Effects of exogenous thyroid hormones on visual pigment composition in coho salmon (<i>Oncorhynchus kisutch</i>)

Temple, Shelby E.; Ramsden, Samuel; Haimberger, Theodore J.; Veldhoen, Kathy; Veldhoen, Nik; Carter, Nicolette L.; Roth, Wolff‐Michael; Hawryshyn, Craig W.

doi:10.1242/jeb.009365

Cited by 25 publications

(35 citation statements)

References 92 publications

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“…Rod absorbance curves were compared (minimum variance fit) to the Munz and Beatty template (Munz and Beatty, 1965), which extends from λ max to a point at 20% of the maximum on the long wavelength arm. The Munz and Beatty template assumes that λ max values of coho rods vary from 503 to 527 nm, which is in close agreement with published models that predict the shift that occurs when A 1 is replaced by A 2 in the same opsin (Bridges, 1965;Dartnall and Lythgoe, 1965;Harosi, 1994;Parry and Bowmaker, 2000) (reviewed by Temple et al, 2008;Tsin et al, 1981;Whitmore and Bowmaker, 1989). However, many of the rods we measured had λ max values that exceeded 527 nm and therefore were not fitted by the Munz and Beatty template (Munz and Beatty, 1965).…”

Section: Microspectrophotometrysupporting

confidence: 86%

“…These photoreceptors express all five vertebrate opsin classes: RH1, UVS, SWS, RH2 and LWS, respectively (Dann et al, 2004), and we have recently shown (Temple et al, 2008) that coho express at least two subtypes of the RH2 opsin (RH2A and RH2B). Preliminary evidence suggests that the expression of these two RH2 opsin subtypes may vary throughout life history (Temple et al, 2008).…”

Section: Introductionmentioning

confidence: 89%

“…All of these mechanisms are present among Pacific salmonids (Oncorhynchus spp. ), which migrate from cold freshwater streams and lakes to the open ocean within days to months of hatching and then migrate back to their natal freshwater streams and lakes a few years later to spawn and die (Beatty, 1966;Bowmaker and Kunz, 1987;Browman and Hawryshyn, 1992;Allison et al, 2003;Hawryshyn et al, 2003;Cheng and Novales Flamarique, 2004;Temple et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…This extended period of freshwater residency necessitates a visual system that is well adapted to the spectral environment and visual tasks at hand. Furthermore, they have been the subject of debate concerning the timing of changes in visual pigment (VP) A 1 /A 2 chromophore ratio (reviewed by Temple et al, 2006), which, combined with a large body of work on other Pacific salmonids, has provided considerable background information about their visual system (Alexander et al, 1994;Alexander et al, 1998;Alexander et al, 2001;Beatty, 1966;Beatty, 1972;Novales Flamarique, 2005;Temple et al, 2006;Temple et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Ontogenetic changes in photoreceptor opsin gene expression in coho salmon(Oncorhynchus kisutch, Walbaum)

Temple

Veldhoen

Phelan

et al. 2008

Journal of Experimental Biology

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SUMMARYPacific salmonids start life in fresh water then migrate to the sea, after a metamorphic event called smoltification, later returning to their natal freshwater streams to spawn and die. To accommodate changes in visual environments throughout life history, salmon may adjust their spectral sensitivity. We investigated this possibility by examining ontogenetic and thyroid hormone (TH)-induced changes in visual pigments in coho salmon (Oncorhynchus kisutch, Walbaum). Using microspectrophotometry, we measured the spectral absorbance (quantified by λ max ) of rods, and middle and long wavelength-sensitive (MWS and LWS) cones in three age classes of coho, representing both freshwater and marine phases. The λ max of MWS and LWS cones differed among freshwater (alevin and parr) and ocean (smolt) phases. The λ max of rods, on the other hand, did not vary, which is evidence that vitamin A 1 /A 2 visual pigment chromophore ratios were similar among freshwater and ocean phases when sampled at the same time of year. Exogenous TH treatment long wavelength shifted the λ max of rods, consistent with an increase in A 2 . However, shifts in cones were greater than predicted for a change in chromophore ratio. Real-time quantitative RT-PCR demonstrated that at least two RH2 opsin subtypes were expressed in MWS cones, and these were differentially expressed among alevin, parr and THtreated alevin groups. Combined with changes in A 1 /A 2 ratio, differential expression of opsin subtypes allows coho to alter the spectral absorbance of their MWS and LWS cones by as much as 60 and 90 nm, respectively. To our knowledge, this is the largest spectral shift reported in a vertebrate photoreceptor.

