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Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism

Abstract

Understanding the biophysical basis of animal magnetoreception has been one of the greatest challenges in sensory biology. Recently it was discovered that the light-dependent magnetic sense of Drosophila melanogaster is mediated by the ultraviolet (UV)-A/blue light photoreceptor cryptochrome (Cry)1. Here we show, using a transgenic approach, that the photoreceptive, Drosophila-like type 1 Cry and the transcriptionally repressive, vertebrate-like type 2 Cry of the monarch butterfly (Danaus plexippus) can both function in the magnetoreception system of Drosophila and require UV-A/blue light (wavelength below 420 nm) to do so. The lack of magnetic responses for both Cry types at wavelengths above 420 nm does not fit the widely held view that tryptophan triad-generated radical pairs mediate the ability of Cry to sense a magnetic field. We bolster this assessment by using a mutant form of Drosophila and monarch type 1 Cry and confirm that the tryptophan triad pathway is not crucial in magnetic transduction. Together, these results suggest that animal Crys mediate light-dependent magnetoreception through an unconventional photochemical mechanism. This work emphasizes the utility of Drosophila transgenesis for elucidating the precise mechanisms of Cry-mediated magnetosensitivity in insects and also in vertebrates such as migrating birds.

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Figure 1: Type 1 Crys rescue light-dependent magnetoreception in Cry-deficient flies.
Figure 2: Monarch type 2 Cry rescues light-dependent magnetosensivity in Cry-deficient flies.
Figure 3: Effects of terminal tryptophan mutations on type 1 and type 2 Cry-mediated magnetosensitivity.
Figure 4: The clock proteins Tim and Cyc are not required for Drosophila magnetoreception.

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Acknowledgements

We thank Q. Yuan for performing the assays in Fig. 3d and the cryptochrome alignments in Supplementary Fig. 1, and P. Emery, C. Merlin and D. R. Weaver for discussions. This work was supported by a grant from the National Institutes of Health.

Author Contributions All authors contributed to experimental design, execution, data analysis and writing the paper.

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Correspondence to Robert J. Gegear or Steven M. Reppert.

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Gegear, R., Foley, L., Casselman, A. et al. Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism. Nature 463, 804–807 (2010). https://doi.org/10.1038/nature08719

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