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J. Biol. Chem., Vol. 283, Issue 6, 3550-3558, February 8, 2008

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Zeaxanthin Radical Cation Formation in Minor Light-harvesting Complexes of Higher Plant Antenna^*

Thomas J. Avenson¹, Tae Kyu Ahn^¶1, Donatas Zigmantas^¶, Krishna K. Niyogi^¶, Zhirong Li^¶, Matteo Ballottari^||, Roberto Bassi^||, and Graham R. Fleming^¶2

From the ^¶Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, the Department of Chemistry, Hildebrand B77, University of California, Berkeley, California 94720-1460, the Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102, and the ^||Department of Science and Technology, University of Verona, Italy 37134

Previous work on intact thylakoid membranes showed that transient formation of a zeaxanthin radical cation was correlated with regulation of photosynthetic light-harvesting via energy-dependent quenching. A molecular mechanism for such quenching was proposed to involve charge transfer within a chlorophyll-zeaxanthin heterodimer. Using near infrared (880-1100 nm) transient absorption spectroscopy, we demonstrate that carotenoid (mainly zeaxanthin) radical cation generation occurs solely in isolated minor light-harvesting complexes that bind zeaxanthin, consistent with the engagement of charge transfer quenching therein. We estimated that less than 0.5% of the isolated minor complexes undergo charge transfer quenching in vitro, whereas the fraction of minor complexes estimated to be engaged in charge transfer quenching in isolated thylakoids was more than 80 times higher. We conclude that minor complexes which bind zeaxanthin are sites of charge transfer quenching in vivo and that they can assume Non-quenching and Quenching conformations, the equilibrium LHC(N) LHC(Q) of which is modulated by the transthylakoid pH gradient, the PsbS protein, and protein-protein interactions.

Received for publication, July 10, 2007 , and in revised form, November 7, 2007.

^* This work was supported by FIRB Contract RBLA0345SF from the Italian Basic Research Foundation and Contract SAMBA Trento Research Council for foundational support (to R. B.). This work was also supported by the Korea Research Foundation Grant (KRF-2006-214-C00037) funded by the Korean Government (MOEHRD) (to T. K. A.), the National Research Initiative Competitive Grant (2006-03279) (to T. J. A.), and by the Office of Basic Energy Sciences, Chemical Sciences Division, U.S. Department of Energy (Contract DE-AC03-76SF000098) (to G. R. F. and K. K. N.). 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.

¹ These authors contributed equally to this work.

² To whom correspondence should be addressed. Tel.: 510-643-3944; Fax: 510-643-7012; E-mail: GRFleming{at}lbl.gov.

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