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. 2008 Aug 21;454(7207):1014-8.
doi: 10.1038/nature07183. Epub 2008 Jul 20.

Cryptochrome mediates light-dependent magnetosensitivity in Drosophila

Robert J Gegear  1 , Amy Casselman, Scott Waddell, Steven M Reppert
Affiliations

Cryptochrome mediates light-dependent magnetosensitivity in Drosophila

Robert J Gegear et al. Nature. .

Abstract

Although many animals use the Earth's magnetic field for orientation and navigation, the precise biophysical mechanisms underlying magnetic sensing have been elusive. One theoretical model proposes that geomagnetic fields are perceived by chemical reactions involving specialized photoreceptors. 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 ( approximately 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 cry(0) and cry(b) 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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Figures

Figure 1
Figure 1. Behavioural apparatus for magnetosensitivity and behavioural responses in different Drosophila strains
a, Behavioral apparatus for magnetosensitivity. Upper (Train), frontal view of the choice chamber apparatus positioned for training. The chamber apparatus consisted of a training tube, an elevator to transfer flies, and a duel-choice point (T-port). For training, the apparatus, with training tube only, was placed upright in an illuminated black box containing a two-coil system. A population of flies (dots) was loaded into the training tube with or without sucrose reinforcement and a magnetic field. Lower (Test), frontal view of the choice chamber apparatus positioned for testing. For testing, the apparatus, with tubes attached to the T-port (T-maze), was rotated to the horizontal, and flies were transferred from elevator section to the T-port. Wavelength-dependence was examined using long-wavelength pass filters. b, Drosophila strains vary in their behavioural response to a magnetic field under full-spectrum light (Fig. 2a). Bars show preference index of the naïve (white) or trained (black) groups. Numbers are groups tested. Values are mean ± s.e.m. *, P<0.05; **, P<0.01; ****, P<0.0001.
Figure 2
Figure 2. Short-wavelength light is required for magnetosensitivity in Canton-S flies
a, Irradiance curves for different light conditions. Light measurements were taken inside the training/test tube. Dashed lines, cut-off points of the blocking filters. b, Wavelength-dependence of magnetic response. Bars show preference index of the naïve (white) or trained (black) groups. Full-spectrum data are from Figure 1b. Numbers are groups tested. *, P<0.05; ****, P<0.0001. c, Irradiance curves depicting full-spectrum light (black line), light >420 nm (red line), and full-spectrum light with reduced total irradiance (full-spectrum, low intensity; blue line). d, Canton-S flies still elicited significant responses to the magnetic field under full-spectrum, low intensity light. ****, P<0.0001. e, Irradiance values from 300 – 420 nm. Data are expanded scale from full-spectrum pattern in panel a. The irradiance values in UV-A/blue in our studies (300 – 420 nm) are in line with those reported for Drosophila CRY function, using other biological responses,; that is, range of 1011 to 1012 photons/s/cm2/nm. Values from b, d, e are mean ± s.e.m.
Figure 3
Figure 3. Drosophila CRY mediates magnetosensitivity
a, Magnetosensitivity in w1118 flies depends on UV-A/blue light. Bars show PI for naïve responses under full-spectrum light, and light > 500 nm and > 420 nm. Numbers are groups tested. ****, P<0.0001. b, Naïve response to a magnetic field is impaired in CRY-deficient cry02 flies, but not in cry02/+ flies. Bars show preference index values for naïve responses. **, P<0.01; ***, P<0.001. c, Naïve and trained responses to a magnetic field are impaired in CRY-deficient cry01 flies. Bars are preference index values for naïve (white) and trained (black) groups. *, P<0.05. d, Naïve and trained responses to a magnetic field are impaired in homozygous cryb and transheterozygous cryb/cry01 flies. Bars show preference index values for naïve (white) or trained (black) groups. C-S, Canton-S. *, P<0.05; ****, P<0.0001. Values from a–d are mean s.e.m.
Figure 4
Figure 4. Constant light disrupts circadian function but not CRY-mediated magnetosensitivity in Canton-S flies
a, Mean activity records in LD (upper) or LL (lower) in double-plotted format (n = 62 for each group). The lighting conditions were identical to those used for housing flies tested for responses to magnet; light irradiance, 1.5×1015 photons/s/cm2/nm. For LD, 94% expressed circadian rhythms when released in constant darkness (period, 24.6 ± 0.03 hours). All the LL flies were arrhythmic. b, Temporal profiles of PERIOD in heads. Protein abundance was rhythmic in LD (p< 0.01, one-way ANOVA), but not in LL. Head extracts were analyzed by western blot and normalized against α-tubulin. Values are mean ± s.e.m. from three sets of heads. c, CRY abundance is decreased in LL. Values are mean ± s.e.m. from three sets of heads collected over 24-hours in LD or LL. Right, western blot probed for CRY showing presence (arrow) in LD or LL in Canton-S (C-S) heads, and absence in cry01 heads. d, Flies in LL elicit behavioural responses to the magnetic field. Values are mean ± s.e.m. ****, p < 0.0001.
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