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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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Population in equilibrium of the different visual pigment states participating in the arrestin cycle in honeybee microvilli with R0 = 1,000 visual pigment molecules and A0 =1,000 arrestin molecules, as a function of the light intensity. The ratio of the photoconversion rate constants, kM/kR = 0.43, results in a metarhodopsin fraction in equilibrium fMe = 0.7 in the absence of pigment turnover. Lefta, c, e ignoring pigment turnover; active metarhodopsin increases linearly with intensity, saturating at the very high level of ca 10 molecules per microvillus (c,e). Rightb, d, f a microvillus under the same conditions, but now including pigment turnover, assuming time constants of 3 min for degradation of Ri and Mi and 10 min for regeneration of rhodopsin, Ra. fMe now depends strongly on intensity with fMe = 0, or, ~100% visual pigment in the Ra state at very low light intensities, and only approaching the nominal photoequilibrium of fMe = 0.7 at high intensities. d With increasing intensity the number of visual pigment molecules is distinctly reduced (bleached) and the total number of number of active molecules, Ma, is much less than would be the case without pigment turnover (compare e,f)
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Fig7: Population in equilibrium of the different visual pigment states participating in the arrestin cycle in honeybee microvilli with R0 = 1,000 visual pigment molecules and A0 =1,000 arrestin molecules, as a function of the light intensity. The ratio of the photoconversion rate constants, kM/kR = 0.43, results in a metarhodopsin fraction in equilibrium fMe = 0.7 in the absence of pigment turnover. Lefta, c, e ignoring pigment turnover; active metarhodopsin increases linearly with intensity, saturating at the very high level of ca 10 molecules per microvillus (c,e). Rightb, d, f a microvillus under the same conditions, but now including pigment turnover, assuming time constants of 3 min for degradation of Ri and Mi and 10 min for regeneration of rhodopsin, Ra. fMe now depends strongly on intensity with fMe = 0, or, ~100% visual pigment in the Ra state at very low light intensities, and only approaching the nominal photoequilibrium of fMe = 0.7 at high intensities. d With increasing intensity the number of visual pigment molecules is distinctly reduced (bleached) and the total number of number of active molecules, Ma, is much less than would be the case without pigment turnover (compare e,f)

Mentions: a Spectral distribution of the photon flux from natural sources: the sky, the sun and grass. b Absorbance spectra of the pigments in the eye of the blowfly C.vicina. The red screening pigment is located distally in the eye in the screening pigment cells (from Schwemer 1979), and the yellow pupillary pigment is located in the soma of the photoreceptor cells (from Stavenga 2004, Fig. 7). c Absorbance spectra of eye pigments of a few other insects: the screening pigment spectrum of the honey bee Apismellifera (from Strother and Casella 1972, Fig. 8), the pupillary pigment of the wasp Vespa germanica (from Stavenga and Kuiper 1977, Fig. 10), and the screening pigment of a Heliconius butterfly (from Langer and Struwe 1972, Fig. 6)


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)

Population in equilibrium of the different visual pigment states participating in the arrestin cycle in honeybee microvilli with R0 = 1,000 visual pigment molecules and A0 =1,000 arrestin molecules, as a function of the light intensity. The ratio of the photoconversion rate constants, kM/kR = 0.43, results in a metarhodopsin fraction in equilibrium fMe = 0.7 in the absence of pigment turnover. Lefta, c, e ignoring pigment turnover; active metarhodopsin increases linearly with intensity, saturating at the very high level of ca 10 molecules per microvillus (c,e). Rightb, d, f a microvillus under the same conditions, but now including pigment turnover, assuming time constants of 3 min for degradation of Ri and Mi and 10 min for regeneration of rhodopsin, Ra. fMe now depends strongly on intensity with fMe = 0, or, ~100% visual pigment in the Ra state at very low light intensities, and only approaching the nominal photoequilibrium of fMe = 0.7 at high intensities. d With increasing intensity the number of visual pigment molecules is distinctly reduced (bleached) and the total number of number of active molecules, Ma, is much less than would be the case without pigment turnover (compare e,f)
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Related In: Results  -  Collection

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Fig7: Population in equilibrium of the different visual pigment states participating in the arrestin cycle in honeybee microvilli with R0 = 1,000 visual pigment molecules and A0 =1,000 arrestin molecules, as a function of the light intensity. The ratio of the photoconversion rate constants, kM/kR = 0.43, results in a metarhodopsin fraction in equilibrium fMe = 0.7 in the absence of pigment turnover. Lefta, c, e ignoring pigment turnover; active metarhodopsin increases linearly with intensity, saturating at the very high level of ca 10 molecules per microvillus (c,e). Rightb, d, f a microvillus under the same conditions, but now including pigment turnover, assuming time constants of 3 min for degradation of Ri and Mi and 10 min for regeneration of rhodopsin, Ra. fMe now depends strongly on intensity with fMe = 0, or, ~100% visual pigment in the Ra state at very low light intensities, and only approaching the nominal photoequilibrium of fMe = 0.7 at high intensities. d With increasing intensity the number of visual pigment molecules is distinctly reduced (bleached) and the total number of number of active molecules, Ma, is much less than would be the case without pigment turnover (compare e,f)
Mentions: a Spectral distribution of the photon flux from natural sources: the sky, the sun and grass. b Absorbance spectra of the pigments in the eye of the blowfly C.vicina. The red screening pigment is located distally in the eye in the screening pigment cells (from Schwemer 1979), and the yellow pupillary pigment is located in the soma of the photoreceptor cells (from Stavenga 2004, Fig. 7). c Absorbance spectra of eye pigments of a few other insects: the screening pigment spectrum of the honey bee Apismellifera (from Strother and Casella 1972, Fig. 8), the pupillary pigment of the wasp Vespa germanica (from Stavenga and Kuiper 1977, Fig. 10), and the screening pigment of a Heliconius butterfly (from Langer and Struwe 1972, Fig. 6)

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