Life-stage dependent changes and thyroid hormone-mediated plasticity in the retinal ultraviolet photoreceptor cell complement of Atlantic salmon (Salmo salar)

BROWMAN, H.I.*; HOLMQVIST, B.; FORSELL, J.; EBBESSON, L.; ALM, P.: Life-stage dependent changes and thyroid hormone-mediated plasticity in the retinal ultraviolet photoreceptor cell complement of Atlantic salmon (Salmo salar).

Several salmonid fishes possess a discrete retinal photoreceptor sensitive to ultraviolet-A (UV) radiation when they are freshwater-resident juveniles (parr). The UV photoreceptor disappears from most of the retina as part of this group of fishes’ natural physiological adaptation (smoltification) to a life in the sea (as juveniles, or smolts) and then re-appears in reproductive-stage adults. The molecular identity of the salmonid UV-sensitive photopigment (the UV opsin), and its detailed temporal and spatial expression in the retina, are unknown. This study presents the first characterization of the ontogeny of UV opsin expressing photoreceptors, and of the changes in their distribution during juvenile-to-adult life stages, in the Atlantic salmon. We identified a partial gene sequence encoding the UV opsin in Atlantic salmon that is approximately 75% and 60% identical to UV sensitive opsins in other teleosts and mammals, respectively. RNA probes were generated for specific visualization of UV opsin mRNA transcripts. The temporal and spatial expression of UV opsin mRNA was then used to survey the natural and thyroid hormone influenced developmental trajectory of UV photoreceptors in the Atlantic salmon retina. Embryos exhibit morphologically “immature” UV photoreceptors restricted to a small portion of the central retina. In alevins, “immature” UV photoreceptors are present in most of the central retina. In parr, mature UV photoreceptors are distributed throughout the retina, except for the central region, and large populations of “immature” UV opsin expressing cells are present in the growth zones. In smolts, UV opsin mRNA is expressed in a residual population of mature photoreceptors in the ventral retina and in “immature” cells at the growth zones. Atlantic salmon parr exposed to thyroid hormone (by immersion) exhibit a precocial loss of photoreceptors expressing UV opsin mRNA. Smolts exposed to thyroid hormone exhibit a precocial recruitment of photoreceptors expressing UV opsin mRNA. The natural and thyroid hormone influenced changes in gene expression of UV opsin are consistent with morphological and microspectrophotometric data from other salmonid fishes (mainly rainbow trout). Immature (putatively precocious) photoreceptors are shown to express UV opsin mRNA in all life stages, initially in the central retina of the embryo and alevin, and later in the growth zones of juveniles and adults.

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