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Originally published In Press as doi:10.1074/jbc.M609842200 on January 19, 2007

J. Biol. Chem., Vol. 282, Issue 13, 9383-9391, March 30, 2007
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Cryptochrome Blue Light Photoreceptors Are Activated through Interconversion of Flavin Redox States*Formula

Jean-Pierre Bouly{ddagger}, Erik Schleicher§, Maribel Dionisio-Sese1, Filip Vandenbussche{ddagger}||, Dominique Van Der Straeten**, Nadia Bakrim{ddagger}, Stefan Meier, Alfred Batschauer, Paul Galland, Robert Bittl§, and Margaret Ahmad{ddagger}**2

From the {ddagger}Université Paris VI, FRE-CNRS 2846, Casier 156, 4 Place Jussieu, 75005 Paris, France, §Freie Universität Berlin, Fachbereich Physik, Arnimallee 14, 14195 Berlin, Germany, FB Biologie-Pflanzenphysiologie, Philipps-Universität, Karl-von-Frisch-Strasse 8, 35032 Marburg, Germany, ||Unit Plant Hormone Signaling and Bio-imaging, Department of Molecular Genetics, Ghent University, Ledeganckstraat 35, B-9000 Ghent, Belgium, and **Pennsylvania State University, Media, Pennsylvania 19063

Cryptochromes are blue light-sensing photoreceptors found in plants, animals, and humans. They are known to play key roles in the regulation of the circadian clock and in development. However, despite striking structural similarities to photolyase DNA repair enzymes, cryptochromes do not repair double-stranded DNA, and their mechanism of action is unknown. Recently, a blue light-dependent intramolecular electron transfer to the excited state flavin was characterized and proposed as the primary mechanism of light activation. The resulting formation of a stable neutral flavin semiquinone intermediate enables the photoreceptor to absorb green/yellow light (500–630 nm) in addition to blue light in vitro. Here, we demonstrate that Arabidopsis cryptochrome activation by blue light can be inhibited by green light in vivo consistent with a change of the cofactor redox state. We further characterize light-dependent changes in the cryptochrome1 (cry1) protein in living cells, which match photoreduction of the purified cry1 in vitro. These experiments were performed using fluorescence absorption/emission and EPR on whole cells and thereby represent one of the few examples of the active state of a known photoreceptor being monitored in vivo. These results indicate that cry1 activation via blue light initiates formation of a flavosemiquinone signaling state that can be converted by green light to an inactive form. In summary, cryptochrome activation via flavin photoreduction is a reversible mechanism novel to blue light photoreceptors. This photocycle may have adaptive significance for sensing the quality of the light environment in multiple organisms.


Received for publication, October 19, 2006 , and in revised form, January 19, 2007.

* This work was supported by Grant 0343737 from the National Science Foundation and by CNRS, Action Concertée Incitative/Biologie Cellulaire, Moleculaire et Structurale (ACI/BCMS), Deutsche Forschungsgemeinschaft (FOR526 BA985/10-2, BI464/8-2), and the Research Foundation-Flanders (postdoctoral fellowship to F. V.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Formula The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1 and 2.

1 Permanent address: Inst. of Biological Sciences, College of Arts and Sciences, University of the Philippines Los Banos College, Laguna 4031, Philippines.

2 To whom correspondence should be addressed: Université Paris VI, FRE-CNRS 2846, Casier 156, 4 Place Jussieu, 75005 Paris. Tel.: 33-1-44272916; Fax: 33-1-44272916; E-mail: ahmad{at}ccr.jussieu.fr.


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