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J. Biol. Chem., Vol. 282, Issue 31, 22605-22618, August 3, 2007

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Elevated Zeaxanthin Bound to Oligomeric LHCII Enhances the Resistance of Arabidopsis to Photooxidative Stress by a Lipid-protective, Antioxidant Mechanism^*

Matthew P. Johnson, Michel Havaux, Christian Triantaphylidès, Brigitte Ksas, Andrew A. Pascal^¶, Bruno Robert^¶, Paul A. Davison, Alexander V. Ruban^||, and Peter Horton¹

From the Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield, S10 2TN, United Kingdom, the CEA-Cadarache, Institut de Biologie Environnementale et de Biotechnologie, Laboratoire d'Ecophysiologie Moléculaire des Plantes, UMR 6191, CNRS-CEA-Université Aix Marseille, F-13108 Saint-Paul-lez-Durance, France, the ^¶Commisariat à l'Energie Atomique (CEA), Institut de Biologie et Technologies de Saclay (iBiTecS), URA 2096, Gif sur Yvette, F-91191, France, and the ^||School of Biological and Chemical Sciences, Queen Mary College, University of London, Mile End, Bancroft Road, London E1 4NS, United Kingdom

The xanthophyll cycle has a major role in protecting plants from photooxidative stress, although the mechanism of its action is unclear. Here, we have investigated Arabidopsis plants overexpressing a gene encoding -carotene hydroxylase, containing nearly three times the amount of xanthophyll cycle carotenoids present in the wild-type. In high light at low temperature wild-type plants exhibited symptoms of severe oxidative stress: lipid peroxidation, chlorophyll bleaching, and photoinhibition. In transformed plants, which accumulate over twice as much zeaxanthin as the wild-type, these symptoms were significantly ameliorated. The capacity of non-photochemical quenching is not significantly different in transformed plants compared with wild-type and therefore an enhancement of this process cannot be the cause of the stress tolerant phenotype. Rather, it is concluded that it results from the antioxidant effect of zeaxanthin. 80–90% of violaxanthin and zeaxanthin in wild-type and transformed plants was localized to an oligomeric LHCII fraction prepared from thylakoid membranes. The binding of these pigments in intact membranes was confirmed by resonance Raman spectroscopy. Based on the structural model of LHCII, we suggest that the protein/lipid interface is the active site for the antioxidant activity of zeaxanthin, which mediates stress tolerance by the protection of bound lipids.

Received for publication, April 3, 2007 , and in revised form, May 18, 2007.

^* This work was supported by grants from the United Kingdom Biotechnology and Biological Sciences Research Council and the INTRO2 European Union FP6 Marie Curie Training Network. 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 To whom correspondence should be addressed. Fax: 441142222712; E-mail: p.horton{at}sheffield.ac.uk.

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