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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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Spectral properties of insect visual pigments. a Absorbance spectra of the two thermostable states, rhodopsin (R490) and metarhodopsin (M575), of the main visual pigment of the blowfly C. vicina; the fine-structured absorbance in the ultraviolet is due to 3-hydroxy-retinol, which sensitizes the visual pigment molecule, both in the rhodopsin and in the metarhodopsin state. b Absorbance spectra of the rhodopsin (R532) and metarhodopsin (M492) of a typical green-sensitive visual pigment. c, d The metarhodopsin fraction in photoequilibrium as a function of monochromatic illumination, calculated with the spectra of a and b, using a relative quantum efficiency φ = 0.94 (blowfly) and φ = 0.71 (green visual pigment)
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Fig2: Spectral properties of insect visual pigments. a Absorbance spectra of the two thermostable states, rhodopsin (R490) and metarhodopsin (M575), of the main visual pigment of the blowfly C. vicina; the fine-structured absorbance in the ultraviolet is due to 3-hydroxy-retinol, which sensitizes the visual pigment molecule, both in the rhodopsin and in the metarhodopsin state. b Absorbance spectra of the rhodopsin (R532) and metarhodopsin (M492) of a typical green-sensitive visual pigment. c, d The metarhodopsin fraction in photoequilibrium as a function of monochromatic illumination, calculated with the spectra of a and b, using a relative quantum efficiency φ = 0.94 (blowfly) and φ = 0.71 (green visual pigment)

Mentions: The conversion follows an exponential time course with time constant τc = 1/(kR+kM). In the case of monochromatic illumination fMe(λ) = 1/[1+φαM(λ)/αR(λ)], with φ = γM/γR the relative quantum efficiency (see e.g. Stavenga and Schwemer 1984; Stavenga et al. 2000). For the main visual pigment of the blowfly C. vicina a value of φ = 0.94 was reported (Schwemer 1979), but for most other visual pigments φ appears to be lower, around 0.7 (see Stavenga and Schwemer 1984). Figure 2 gives as examples the blue-green absorbing rhodopsin R490 (peak wavelength 490 nm) of the R1–6 photoreceptors of the blowfly C. vicina with its strongly bathochromic shifted, orange absorbing metarhodopsin M575 (Fig. 2a; from Stavenga 2010) and the green-absorbing rhodopsin R532 from the eye of the comma butterfly Polygonia c-album with its hypsochromic shifted, blue-green absorbing metarhodopsin M492 (Fig. 2b; from Vanhoutte and Stavenga 2005). The latter visual pigment can be taken as characteristic for the dominant, green-absorbing visual pigment class populating the majority of the photoreceptors in most insects (Hamdorf 1979; Briscoe and Chittka 2001; Briscoe et al. 2003; Wakakuwa et al. 2007). For simplicity and convenience, we assume hereafter that this pigment is also representative for the green visual pigment of honeybees, although strictly speaking this will be slightly incorrect, because the spectral sensitivity of the honeybee green receptor peaks at 544 nm (Peitsch et al. 1992). The absorbance of the metarhodopsin in the ultraviolet is assumed to be lower than that of the rhodopsin (Fig. 2b), but the precise spectral characteristics of insect visual pigments in the UV are uncertain (see Stavenga 2010). The dependence of the metarhodopsin fraction in photoequilibrium on monochromatic illumination is completely opposite for the two visual pigments of Fig. 2a and b. Whereas, red light causes a photoequilibrium with negligible metarhodopsin for the blowfly visual pigment (Fig. 2c), negligible rhodopsin results in the case of the green-absorbing rhodopsin (Fig. 2d; see also Hamdorf 1979).Fig. 2


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)

Spectral properties of insect visual pigments. a Absorbance spectra of the two thermostable states, rhodopsin (R490) and metarhodopsin (M575), of the main visual pigment of the blowfly C. vicina; the fine-structured absorbance in the ultraviolet is due to 3-hydroxy-retinol, which sensitizes the visual pigment molecule, both in the rhodopsin and in the metarhodopsin state. b Absorbance spectra of the rhodopsin (R532) and metarhodopsin (M492) of a typical green-sensitive visual pigment. c, d The metarhodopsin fraction in photoequilibrium as a function of monochromatic illumination, calculated with the spectra of a and b, using a relative quantum efficiency φ = 0.94 (blowfly) and φ = 0.71 (green visual pigment)
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Fig2: Spectral properties of insect visual pigments. a Absorbance spectra of the two thermostable states, rhodopsin (R490) and metarhodopsin (M575), of the main visual pigment of the blowfly C. vicina; the fine-structured absorbance in the ultraviolet is due to 3-hydroxy-retinol, which sensitizes the visual pigment molecule, both in the rhodopsin and in the metarhodopsin state. b Absorbance spectra of the rhodopsin (R532) and metarhodopsin (M492) of a typical green-sensitive visual pigment. c, d The metarhodopsin fraction in photoequilibrium as a function of monochromatic illumination, calculated with the spectra of a and b, using a relative quantum efficiency φ = 0.94 (blowfly) and φ = 0.71 (green visual pigment)
Mentions: The conversion follows an exponential time course with time constant τc = 1/(kR+kM). In the case of monochromatic illumination fMe(λ) = 1/[1+φαM(λ)/αR(λ)], with φ = γM/γR the relative quantum efficiency (see e.g. Stavenga and Schwemer 1984; Stavenga et al. 2000). For the main visual pigment of the blowfly C. vicina a value of φ = 0.94 was reported (Schwemer 1979), but for most other visual pigments φ appears to be lower, around 0.7 (see Stavenga and Schwemer 1984). Figure 2 gives as examples the blue-green absorbing rhodopsin R490 (peak wavelength 490 nm) of the R1–6 photoreceptors of the blowfly C. vicina with its strongly bathochromic shifted, orange absorbing metarhodopsin M575 (Fig. 2a; from Stavenga 2010) and the green-absorbing rhodopsin R532 from the eye of the comma butterfly Polygonia c-album with its hypsochromic shifted, blue-green absorbing metarhodopsin M492 (Fig. 2b; from Vanhoutte and Stavenga 2005). The latter visual pigment can be taken as characteristic for the dominant, green-absorbing visual pigment class populating the majority of the photoreceptors in most insects (Hamdorf 1979; Briscoe and Chittka 2001; Briscoe et al. 2003; Wakakuwa et al. 2007). For simplicity and convenience, we assume hereafter that this pigment is also representative for the green visual pigment of honeybees, although strictly speaking this will be slightly incorrect, because the spectral sensitivity of the honeybee green receptor peaks at 544 nm (Peitsch et al. 1992). The absorbance of the metarhodopsin in the ultraviolet is assumed to be lower than that of the rhodopsin (Fig. 2b), but the precise spectral characteristics of insect visual pigments in the UV are uncertain (see Stavenga 2010). The dependence of the metarhodopsin fraction in photoequilibrium on monochromatic illumination is completely opposite for the two visual pigments of Fig. 2a and b. Whereas, red light causes a photoequilibrium with negligible metarhodopsin for the blowfly visual pigment (Fig. 2c), negligible rhodopsin results in the case of the green-absorbing rhodopsin (Fig. 2d; see also Hamdorf 1979).Fig. 2

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