Visual pigments and opsin expression in the juveniles of three species of fish (rainbow trout, zebrafish, and killifish) following prolonged exposure to thyroid hormone or retinoic acid

Abstract

Thyroid hormone (TH) and retinoic acid (RA) are powerful modulators of photoreceptor differentiation during vertebrate retinal development. In the embryos and young juveniles of salmonid fishes and rodents, TH induces switches in opsin expression within individual cones, a phenomenon that also occurs in adult rodents following prolonged (12 week) hypothyroidism. Whether changes in TH levels also modulate opsin expression in the differentiated retina of fish is unknown. Like TH, RA is essential for retinal development, but its role in inducing opsin switches, if any, has not been studied. Here we investigate the action of TH and RA on single-cone opsin expression in juvenile rainbow trout, zebrafish, and killifish and on the absorbance of visual pigments in rainbow trout and zebrafish. Prolonged TH exposure increased the wavelength of maximum absorbance (λmax ) of the rod and the medium (M, green) and long (L, red) wavelength visual pigments in all fish species examined. However, unlike the opsin switch that occurred following TH exposure in the single cones of small juvenile rainbow trout (alevin), opsin expression in large juvenile rainbow trout (smolt), zebrafish, or killifish remained unchanged. RA did not induce any opsin switches or change the visual pigment absorbance of photoreceptors. Neither ligand altered cone photoreceptor densities. We conclude that RA has no effect on opsin expression or visual pigment properties in the differentiated retina of these fishes. In contrast, TH affected both single-cone opsin expression and visual pigment absorbance in the rainbow trout alevin but only visual pigment absorbance in the smolt and in zebrafish. The latter results could be explained by a combination of opsin switches and chromophore shifts from vitamin A1 to vitamin A2.

Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones

“…Expression of RH2-1 and, especially, RH2-2 (l max : 476 nm) predominates throughout the central retina, whereas RH2-3 (l max : 488 nm) and RH2-4 are confined to small patches in the ventral and peripheral retina [34]. In the centro-temporal retina, which mediated the majority of prey attacks (table 1), the predominant opsin transcript is RH2-2 [34], corresponding to the M cone measured by microspectrophotometry in this and other studies [19,29]. Together, these results illustrate the overall dominant expression of the RH2-2 opsin isoform in the zebrafish retina.…”

“…There was, however, no regular pattern to the presence of UV cones in lor fish. By comparison, control fish had the typical row mosaic arrangement with alternating UV and S cones throughout the retina (figure 2e,f) [19,29]. Cone density measurements from three retinas revealed mean UV : S : M : L cone fractions of 0.08 : 0.9 : 2 : 2 for the lor retina and 1 : 1 : 2 : 2 for the control retina.…”

“…The zebrafish is a typical, small zooplanktivorous fish that retains UV cones as part of a tetrachromatic visual system based, additionally, on S, M and L cones [19,23,[29][30][31]. Mutation screens carried out in the Fadool laboratory identified the lor (lots of rods) mutant characterized by greatly diminished numbers of UV cones, their place in the photoreceptor mosaic occupied, instead, by rods [32].…”

“…As the juvenile grows, a physiological transformation involving thyroid hormone changes the UV cones into blue (S) cones by switching opsin production from SWS1 to SWS2. Prior to this natural transformation, the juvenile can be treated exogenously with thyroid hormone to induce, prematurely, the opsin switch [18,19]. Using thyroid hormone treatment and the appropriate controls, the UV cone was shown to improve the foraging performance of small zooplanktivorous rainbow trout [15].…”

“…Fishes that are small and zooplanktivorous, like the zebrafish, giant Danio, killifishes and threespine stickleback, retain UV cones throughout life [19][20][21][22]. Fishes that grow from small juveniles into much larger adults, like the salmonid fishes and flatfishes, progressively lose their UV cones [17,23].…”