Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism.
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). 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.
Gegear
Robert J
RJ
Department of Neurobiology, University of Massachusetts Medical School, 364 Plantation Street, Worcester, Massachusetts 01605, USA. robert.gegear@umassmed.edu
Foley
Lauren E
LE
Casselman
Amy
A
Reppert
Steven M
SM
D025041:Animal Migration / Q000502:physiology / Q000528:radiation effects; D000818:Animals; D030801:Animals, Genetically Modified; D002080:Butterflies / Q000235:genetics / Q000378:metabolism* / Q000528:radiation effects; D056931:Cryptochromes / Q000172:deficiency / Q000235:genetics / Q000378:metabolism*; D029721:Drosophila Proteins / Q000172:deficiency / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000235:genetics / Q000378:metabolism* / Q000528:radiation effects; D005136:Eye Proteins / Q000235:genetics / Q000378:metabolism; D008280:Magnetics; D009949:Orientation / Q000502:physiology / Q000528:radiation effects; D055668:Photochemical Processes / Q000528:radiation effects; D017956:Photoreceptor Cells, Invertebrate / Q000378:metabolism / Q000528:radiation effects; D019076:Transgenes / Q000235:genetics
D056931:Cryptochromes; D029721:Drosophila Proteins; D005136:Eye Proteins; C119828:cry protein, Drosophila; C096445:tim protein, Drosophila