Metarhodopsin control by arrestin, light-filtering screening pigments, and visual pigment turnover in invertebrate microvillar photoreceptors

Abstract

The visual pigments of most invertebrate photoreceptors have two thermostable photo-interconvertible states, the ground state rhodopsin and photo-activated metarhodopsin, which triggers the phototransduction cascade until it binds arrestin. The ratio of the two states in photoequilibrium is determined by their absorbance spectra and the effective spectral distribution of illumination. Calculations indicate that metarhodopsin levels in fly photoreceptors are maintained below ~35% in normal diurnal environments, due to the combination of a blue-green rhodopsin, an orange-absorbing metarhodopsin and red transparent screening pigments. Slow metarhodopsin degradation and rhodopsin regeneration processes further subserve visual pigment maintenance. In most insect eyes, where the majority of photoreceptors have green-absorbing rhodopsins and blue-absorbing metarhodopsins, natural illuminants are predicted to create metarhodopsin levels greater than 60% at high intensities. However, fast metarhodopsin decay and rhodopsin regeneration also play an important role in controlling metarhodopsin in green receptors, resulting in a high rhodopsin content at low light intensities and a reduced overall visual pigment content in bright light. A simple model for the visual pigment–arrestin cycle is used to illustrate the dependence of the visual pigment population states on light intensity, arrestin levels and pigment turnover.

Molecular evolution and expression of the CRAL_TRIO protein family in insects

“…In Drosophila, all-trans 3-hydroxyretinal can be converted into 11-cis 3-hydroxyretinal by light but it is also the case that 11-cis 3-hydroxyretinal can be made from dietary Vitamin A. The fly chromophore does not rapidly dissociate from the opsin after light excitation, whereas in butterflies it can (Bernard, 1983a(Bernard, , 1983bStavenga and Hardie, 2011). This suggests that in lepidopteran species, production of the chromophore may be even more dependent on enzymatic processes than in Drosophila.…”

Increasing the illumination slowly over several weeks protects against light damage in the eyes of the crustacean Mysis relicta

“…This could be accompanied by elevated MII content and/or a decline in overall visual-pigment content, both reported to occur in bright light (Stavenga and Hardie, 2011). Decreases in visual-pigment content and/or changes in R:MII balance might therefore directly contribute to increased resilience by decreasing the direct challenges from massive phototransduction.…”

“…The latter mechanism is generally thought to dominate regeneration in bistable arthropod pigments, establishing illumination-dependent R:MII equilibria (e.g. Stavenga andHardie, 2011). Feldman et al (2010) argued that this might work in S p , whereas L p animals in their very dark habitat can only rely on 'dark' regeneration.…”

Evolution of Phototransduction Genes in Lepidoptera

“…Notably, Lepidoptera are thought to rely more on enzymatic regeneration of 11-cis-retinal than is the case in Diptera (Bernard 1983a and b;Stavenga and Hardie 2011). As the unclassified opsin has high expression in eyes and is phylogenetically similar to retinochrome, both proteins may have related enzymatic roles in vision if the unclassified opsin is expressed near the photoreceptor cells.…”

“…Concurrently, by a mechanism that is not well understood, there is an opening of Ca 2+ -permeable light-sensitive transient receptor potential (TRP) and transient receptor potential-like (TRPL) channels which causes depolarization of the cell (Montell & Rubin 1989;Hardie & Minke 1992;Niemeyer et al 1996;Shieh & Zhu 1996;Montell 2005). Finally, phototransduction is terminated when the activated rhodopsin (metarhodopsin) binds arrestin (Dolph et al 1993;Stavenga & Hardie 2011).…”