Visual pigment composition in zebrafish: Evidence for a rhodopsin–porphyropsin interchange system

Abstract

Numerous reports have concluded that zebrafish (Danio rerio) possesses A1-based visual pigments in their rod and cone photoreceptors. In the present study, we investigated the possibility that zebrafish have a paired visual pigment system. We measured the spectral absorption characteristics of photoreceptors from zebrafish maintained in different temperature regimes and those treated with exogenous thyroid hormone using CCD-based microspectrophotometry. Rods from fish housed at 15 degrees C and 28 degrees C were not significantly different, having lambda max values of 503 +/- 5 nm (n = 106) and 504 +/- 6 nm (n = 88), respectively. Thyroid hormone treatment (held at 28 degrees C), however, significantly shifted the lambda max of rods from 503 +/- 5 nm (n = 194) to 527 +/- 8 nm (n = 212). Cone photoreceptors in fish housed at 28 degrees C (without thyroid hormone treatment) had lambda max values of 361 +/- 3 nm (n = 2) for ultraviolet-, 411 +/- 5 nm (n = 18) for short-, 482 +/- 6 nm (n = 9) for medium-, and 565 +/- 10 nm (n = 14) for long-wavelength sensitive cones. Thyroid hormone treatment of fish held at 28 degrees C significantly shifted the lambda max of long-wavelength sensitive cones to 613 +/- 11 nm (n = 20), substantially beyond that of the lambda max of the longest possible A1-based visual pigment (approximately 580 nm). Thyroid hormone treatment produced smaller shifts of lambda max in other cone types and increased the half-band width. All shifts in photoreceptor lambda max values resulting from thyroid hormone treatment matched predictions for an A1- to A2-based visual pigment system. We therefore conclude that zebrafish possess a rhodopsin-porphyropsin interchange system that functions to spectrally tune rod and cone photoreceptors. We believe that these observations should be carefully considered during analysis of zebrafish spectral sensitivity.

Cyp27c1 Red-Shifts the Spectral Sensitivity of Photoreceptors by Converting Vitamin A1 into A2

“…The flash sensitivity of individual red cones was determined from the amplitudes of their electrical responses to a series of dim flashes of 560, 600, 660, and 700 nm light, and fitted with a model that incorporates contributions from both vitamin A 1 - and A 2 -based pigments [8]. No significant difference was observed between the sensitivities of vehicle-treated cyp27c1 Δ1/Δ2 and wild-type red cones at any of the wavelengths tested, and both wild-type and mutant red cones had maximal sensitivity (λ max ) at 561 nm, in close agreement with a previous estimate of λ max = 565 nm, determined by MSP (Figure 4D,E) [18]. In addition, knockout of cyp27c1 did not affect the dark current or the kinetics of the flash responses of the red cones, indicating that phototransduction remained intact (Figure 4E).…”

“…Zebrafish photoreceptors predominantly contain vitamin A 1 -based visual pigments under normal laboratory conditions, but treatment with thyroid hormone (TH) induces a conversion to vitamin A 2 -based pigments [18]. To corroborate this result, we treated zebrafish with TH and then analyzed the retinoid content of retinas and retinal pigment epithelium (RPE) by high-performance liquid chromatography (HPLC).…”

“…To test this hypothesis, we used single-cell suction electrode recording to measure the sensitivity of individual red cones from cyp27c1 Δ1/Δ2 mutants and wild-type siblings, treated with either TH or vehicle control. We measured red cones because they undergo the largest red-shift upon switching to 11- cis 3,4-didehydroretinal [18]. The flash sensitivity of individual red cones was determined from the amplitudes of their electrical responses to a series of dim flashes of 560, 600, 660, and 700 nm light, and fitted with a model that incorporates contributions from both vitamin A 1 - and A 2 -based pigments [8].…”

Visual Behavior in Zebrafish

“…The peak sensitivities have been measured with slightly variable values for both rods (501-503 nm) and cones (UV cone, 360-361 nm; S cone, 407-417 nm; M cone 473-480 nm; L cone, 556-564 nm). [5][6][7][8] Hence zebrafish vision is tetrachromatic, while human trichromatic vision lacks sensitivity to ultraviolet light.…”

Rapid Recovery of Visual Function Associated with Blue Cone Ablation in Zebrafish

“…Zebrafish have excellent colour discrimination ability [20] driven by four cone photoreceptor types: blue-sensitive, green-sensitive, red-sensitive, and ultraviolet (UV)-sensitive cones [21]. These outputs are compared, fostering tetrachromatic vision [20].…”