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Avian ultraviolet/violet cones identified as probable magnetoreceptors.

Niessner C, Denzau S, Gross JC, Peichl L, Bischof HJ, Fleissner G, Wiltschko W, Wiltschko R - PLoS ONE (2011)

Bottom Line: In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina.We provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model.Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.

View Article: PubMed Central - PubMed

Affiliation: Fachbereich Biowissenschaften der J.W. Goethe-Universit├Ąt Frankfurt, Frankfurt am Main, Germany.

ABSTRACT

Background: The Radical-Pair-Model postulates that the reception of magnetic compass directions in birds is based on spin-chemical reactions in specialized photopigments in the eye, with cryptochromes discussed as candidate molecules. But so far, the exact subcellular characterization of these molecules in the retina remained unknown.

Methodology/principal findings: We here describe the localization of cryptochrome 1a (Cry1a) in the retina of European robins, Erithacus rubecula, and domestic chickens, Gallus gallus, two species that have been shown to use the magnetic field for compass orientation. In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina. Electron microscopy shows Cry1a in ordered bands along the membrane discs of the outer segment, and cell fractionation reveals Cry1a in the membrane fraction, suggesting the possibility that Cry1a is anchored along membranes.

Conclusions/significance: We provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model. Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.

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Immuno-labeling for Cry1a and UV cone opsin, and their co-localization in the retina.(A), Vertical section of chicken retina; (B), whole mount of chicken retina; (C), vertical section of European robin retina; (D), whole mount of robin retina. The different layers in the vertical sections are indicated: 1 outer and inner segments of the photoreceptors with the oil droplets in between; 2 outer nuclear layer; 3 outer plexiform layer; 4 inner nuclear layer; 5 inner plexiform layer; 6 ganglion cell layer. Left column: (A1 to D1): Cry1a immunofluorescence (rendered in green) is inside the outer segment of a very slender photoreceptor type. Middle column: (A2 to D2): UV/V cone opsin immunofluorescence (rendered in blue) in the same section. Right column: (A3 to D3): Merge of the images, indicating that Cry1a and the UV/V cone opsin co-localize. In robins, the the population density of the Cry1a/UV appers to be higher than in chickens.
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pone-0020091-g001: Immuno-labeling for Cry1a and UV cone opsin, and their co-localization in the retina.(A), Vertical section of chicken retina; (B), whole mount of chicken retina; (C), vertical section of European robin retina; (D), whole mount of robin retina. The different layers in the vertical sections are indicated: 1 outer and inner segments of the photoreceptors with the oil droplets in between; 2 outer nuclear layer; 3 outer plexiform layer; 4 inner nuclear layer; 5 inner plexiform layer; 6 ganglion cell layer. Left column: (A1 to D1): Cry1a immunofluorescence (rendered in green) is inside the outer segment of a very slender photoreceptor type. Middle column: (A2 to D2): UV/V cone opsin immunofluorescence (rendered in blue) in the same section. Right column: (A3 to D3): Merge of the images, indicating that Cry1a and the UV/V cone opsin co-localize. In robins, the the population density of the Cry1a/UV appers to be higher than in chickens.

Mentions: The results in both species were the same: Cry1a was found in one specific population of very slender photoreceptors of the single cone type (Fig. 1). Double labeling with the Cry1a antiserum and the UV/V opsin antiserum showed that this receptor is the UV/V (SWS1) cone, which has a higher population density in robins than in chickens (Fig. 1). Birds have four color cone types [19]; the long wavelength-sensitive (LWS) cones did not contain Cry1a labels and the same appears to hold for the other two cone types (SWS, MWS). Cry1a was found only in UV/V cones, and all these cones contained Cry1a in chickens as well as in robins. Avian cone outer and inner segments are clearly separated by an oil droplet; in these cones, Cry1a label was present in the outer, but not in the inner segment (Fig. 1A,C). Since Cry1a occupied a smaller region within the outer segment than the opsin, it may appear as if in the section shown in Fig.1C some UV/V cones do not contain Cry1a. However, focusing through the section and the flat view in the whole mounts clearly showed that Cry1a label was present in every UV/V cone. The topographic distribution of the Cry1a-containing cone was assessed in flattened whole retinae, showing that these cones were present across the entire retina in both species, with no obvious density peaks (Fig. 1B,D).


