Photoreceptor layer of salmonid fishes: Transformation and loss of single cones in juvenile fish

Abstract

The retinas of many vertebrates have cone photoreceptors that express multiple visual pigments. In many of these animals, including humans, the original cones to appear in the retina (which express UV or blue opsin) may change opsin types, giving rise to new spectral phenotypes. Here we used microspectrophotometry and in situ hybridization with cDNA probes to study the distribution of UV and blue cones in the retinas of four species of Pacific salmon (coho, chum, chinook, and pink salmon), in the Atlantic salmon, and in the rainbow/steelhead trout. In Pacific salmon and in the trout, all single cones express a UV opsin at hatching (lambda(max) of the visual pigment approximately 365 nm), and these cones later transform into blue cones by opsin changeover (lambda(max) of the blue visual pigment approximately 434 nm). Cones undergoing UV opsin downregulation exhibit either of two spectral absorbance profiles. The first is characterized by UV and blue absorbance peaks, with blue absorbance dominating the base of the outer segment. The second shows UV absorbance diminishing from the outer segment tip to the base, with no sign of blue absorbance. The first absorbance profile indicates a transformation from UV to blue phenotype by opsin changeover, while the second type suggests that the cone is undergoing apoptosis. These two events (transformation and loss of corner cones) are closely associated in time and progress from ventral to dorsal retina. Each double cone member contains green (lambda(max) approximately 510 nm) or red (lambda(max) approximately 565 nm) visual pigment (double cones are green/red pairs), and, like the rods (lambda(max) approximately 508 nm), do not exhibit opsin changeover. Unlike Pacific salmonids, the Atlantic salmon shows a mixture of UV and blue cones and a partial loss of corner cones at hatching. This study establishes the UV-to-blue cone transformation as a general feature of retinal growth in Pacific salmonids (genus Oncorhynchus).

Thyroid hormone accelerates opsin expression during early photoreceptor differentiation and induces opsin switching in differentiated TRα‐expressing cones of the salmonid retina

“…In rat, gerbil, fruit fly, and salmonid fishes, opsins can arise through switches in expression within terminally differentiated photoreceptors (Szél et al, 1994;Cheng et al, 2006Sprecher and Desplan, 2008). Salmonid fishes in particular may be very valuable for studying thyroid hormone-dependent opsin switches and related plasticity in cone spectral phenotype (Novales Flamarique, 2005;.…”

“…Centre cones are located in the middle of the square, at the hypothetical intersection of double cone partitions. Corner cones, when present, occupy the corners of the square, facing the partitions of neighboring double cones (Novales Flamarique et al, 1998;Cheng et al, 2006). Our laboratory has shown that terminally differentiated centre and corner cones of the salmonid retina undergo an irreversible switch from UV (SWS1) to blue (SWS2) opsin expression Novales Flamarique, 2004, 2007;Cheng et al, 2006.…”

“…Corner cones, when present, occupy the corners of the square, facing the partitions of neighboring double cones (Novales Flamarique et al, 1998;Cheng et al, 2006). Our laboratory has shown that terminally differentiated centre and corner cones of the salmonid retina undergo an irreversible switch from UV (SWS1) to blue (SWS2) opsin expression Novales Flamarique, 2004, 2007;Cheng et al, 2006. The opsin switch, detected by changes in opsin mRNA expression and visual pigment (opsin þ chromophore) absorbance (Cheng and Novales Flamarique, 2004;Cheng et al, 2006), commences shortly after hatching and coincides with reported global increases in thyroid hormone and TRa expression.…”

Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons

“…Although examples of such switches in sensory specificity of terminally differentiated, functional, sensory receptors are extremely rare, this strategy might be more common than currently anticipated. In the Pacific pink salmon and rainbow trout, newly hatched fish express an ultraviolet opsin that changes to a blue opsin as the fish ages [16][17][18] . As in flies, this switch might reflect an adaptation of vision to the changing lifestyle.…”

“…Interestingly, reports from several other species, including amphibians, rodents and humans, show co-expression of opsins 17,18,[20][21][22] .In humans, for instance, it has been proposed that cones first express S opsin and later switch to L/M opsin. However, this likely reflects a developmental process rather than a functional adaptation 22 .…”