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Curr Biol. 2018 Jan 22;28(2):211-223.e4. doi: 10.1016/j.cub.2017.12.003. Epub 2018 Jan 4.

Double-Cone Localization and Seasonal Expression Pattern Suggest a Role in Magnetoreception for European Robin Cryptochrome 4.

Author information

1
Institut für Biologie und Umweltwissenschaften, Carl-von-Ossietzky-Universität Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26129 Oldenburg, Germany.
2
Department of Physics, Chemistry and Pharmacy, University of Southern Denmark, Campusvej 55, 5230 Odense, Denmark.
3
Helmholtz Zentrum München, German Research Center for Environmental Health, Institute for Diabetes and Obesity, Monoclonal Antibody Core Facility, Ingolstädter Landstrasse 1, 85764 Neuherberg, Germany.
4
Department of Neuroscience, Carl-von-Ossietzky-Universität Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26129 Oldenburg, Germany; Research Centre for Neurosensory Sciences, Carl-von-Ossietzky-Universität Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26129 Oldenburg, Germany.
5
Institut für Biologie und Umweltwissenschaften, Carl-von-Ossietzky-Universität Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26129 Oldenburg, Germany; Research Centre for Neurosensory Sciences, Carl-von-Ossietzky-Universität Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26129 Oldenburg, Germany. Electronic address: henrik.mouritsen@uni-oldenburg.de.

Abstract

Birds seem to use a light-dependent, radical-pair-based magnetic compass. In vertebrates, cryptochromes are the only class of proteins that form radical pairs upon photo-excitation. Therefore, they are currently the only candidate proteins for light-dependent magnetoreception. Cryptochrome 4 (Cry4) is particularly interesting because it has only been found in vertebrates that use a magnetic compass. However, its structure and localization within the retina has remained unknown. Here, we sequenced night-migratory European robin (Erithacus rubecula) Cry4 from the retina and predicted the currently unresolved structure of the erCry4 protein, which suggests that erCry4 should bind Flavin. We also found that Cry1a, Cry1b, and Cry2 mRNA display robust circadian oscillation patterns, whereas Cry4 shows only a weak circadian oscillation. When we compared the relative mRNA expression levels of the cryptochromes during the spring and autumn migratory seasons relative to the non-migratory seasons in European robins and domestic chickens (Gallus gallus), the Cry4 mRNA expression level in European robin retinae, but not in chicken retinae, is significantly higher during the migratory season compared to the non-migratory seasons. Cry4 protein is specifically expressed in the outer segments of the double cones and long-wavelength single cones in European robins and chickens. A localization of Cry4 in double cones seems to be ideal for light-dependent magnetoreception. Considering all of the data presented here, especially including its localization within the European robin retina, its likely binding of Flavin, and its increased expression during the migratory season in the migratory bird but not in chicken, Cry4 could be the magnetoreceptive protein.

KEYWORDS:

bird migration; eye; magnetic sense; magnetic sensing; magneto-perception; navigation; orientation; photoreceptor; photoreceptor cells; vision

PMID:
29307554
DOI:
10.1016/j.cub.2017.12.003

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