Avian ultraviolet/violet cones identified as probable magnetoreceptors.

Niessner C, Denzau S, Gross JC, Peichl L, Bischof HJ, Fleissner G, Wiltschko W, Wiltschko R - PLoS ONE (2011)

Immuno-labeling for Cry1a and UV cone opsin, and their co-localization in the retina.(A), Vertical section of chicken retina; (B), whole mount of chicken retina; (C), vertical section of European robin retina; (D), whole mount of robin retina. The different layers in the vertical sections are indicated: 1 outer and inner segments of the photoreceptors with the oil droplets in between; 2 outer nuclear layer; 3 outer plexiform layer; 4 inner nuclear layer; 5 inner plexiform layer; 6 ganglion cell layer. Left column: (A1 to D1): Cry1a immunofluorescence (rendered in green) is inside the outer segment of a very slender photoreceptor type. Middle column: (A2 to D2): UV/V cone opsin immunofluorescence (rendered in blue) in the same section. Right column: (A3 to D3): Merge of the images, indicating that Cry1a and the UV/V cone opsin co-localize. In robins, the the population density of the Cry1a/UV appers to be higher than in chickens.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3102070&req=5

pone-0020091-g001: Immuno-labeling for Cry1a and UV cone opsin, and their co-localization in the retina.(A), Vertical section of chicken retina; (B), whole mount of chicken retina; (C), vertical section of European robin retina; (D), whole mount of robin retina. The different layers in the vertical sections are indicated: 1 outer and inner segments of the photoreceptors with the oil droplets in between; 2 outer nuclear layer; 3 outer plexiform layer; 4 inner nuclear layer; 5 inner plexiform layer; 6 ganglion cell layer. Left column: (A1 to D1): Cry1a immunofluorescence (rendered in green) is inside the outer segment of a very slender photoreceptor type. Middle column: (A2 to D2): UV/V cone opsin immunofluorescence (rendered in blue) in the same section. Right column: (A3 to D3): Merge of the images, indicating that Cry1a and the UV/V cone opsin co-localize. In robins, the the population density of the Cry1a/UV appers to be higher than in chickens.
Mentions: The results in both species were the same: Cry1a was found in one specific population of very slender photoreceptors of the single cone type (Fig. 1). Double labeling with the Cry1a antiserum and the UV/V opsin antiserum showed that this receptor is the UV/V (SWS1) cone, which has a higher population density in robins than in chickens (Fig. 1). Birds have four color cone types [19]; the long wavelength-sensitive (LWS) cones did not contain Cry1a labels and the same appears to hold for the other two cone types (SWS, MWS). Cry1a was found only in UV/V cones, and all these cones contained Cry1a in chickens as well as in robins. Avian cone outer and inner segments are clearly separated by an oil droplet; in these cones, Cry1a label was present in the outer, but not in the inner segment (Fig. 1A,C). Since Cry1a occupied a smaller region within the outer segment than the opsin, it may appear as if in the section shown in Fig.1C some UV/V cones do not contain Cry1a. However, focusing through the section and the flat view in the whole mounts clearly showed that Cry1a label was present in every UV/V cone. The topographic distribution of the Cry1a-containing cone was assessed in flattened whole retinae, showing that these cones were present across the entire retina in both species, with no obvious density peaks (Fig. 1B,D).

Bottom Line: In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina.We provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model.Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.

View Article: PubMed Central - PubMed

Affiliation: Fachbereich Biowissenschaften der J.W. Goethe-Universit├Ąt Frankfurt, Frankfurt am Main, Germany.

ABSTRACT

Background: The Radical-Pair-Model postulates that the reception of magnetic compass directions in birds is based on spin-chemical reactions in specialized photopigments in the eye, with cryptochromes discussed as candidate molecules. But so far, the exact subcellular characterization of these molecules in the retina remained unknown.

Methodology/principal findings: We here describe the localization of cryptochrome 1a (Cry1a) in the retina of European robins, Erithacus rubecula, and domestic chickens, Gallus gallus, two species that have been shown to use the magnetic field for compass orientation. In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina. Electron microscopy shows Cry1a in ordered bands along the membrane discs of the outer segment, and cell fractionation reveals Cry1a in the membrane fraction, suggesting the possibility that Cry1a is anchored along membranes.

Conclusions/significance: We provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model. Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.

Show MeSH
Related in: MedlinePlus