and spectrum. Here, we analysed the ontogeny of six visual photopigments, namely, rod opsin (rh1), short wavelength-sensitive (sws1 and sws2), medium wavelength-sensitive (rh2.3 and rh2.4), and long wavelength-sensitive (lws) cone opsins, in sole specimens maintained in light-dark cycles of white (LDW), blue (LDB), red (LDR), and continuous white (LL) lights by using RT-qPCR and in situ hybridisation. Most of the opsins displayed a similar developmental expression pattern under all tested conditions. However, lower transcripts were detected under LDR and LL compared to LDW and LDB. A significant increase in gene expression was detected before and after metamorphosis, reaching minimum transcript levels at hatching and during metamorphosis. Interestingly, green opsins (rh2.3 and rh2.4) displayed a significant increase only before metamorphosis, with their expression remaining low during and after metamorphosis. The rod opsin and short-, medium-, and long-wavelength sensitive cone opsins were detected in retinal photoreceptors of the sole from pre-metamorphic to adult stages by in situ hybridisation. In adults, the short-wavelength cone opsins (sws1 and sws2) were found in single cones, whereas the medium- (rh2.4) and long-wavelength (lws) cone opsins were present in double cones. The results obtained by in situ hybridisation in the retina of developing sole, in terms of number of positive cells and/or intensity of labelling, were consistent with the ontogenetic transcript patterns found by RT-qPCR, suggesting that most of the visual opsin expressions detected in the whole specimens could correspond to retinal expression. Taken together, our results pointed out that the ontogeny of the Senegalese sole is accompanied by remodelling in opsin gene expression, with the green-cone opsins being the most abundant photopigments in pre-metamorphosis and rod opsin the dominant visual photopigment from the completion of metamorphosis onwards. These results enlarge our knowledge of flatfish metamorphosis and ecology and provide useful information to develop light protocols adapted to different ontogenetic stages that could improve welfare and production in sole aquaculture.