Abstract
In metazoans, there is a remarkable diversity of photosensitive structures; their shapes, physiology, optical properties, and development are different. To approach the evolution of photosensitive structures and visual function, cephalopods are particularly interesting organisms due to their most highly centralized nervous system and their camerular eyes which constitute a convergence with those of vertebrates. The eye morphogenesis in numerous metazoans is controlled mainly by a conserved Retinal Determination Gene Network (RDGN) including pax, six, eya, and dac playing also key developmental roles in non-retinal structures and tissues of vertebrates and Drosophila. Here we have identified and explored the role of Sof-dac, Sof-six1/2, Sof-eya in eye morphogenesis, and nervous structures controlling the visual function in Sepia officinalis. We compare that with the already shown expressions in eye development of Sof-otx and Sof-pax genes. Rhodopsin is the pigment responsible for light sensitivity in metazoan, which correlate to correlate visual function and eye development. We studied Sof-rhodopsin expression during retina differentiation. By in situ hybridization, we show that (1) all of the RDGN genes, including Sof-pax6, are expressed in the eye area during the early developmental stages but they are not expressed in the retina, unlike Sof-otx, which could have a role in retina differentiation; (2) Sof-rhodopsin is expressed in the retina just before vision gets functional, from stage 23 to hatching. Our results evidence a role of Sof-six1/2, Sof-eya, and Sof-dac in eye development. However, the gene network involved in the retinal photoreceptor differentiation remains to be determined. Moreover, for the first time, Sof-rhodopsin expression is shown in the embryonic retina of cuttlefish suggesting the evolutionary conservation of the role of rhodopsin in visual phototransduction within metazoans. These findings are correlated with the physiological and behavioral observations suggesting that S. officinalis is able to react to light stimuli from stage 25 of organogenesis on, as soon as the first retinal pigments appear.
Highlights
In metazoans, the evolution of photosensitives structures is difficult to establish as there are a high diversity of shapes, at histological and cellular level, and functioning at physiological and optical level, and analogous “eyes” appeared during evolution several times in different lineages (Land, 1988)
No clear expression in retina cells has been shown in the other species. These findings suggest the non-conservation of pax6 in the differentiation of the retinal photoreceptors by the loss of the conserved Retinal Determination Gene Network (RDGN) upstream regulation: this could explain the loss of expression of six, eya, and dac in the retina
The results obtained indicate that three genes important for eye morphogenesis and photoreceptors differentiation in numerous groups of metazoans are involved in eye formation but never in retina cell differentiation during S. officinalis embryonic stages studied (17 to 30)
Summary
The evolution of photosensitives structures is difficult to establish as there are a high diversity of shapes, at histological and cellular level, and functioning at physiological and optical level, and analogous “eyes” appeared during evolution several times in different lineages (Land, 1988). Pax is considered as a universal master gene controlling eye morphogenesis, and its expression is reported in developing photoreceptors (Echelard et al, 1993; Chi and Epstein, 2002; Pichaud and Desplan, 2002; Gehring, 2005; for review see Kumar, 2009). Eye formation is known to be controlled by the Retinal Determination Gene Network (RDGN). It has been shown that pax is an upstream regulator in the RDGN in Drosophila (Czerny et al, 1999) Besides this network, otx (Orthodenticle homeobox 2) and Notch play a key role in photoreceptor cell differentiation and retinal organization (for review see Boyl et al, 2001; Buresi et al, 2012; Koenig et al, 2016). The activated visual pigment molecule (opsin) induces a transduction cascade that results in the opening or closing of cation cGMP-gated channels in the photoreceptors (Hargrave, 2001)
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