Cryptochrome mediates light-dependent magnetosensitivity in Drosophila

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Abstract

Although many animals use the Earth’s magnetic field for orientation and navigation1,2, the precise biophysical mechanisms underlying magnetic sensing have been elusive. One theoretical model proposes that geomagnetic fields are perceived by chemical reactions involving specialized photoreceptors3. However, the specific photoreceptor involved in such magnetoreception has not been demonstrated conclusively in any animal. Here we show that the ultraviolet-A/blue-light photoreceptor cryptochrome (Cry) is necessary for light-dependent magnetosensitive responses in Drosophila melanogaster. In a binary-choice behavioural assay for magnetosensitivity, wild-type flies show significant naive and trained responses to a magnetic field under full-spectrum light (300–700 nm) but do not respond to the field when wavelengths in the Cry-sensitive, ultraviolet-A/blue-light part of the spectrum (<420 nm) are blocked. Notably, Cry-deficient cry0 and cryb flies do not show either naive or trained responses to a magnetic field under full-spectrum light. Moreover, Cry-dependent magnetosensitivity does not require a functioning circadian clock. Our work provides, to our knowledge, the first genetic evidence for a Cry-based magnetosensitive system in any animal.

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Figure 1: Behavioural apparatus for magnetosensitivity and behavioural responses in different Drosophila strains.
Figure 2: Short-wavelength light is required for magnetosensitivity in Canton-S flies.
Figure 3: Drosophila Cry mediates magnetosensitivity.
Figure 4: Constant light disrupts circadian function but not Cry-mediated magnetosensitivity in Canton-S flies.

References

  1. 1

    Lohmann, K. J., Lohmann, C. M. F. & Putman, N. F. Magnetic maps in animals: nature’s GPS. J. Exp. Biol. 210, 3697–3705 (2007)

  2. 2

    Wiltschko, W. & Wiltschko, R. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 675–693 (2005)

  3. 3

    Ritz, T., Adem, S. & Schulten, K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718 (2000)

  4. 4

    Luschi, P. et al. Marine turtles use geomagnetic cues during open-sea homing. Curr. Biol. 17, 126–133 (2007)

  5. 5

    Johnsen, S. & Lohmann, K. J. The physics and neurobiology of magnetoreception. Nature Rev. Neurosci. 6, 703–712 (2005)

  6. 6

    Kirschvink, J. L. & Gould, J. L. Biogenic magnetite as a basis for magnetic-field detection in animals. Biosystems 13, 181–201 (1981)

  7. 7

    Walker, M. M. A model for encoding of magnetic field intensity by magnetite-based magnetoreceptor cells. J. Theor. Biol. 250, 85–91 (2008)

  8. 8

    Kirschvink, J. L., Walker, M. M. & Diebel, C. E. Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 11, 462–467 (2001)

  9. 9

    Leask, M. J. M. Physicochemical mechanism for magnetic-field detection by migratory birds and homing pigeons. Nature 267, 144–145 (1977)

  10. 10

    Schulten, K., Swenberg, C. E. & Weller, A. Biomagnetic sensory mechanism based on magnetic-field modulated coherent electron-spin motion. Z. Phy. Chem. (Frankfurt) 111, 1–5 (1978)

  11. 11

    Cashmore, A. R. Cryptochromes: Enabling plants and animals to determine circadian time. Cell 114, 537–543 (2003)

  12. 12

    Partch, C. L. & Sancar, A. Photochemistry and photobiology of cryptochrome blue-light photopigments: The search for a photocycle. Photochem. Photobiol. 81, 1291–1304 (2005)

  13. 13

    Zhu, H. et al. The two CRYs of the butterfly. Curr. Biol. 15, R953–R954 (2005)

  14. 14

    Yuan, Q., Metterville, D., Briscoe, A. D. & Reppert, S. M. Insect cryptochromes: Gene duplication and loss define diverse ways to construct insect circadian clocks. Mol. Biol. Evol. 24, 948–955 (2007)

  15. 15

    Öztürk, N., Song, S. H., Selby, C. P. & Sancar, A. Animal type 1 cryptochromes—analysis of the redox state of the flavin cofactor by site-directed mutagenesis. J. Biol. Chem. 283, 3256–3263 (2008)

  16. 16

    Phillips, J. B. & Borland, S. C. Behavioral evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 359, 142–144 (1992)

  17. 17

    Ritz, T., Dommer, D. H. & Phillips, J. B. Shedding light on vertebrate magnetoreception. Neuron 34, 503–506 (2002)

  18. 18

    Wiltschko, R. & Wiltschko, W. Magnetoreception. Bioessays 28, 157–168 (2006)

  19. 19

    VanVickle-Chavez, S. J. & Van Gelder, R. N. Action spectrum of Drosophila cryptochrome. J. Biol. Chem. 282, 10561–10566 (2007)

  20. 20

    Helfrich-Forster, C. et al. The extraretinal eyelet of Drosophila: Development, ultrastructure, and putative circadian function. J. Neurosci. 22, 9255–9266 (2002)

  21. 21

    Dolezelova, E., Dolezel, D. & Hall, J. C. Rhythm defects caused by newly engineered null mutations in Drosophila’s cryptochrome gene. Genetics 177, 329–345 (2007)

  22. 22

    Emery, P. et al. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669–679 (1998)

  23. 23

    Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila . Cell 95, 681–692 (1998)

  24. 24

    Kirschvink, J. L. Uniform magnetic-fields and double-wrapped coil systems—improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13, 401–411 (1992)

  25. 25

    Stanewsky, R. Genetic analysis of the circadian system in Drosophila melanogaster and mammals. J. Neurobiol. 54, 111–147 (2003)

  26. 26

    Wehner, R. & Labhart, T. Perception of geomagnetic field in fly Drosophila melanogaster . Experientia 26, 967–968 (1970)

  27. 27

    Phillips, J. B. & Sayeed, O. Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster . J. Comp. Physiol. A Sens. Neural Behav. Physiol. 172, 303–308 (1993)

  28. 28

    Maeda, K. et al. Chemical compass model of avian magnetoreception. Nature 453, 387–390 (2008)

  29. 29

    Tully, T. & Quinn, W. G. Classical-conditioning and retention in normal and mutant Drosophila melanogaster . J. Comp. Physiol. A Sens. Neural Behav. Physiol. 157, 263–277 (1985)

  30. 30

    Rush, B. L., Murad, A., Emery, P. & Giebultowicz, J. M. Ectopic CRYPTOCHROME renders TIM light sensitive in the Drosophila ovary. J. Biol. Rhythms 21, 272–278 (2006)

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Acknowledgements

We thank H. Zhu for the protein work in Fig. 4b, c; L. Foley for assistance; J. C. Hall for the cry0 flies; P. Emery for the Per and Cry antibodies; and P. Emery, P. Perrat, B. Leung, S. DasGupta, M. Krashes and H. Zhu for discussions. This work was supported by grants from the NIH.

Author Contributions S.M.R. and R.J.G. conceived the idea of using Drosophila to study magnetosensitivity; S.W. and R.J.G. conceived the idea of using appetitive conditioning to study magnetoresponses; R.J.G. designed the experimental apparatus; R.J.G., S.W., A.C. and S.M.R. designed the experiments and analysed the data; R.J.G. performed the experiments with help from A.C.; R.J.G., S.M.R., S.W. and A.C wrote the paper.

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Correspondence to Steven M. Reppert.

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