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

Stavenga DG, Hardie RC - J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. (2010)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiophysics, University of Groningen, Groningen, The Netherlands. D.G.Stavenga@rug.nl

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.

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Photoequilibria resulting after prolonged illumination of the visual pigments of Fig. 2 with the three natural light sources of Fig. 1a, filtered by the various photostable pigments: for the blowfly, the red screening pigment and the yellow pupillary pigment of Fig. 1b, and for the honeybee the screening pigment of Fig. 1c. a The resulting metarhodopsin fractions for the blowfly are given by the lower six curves and by the upper three curves for the honeybee. The pigment density indicates the value at the wavelength of maximal absorbance (a density of 1, 2, 3… means attenuation by a factor of 10, 100, 1,000…). b Photoequilibria resulting after prolonged illumination with sky and grass light of the blowfly and honeybee visual pigments in a 300 μm long rhabdom(ere), when filtered distally by the blowfly pupillary pigment and honeybee screening pigment, respectively, with peak densities 0 (no filter), 1 and 2. c Dependence of the photoconversion rate on the distance from the rhabdomere tip, normalized to the value at the tip, for the blowfly visual pigment illuminated with sky and grass light, for the same three densities of filtering pigment as in b
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Fig3: Photoequilibria resulting after prolonged illumination of the visual pigments of Fig. 2 with the three natural light sources of Fig. 1a, filtered by the various photostable pigments: for the blowfly, the red screening pigment and the yellow pupillary pigment of Fig. 1b, and for the honeybee the screening pigment of Fig. 1c. a The resulting metarhodopsin fractions for the blowfly are given by the lower six curves and by the upper three curves for the honeybee. The pigment density indicates the value at the wavelength of maximal absorbance (a density of 1, 2, 3… means attenuation by a factor of 10, 100, 1,000…). b Photoequilibria resulting after prolonged illumination with sky and grass light of the blowfly and honeybee visual pigments in a 300 μm long rhabdom(ere), when filtered distally by the blowfly pupillary pigment and honeybee screening pigment, respectively, with peak densities 0 (no filter), 1 and 2. c Dependence of the photoconversion rate on the distance from the rhabdomere tip, normalized to the value at the tip, for the blowfly visual pigment illuminated with sky and grass light, for the same three densities of filtering pigment as in b

Mentions: When the insect visual pigments of Fig. 2 are irradiated for a sufficiently prolonged period, a photoequilibrium will be established depending on the spectral properties and quantum efficiencies of the two photointerconvertible states, rhodopsin and metarhodopsin, and the spectral composition of the light source. For the blowfly R1–6 visual pigment of Fig. 2a, the metarhodopsin fractions resulting with unfiltered light from the sky, sun and grass (Fig. 1a), calculated with Eq. 2 and the rate constants of photoconversion following from Eq. 1, are about 0.4, 0.35, and 0.2, respectively (Fig. 3a, pigment density 0). For the green rhodopsin of Fig. 2b, which is taken as an exemplar for the long-wavelength absorbing visual pigments of invertebrates, the metarhodopsin in photoequilibrium with unfiltered light is about 0.6.Fig. 3


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

Stavenga DG, Hardie RC - J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. (2010)

Photoequilibria resulting after prolonged illumination of the visual pigments of Fig. 2 with the three natural light sources of Fig. 1a, filtered by the various photostable pigments: for the blowfly, the red screening pigment and the yellow pupillary pigment of Fig. 1b, and for the honeybee the screening pigment of Fig. 1c. a The resulting metarhodopsin fractions for the blowfly are given by the lower six curves and by the upper three curves for the honeybee. The pigment density indicates the value at the wavelength of maximal absorbance (a density of 1, 2, 3… means attenuation by a factor of 10, 100, 1,000…). b Photoequilibria resulting after prolonged illumination with sky and grass light of the blowfly and honeybee visual pigments in a 300 μm long rhabdom(ere), when filtered distally by the blowfly pupillary pigment and honeybee screening pigment, respectively, with peak densities 0 (no filter), 1 and 2. c Dependence of the photoconversion rate on the distance from the rhabdomere tip, normalized to the value at the tip, for the blowfly visual pigment illuminated with sky and grass light, for the same three densities of filtering pigment as in b
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Related In: Results  -  Collection

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Fig3: Photoequilibria resulting after prolonged illumination of the visual pigments of Fig. 2 with the three natural light sources of Fig. 1a, filtered by the various photostable pigments: for the blowfly, the red screening pigment and the yellow pupillary pigment of Fig. 1b, and for the honeybee the screening pigment of Fig. 1c. a The resulting metarhodopsin fractions for the blowfly are given by the lower six curves and by the upper three curves for the honeybee. The pigment density indicates the value at the wavelength of maximal absorbance (a density of 1, 2, 3… means attenuation by a factor of 10, 100, 1,000…). b Photoequilibria resulting after prolonged illumination with sky and grass light of the blowfly and honeybee visual pigments in a 300 μm long rhabdom(ere), when filtered distally by the blowfly pupillary pigment and honeybee screening pigment, respectively, with peak densities 0 (no filter), 1 and 2. c Dependence of the photoconversion rate on the distance from the rhabdomere tip, normalized to the value at the tip, for the blowfly visual pigment illuminated with sky and grass light, for the same three densities of filtering pigment as in b
Mentions: When the insect visual pigments of Fig. 2 are irradiated for a sufficiently prolonged period, a photoequilibrium will be established depending on the spectral properties and quantum efficiencies of the two photointerconvertible states, rhodopsin and metarhodopsin, and the spectral composition of the light source. For the blowfly R1–6 visual pigment of Fig. 2a, the metarhodopsin fractions resulting with unfiltered light from the sky, sun and grass (Fig. 1a), calculated with Eq. 2 and the rate constants of photoconversion following from Eq. 1, are about 0.4, 0.35, and 0.2, respectively (Fig. 3a, pigment density 0). For the green rhodopsin of Fig. 2b, which is taken as an exemplar for the long-wavelength absorbing visual pigments of invertebrates, the metarhodopsin in photoequilibrium with unfiltered light is about 0.6.Fig. 3

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiophysics, University of Groningen, Groningen, The Netherlands. D.G.Stavenga@rug.nl

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.

Show MeSH
Related in: MedlinePlus