Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field

Abstract

Vision frequently mediates critical behaviours, and photoreceptors must respond to the light available to accomplish these tasks. Most photoreceptors are thought to contain a single visual pigment, an opsin protein bound to a chromophore, which together determine spectral sensitivity. Mechanisms of spectral tuning include altering the opsin, changing the chromophore and incorporating pre-receptor filtering. A few exceptions to the use of a single visual pigment have been documented in which a single mature photoreceptor coexpresses opsins that form spectrally distinct visual pigments, and in these exceptions the functional significance of coexpression is unclear. Here we document for the first time photoreceptors coexpressing spectrally distinct opsin genes in a manner that tunes sensitivity to the light environment. Photoreceptors of the cichlid fish, Metriaclima zebra, mix different pairs of opsins in retinal regions that view distinct backgrounds. The mixing of visual pigments increases absorbance of the corresponding background, potentially aiding the detection of dark objects. Thus, opsin coexpression may be a novel mechanism of spectral tuning that could be useful for detecting prey, predators and mates. However, our calculations show that coexpression of some opsins can hinder colour discrimination, creating a trade-off between visual functions.

A second visual rhodopsin gene,rh1-2, is expressed in zebrafish photoreceptors and found in other ray-finned fishes

“…Previous studies have hypothesized that cone opsin co-expression in humans could provide a developmental advantage (Xiao and Hendrickson, 2000). Alternatively, cone opsin co-expression in the cichlid fish Metriaclima zebra is thought to contribute to spectral tuning, although the λ max differences in these opsins is 35-48 nm (Dalton et al, 2014), far exceeding the 5 nm difference between rhodopsin and Rh1-2. However, rhodopsin also serves an important structural role in rod photoreceptors, where it is packed into the outer segments and forms an array of dimers (Fotiadis et al, 2003).…”

From crypsis to mimicry: changes in colour and the configuration of the visual system during ontogenetic habitat transitions in a coral reef fish

“…This suggests that the large absorbance spectra in the adult LWS twin cones may derive from the co-expression of RH2Aβ with LWS (RH2Aβ with RH2Aα in the case of the MWS twin cone). The proposed dottyback scenario of coexpression involving two orthologous green genes (RH2A) with a difference in λ max of ∼10 nm and a longer shifted red gene (LWS), has recently been reported for the freshwater cichlid Metriaclima zebra (Dalton et al, 2014). In M. zebra, co-expressing multiple visual pigments within a single photoreceptor significantly enhances luminance discrimination, but the drawback seems to be a decrease in chromatic colour discrimination (Dalton et al, 2014).…”

“…The proposed dottyback scenario of coexpression involving two orthologous green genes (RH2A) with a difference in λ max of ∼10 nm and a longer shifted red gene (LWS), has recently been reported for the freshwater cichlid Metriaclima zebra (Dalton et al, 2014). In M. zebra, co-expressing multiple visual pigments within a single photoreceptor significantly enhances luminance discrimination, but the drawback seems to be a decrease in chromatic colour discrimination (Dalton et al, 2014). In support of these findings, we found a very similar pattern when modelling dottyback and coral trout visual tasks using the broad absorbance spectra instead of A 1 -based visual templates.…”

Eye development in the four-eyed fish Anableps anableps : cranial and retinal adaptations to simultaneous aerial and aquatic vision

“…The gene repertoire and expression of opsins can vary according to the environment [37], and opsin expression can change in individuals in response to alterations in photic environment [24,26,27]. For instance, in the African cichlid fish Metriaclima zebra, lws and rh2aa opsins are coexpressed in double cones of the ventral but not the dorsal retina [25]. However, exposing developing embryos to light stimulus from below resulted in coexpression of lws and rh2aa throughout the adult M. zebra retina [38].…”

“…Opsin expression in the retina can change in response to different light stimuli [24][25][26][27]. Previous studies showed that rh2-1 and lws expression in Anableps occur exclusively in the ventral or dorsal regions of the retina, respectively [23].…”