Many animals use the Earth’s geomagnetic field for orientation and navigation. Yet, the molecular and cellular underpinnings of the magnetic sense remain largely unknown. A biophysical model proposed that magnetoreception can be achieved through quantum effects of magnetically-sensitive radical pairs formed by the photoexcitation of cryptochrome (CRY) proteins. Studies in Drosophila are the only ones to date to have provided compelling evidence for the ultraviolet (UV)-A/blue light-sensitive type 1 CRY (CRY1) involvement in animal magnetoreception, and surprisingly extended this discovery to the light-insensitive mammalian-like type 2 CRYs (CRY2s) of both monarchs and humans. Here, we show that monarchs respond to a reversal of the inclination of the Earth’s magnetic field in an UV-A/blue light and CRY1, but not CRY2, dependent manner. We further demonstrate that both antennae and eyes, which express CRY1, are magnetosensory organs. Our work argues that only light-sensitive CRYs function in animal light-dependent inclination-based magnetic sensing.

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Cryptochromes (CRYs) are blue and UV light photoreceptors, known to play key roles in circadian rhythms and in the light-dependent magnetosensitivity of insects. Two novel cryptochrome genes were cloned from the brown planthopper, and were given the designations of Nlcry1 and Nlcry2, with the accession numbers KM108578 and KM108579 in GenBank. The complementary DNA sequences of Nlcry1 and Nlcry2 are 1935 bp and 2463 bp in length, and they contain an open reading frame of 1629 bp and 1872 bp, encoding amino acids of 542 and 623, with a predicted molecular weight of 62.53 kDa and 70.60 kDa, respectively. Well-conserved motifs such as DNA-photolyase and FAD-binding-7 domains were observed in Nlcry1 and Nlcry2. Phylogenetic analysis demonstrated the proteins of Nlcry1 and Nlcry2 to be clustered into the insect's cryptochrome 1 and cryptochrome 2, respectively. Quantitative polymerase chain reaction showed that the daily oscillations of messenger RNA (mRNA) expression in the head of the brown planthopper were mild for Nlcry1, and modest for Nlcry2. Throughout all developmental stages, Nlcry1 and Nlcry2 exhibited extreme fluctuations and distinctive expression profiles. Cryptochrome mRNA expression peaked immediately after adult emergence and then decreased subsequently. The tissue expression profiles of newly emerged brown planthopper adults showed higher expression levels of CRYs in the head than in the thorax or abdomen, as well as significantly higher levels of CRYs in the heads of the macropterous strain than in the heads of the brachypterous strain. Taken together, the results of our study suggest that the two cryptochrome genes characterized in the brown planthopper might be associated with developmental physiology and migration.

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