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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 fly microvilli as a function of the light intensity, neglecting visual pigment turnover. The microvilli are assumed to have R0 = 1,000 visual pigment molecules, of which in total 200 exist in one of the two possible metarhodopsin states, Ma and Mi (fMe = 0.2), and the other 800 are in the Ra and Ri states. Lefta, c, e the case of a fruitfly, Drosophila, microvillus with A0 = 370 arrestin molecules. Rightb, d, f the case of a blowfly, Calliphora, microvillus with A0 = 1,000 arrestin molecules. At logI = 0 the photoconversion time constant is 1 s. At low intensities the number of active metarhodopsin molecules, Ma, is linearly related to the light intensity. At high intensities that number saturates, depending on the number of available arrestin molecules. The maximum intensity experienced under natural conditions is unlikely to be greater than logI = 0 for skylight (see text)
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Fig6: Population in equilibrium of the different visual pigment states participating in the arrestin cycle in fly microvilli as a function of the light intensity, neglecting visual pigment turnover. The microvilli are assumed to have R0 = 1,000 visual pigment molecules, of which in total 200 exist in one of the two possible metarhodopsin states, Ma and Mi (fMe = 0.2), and the other 800 are in the Ra and Ri states. Lefta, c, e the case of a fruitfly, Drosophila, microvillus with A0 = 370 arrestin molecules. Rightb, d, f the case of a blowfly, Calliphora, microvillus with A0 = 1,000 arrestin molecules. At logI = 0 the photoconversion time constant is 1 s. At low intensities the number of active metarhodopsin molecules, Ma, is linearly related to the light intensity. At high intensities that number saturates, depending on the number of available arrestin molecules. The maximum intensity experienced under natural conditions is unlikely to be greater than logI = 0 for skylight (see text)

Mentions: Figure 6 presents two model fly microvilli with A0 = 370 (representative for the fruitfly; Fig. 6a, c, e) and A0 = 1,000 (Fig. 6b, d, f; assumed for the blowfly because of the inability to create a full PDA in this case—see “Discussion”), where the illumination creates a steady state with a total metarhodopsin fraction fMe = 0.2. Because of its slow time course, turnover of fly visual pigment was neglected in the calculations. The relative photon flux or log intensity, logI, was normalized so that at logI = 0 the sum of the photoconversion rate constants kR+kM = 1 s−1, that is, the time constant for creating a photoequilibrium is 1 s. For the fly visual pigment (Fig. 2a), the time constants for unfiltered light from the sky or grass are 1.2 and 9.1 s, respectively (see Methods), corresponding to logI = −0.08 and logI = −0.96. The time constants increase in proportion to the degree of filtering by the pupil mechanism. For instance, with a pupil mechanism that effectively suppresses the incident light by one log unit, the time constants increase tenfold to 12 and 91 s, respectively; the visual pigment distribution due to light from the sky and grass then has to be read at logI = −1.08 and logI = −1.96, respectively.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 fly microvilli as a function of the light intensity, neglecting visual pigment turnover. The microvilli are assumed to have R0 = 1,000 visual pigment molecules, of which in total 200 exist in one of the two possible metarhodopsin states, Ma and Mi (fMe = 0.2), and the other 800 are in the Ra and Ri states. Lefta, c, e the case of a fruitfly, Drosophila, microvillus with A0 = 370 arrestin molecules. Rightb, d, f the case of a blowfly, Calliphora, microvillus with A0 = 1,000 arrestin molecules. At logI = 0 the photoconversion time constant is 1 s. At low intensities the number of active metarhodopsin molecules, Ma, is linearly related to the light intensity. At high intensities that number saturates, depending on the number of available arrestin molecules. The maximum intensity experienced under natural conditions is unlikely to be greater than logI = 0 for skylight (see text)
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Related In: Results  -  Collection

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Fig6: Population in equilibrium of the different visual pigment states participating in the arrestin cycle in fly microvilli as a function of the light intensity, neglecting visual pigment turnover. The microvilli are assumed to have R0 = 1,000 visual pigment molecules, of which in total 200 exist in one of the two possible metarhodopsin states, Ma and Mi (fMe = 0.2), and the other 800 are in the Ra and Ri states. Lefta, c, e the case of a fruitfly, Drosophila, microvillus with A0 = 370 arrestin molecules. Rightb, d, f the case of a blowfly, Calliphora, microvillus with A0 = 1,000 arrestin molecules. At logI = 0 the photoconversion time constant is 1 s. At low intensities the number of active metarhodopsin molecules, Ma, is linearly related to the light intensity. At high intensities that number saturates, depending on the number of available arrestin molecules. The maximum intensity experienced under natural conditions is unlikely to be greater than logI = 0 for skylight (see text)
Mentions: Figure 6 presents two model fly microvilli with A0 = 370 (representative for the fruitfly; Fig. 6a, c, e) and A0 = 1,000 (Fig. 6b, d, f; assumed for the blowfly because of the inability to create a full PDA in this case—see “Discussion”), where the illumination creates a steady state with a total metarhodopsin fraction fMe = 0.2. Because of its slow time course, turnover of fly visual pigment was neglected in the calculations. The relative photon flux or log intensity, logI, was normalized so that at logI = 0 the sum of the photoconversion rate constants kR+kM = 1 s−1, that is, the time constant for creating a photoequilibrium is 1 s. For the fly visual pigment (Fig. 2a), the time constants for unfiltered light from the sky or grass are 1.2 and 9.1 s, respectively (see Methods), corresponding to logI = −0.08 and logI = −0.96. The time constants increase in proportion to the degree of filtering by the pupil mechanism. For instance, with a pupil mechanism that effectively suppresses the incident light by one log unit, the time constants increase tenfold to 12 and 91 s, respectively; the visual pigment distribution due to light from the sky and grass then has to be read at logI = −1.08 and logI = −1.96, respectively.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