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Quantum Compass of Migratory Birds

signaling cascade plant CRY has been suggested to act as a magnetoreceptor (Xu et al., 2012). Artifcial

reversal of the GMF has confrmed that Arabidopsis can respond not only to magnetic feld intensity

but also to magnetic feld direction and polarity (Bertea et al., 2015). Moreover, the GMF was found to

impact photomorphogenic-promoting gene expression in etiolated seedlings of Arabidopsis, indicating

the existence of a light-independent magnetoreception mechanism (Agliassa et al., 2018b). With regard

to exposure of plants to magnetic felds higher than the GMF, the magnetic felds ranging ~1–30 mT have

been reported to produce changes in quantum yield of favin semiquinone radicals in AtCRY1 (Maeda

et al., 2012).

In the context of animal magnetoreception, one can well imagine that relaxation and recombina­

tion rates for the CRY radical pair might have been optimized for function by evolution, e.g., through

interaction with binding partners, slight variations of protein structure as well as solution accessibility

(protonation/deprotonation) of the radicals, especially the terminal tryptophan (Hiscock et al., 2016b).

Te second condition of strong axiality of the hyperfne couplings is, at least to some degree, fulflled by

the favin radical (Lee et al., 2013). However, a hyperfne-coupling-free second radical is harder to imag­

ine (Kerpal et al., 2019). Te frequently evoked hypothesis of the involvement of a superoxide radical O

•

2

−

fails as demonstrated in the literature (Hogben et al., 2009), owing to the large spin-orbit coupling in O

•

2

−

leading to extremely fast electron spin relaxation (Kerpal et al., 2019). As a result, all spin coherence is

lost on a nanosecond timescale and with it any magnetic feld sensitivity (Kerpal et al., 2019).

As mentioned above, the magnetically sensitive species is commonly assumed to be [FAD^•− TrpH^•+],

formed by sequential light-induced intraprotein electron transfers from a chain of tryptophan residues

to the FAD chromophore (Henbest et al., 2008; Weber et al., 2010; Maeda et al., 2012). However, some

evidence points to superoxide, O

•

2

−, as an alternative partner for the favin radical. Te absence of hyper­

fne interactions in O

•

2

− could lead to a more sensitive magnetic compass, but only if the electron spin

relaxation of the O

•

2

− radical is much slower than normally expected for a small mobile radical with an

orbitally degenerate electronic ground state. Player and Hore (2019) used spin dynamics simulations to

model the sensitivity of a favin-superoxide radical pair to the direction of a 50 μT magnetic feld. By

varying parameters that characterize the local environment and molecular dynamics of the radicals,

Player and Hore (2019) identifed the highly restrictive conditions under which a O

•

2

−-containing radical

pair could form the basis of a geomagnetic compass sensor. Player and Hore (2019) concluded that the

involvement of superoxide in compass magnetoreception must remain highly speculative until further

experimental evidence is forthcoming.

One further hypothesis regards the involvement of the ascorbyl radical characterized by few and

small isotropic hyperfne couplings (Evans et al., 2016). In the solution, the favin/ascorbyl pair demon­

strated sensitivity to weak felds much exceeding previously reported efects in other favin-containing

radical pairs, including CRYs (Evans et al., 2016). However, recent molecular dynamics simulations sug­

gest that the brief and infrequent encounters of the ascorbyl radical with CRY make this also an unlikely

candidate in the search for an Earth strength feld sensor (Nielsen et al., 2017).

4.5 Discussion and Conclusions

A great deal of experimental work on the structure and function of migratory bird CRY (as described

above) has been carried out so far. Simply speaking, a photo-pigment CRY could function as a magnetic

receptor molecule with a chromophore FAD in the retina (Rodgers and Hore, 2009; Hore and Mouritsen,

2016). However, the exact details are still unknown, because using the above-mentioned RPM-based

magnetoreception, there remain unsolved mechanisms/pathways to determine the direction indicating

“compass information,” and more specifcally, the location indicating “map information” of the latitude

and longitude coordinates. Here, the plausible basic reaction mechanisms of biological systems and con­

ventional artifcial systems are reviewed and discussed. Light-dependent magnetic feld efects in vitro

have been reported for CRY1 from the plant Arabidopsis thaliana (AtCRY1), and the closely related DNA

photolyase from Escherichia coli (EcPL) (Goez et al., 2009; Maeda et al., 2012). Te magnetic responses of