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Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism

2010; Nature Portfolio; Volume: 463; Issue: 7282 Linguagem: Inglês

10.1038/nature08719

1476-4687

Robert J. Gegear, Lauren E. Foley, Amy Casselman, Steven M. Reppert,

Magnetic and Electromagnetic Effects

Just how animals are able to use the Earth's magnetic field for navigation is the subject of much current interest. It is known that the UV-A/blue light photoreceptor cryptochrome (Cry) mediates the light-dependent magnetic sense in Drosophila. Steven Reppert and colleagues now use genetic manipulation to show that two cryptochromes from the monarch butterfly, Drosophila-like Cry1 and vertebrate-like Cry2, can restore magnetic sensation in cry-deficient Drosophila. This suggests that both types of Cry have the capacity to sense magnetic fields in the migratory monarch butterfly via a mechanism that remains unclear — and that light sensitivity is involved in some way. Animals use the Earth's magnetic field for orientation but the biophysical basis of this is unclear. The light-dependent magnetic sense of Drosophila melanogaster was recently shown to be mediated by the cryptochrome (Cry) photoreceptor; here, using a transgenic approach, the type 1 and 2 Cry of the monarch butterfly are shown to both function in the magnetoreception system of Drosophila, and probably use 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)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.