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Section: Microspectrophotometrysupporting

confidence: 86%

Section: Introductionmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Ontogenetic changes in photoreceptor opsin gene expression in coho salmon(Oncorhynchus kisutch, Walbaum)

Temple

Veldhoen

Phelan

et al. 2008

Journal of Experimental Biology

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“…Salmonid fishes have a paired visual pigment system with mixtures of A 1 and A 2 chromophores in both rod and cone outer segments (Temple et al, 2008a;Temple et al, 2008b). To determine the correspondence between visual pigments and sensitivity peaks, only as a first order approximation, absorption templates of visual pigments (Govardovskii et al, 2000) were fitted to the sensitivity curves using a least-squares fit.…”

Section: Fitting Visual Pigment Templatesmentioning

confidence: 99%

Spectral and polarization sensitivity of juvenile Atlantic salmon (Salmo salar): phylogenetic considerations

Hawryshyn

Ramsden

Betke

et al. 2010

Journal of Experimental Biology

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1999) hypothesized, based on molecular evidence, that Salmo and Oncorhynchus were not sister taxa. Recent reconstruction of the phylogenetic relationships among the Salmonidae, based on more complete mitochondrial and nuclear DNA data sets (Crespi and Fulton, 2004;Ishiguro et al., 2003), however, has revealed that Salvelinus and Oncorhynchus form sister taxa, with Salmo as the outgroup. This new relationship changes past interpretations of trait evolution within the Salmoninae. Therefore, the conclusion that the traits for spectral sensitivity and polarization sensitivity are ancestral to the clade containing Salmo, Oncorhynchus and Salvelinus (Parkyn Accepted 2 June 2010 SUMMARY We were interested in comparing the characteristics of polarization sensitivity in Atlantic salmon to those in Pacific salmon. Here we show that the common ancestor to the clade containing Salmo salar, Oncorhynchus mykiss, O. nerka, O. clarkii and Salvelinus fontinalis has the trait of ultraviolet polarization sensitivity. We examined spectral and polarization sensitivity of juvenile Atlantic salmon (Salmo salar) using both optic nerve compound action potential (CAP) and electroretinogram (ERG) recordings. Our experiments employed photic manipulation to adjust the sensitivity of the four cone mechanisms of Atlantic salmon. A spectrally broad background was used to ensure a contribution of all cone mechanisms to both spectral and polarization sensitivity. Chromatic adaptation was used to isolate the sensitivity of each of the four cone mechanisms for both spectral and polarization sensitivity. Under spectrally broad conditions, UV sensitive (UVS), mid wavelength sensitive (MWS) and long wavelength sensitive (LWS) cone mechanisms contributed to polarization sensitivity. CAP recordings produced the typical 'W' shaped polarization sensitivity curve reflecting two active polarization detectors with peaks at e-vector orientations of 0deg, 90deg and 180deg, and troughs at 30deg and 150deg. ERG recordings produced a four-peaked polarization sensitivity curve reflecting two active polarization detectors and negative feedback activity, with peaks at e-vectors 0deg, 45deg, 90deg, 135deg and 180deg, and troughs at 30deg, 60deg, 120deg and 150deg. Polarization-sensitivity measurements of isolated cone mechanisms revealed two orthogonal polarization detector mechanisms in Atlantic salmon, identical to that found in rainbow trout and other Pacific salmonid fishes. Moreover, under spectrally broad background conditions, CAP and ERG polarization sensitivity of Atlantic salmon did not differ significantly from that reported in Pacific salmonids.

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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

Suliman

Flamarique

2013

J of Comparative Neurology

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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.

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Effects of exogenous thyroid hormones on visual pigment composition in coho salmon (Oncorhynchus kisutch)

Cited by 25 publications

References 92 publications

Ontogenetic changes in photoreceptor opsin gene expression in coho salmon(Oncorhynchus kisutch, Walbaum)

Ontogenetic changes in photoreceptor opsin gene expression in coho salmon(Oncorhynchus kisutch, Walbaum)

Spectral and polarization sensitivity of juvenile Atlantic salmon (Salmo salar): phylogenetic considerations

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

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