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

• Published in: The Journal of biological chemistry 2007-08, Vol.282 (31), p.22605-22618
• Main Authors: Johnson, Matthew P., Havaux, Michel, Triantaphylides, Christian, Ksas, Brigitte, Pascal, Andrew A., Robert, Bruno, Davison, Paul A., Ruban, Alexander V., Horton, Peter
• Format: Article
• Language: English
• Subjects: Antioxidants - chemistry; Antioxidants - metabolism; Apoproteins - metabolism; Arabidopsis - metabolism; Light; Lipids - chemistry; Oxidants - metabolism; Oxidative Stress; Photochemistry - methods; Photosystem II Protein Complex - metabolism; Plant Leaves - metabolism; Plant Proteins - metabolism; Protein Binding; Spectrum Analysis, Raman; Temperature; Thylakoids - metabolism; Xanthophylls - biosynthesis; Xanthophylls - chemistry; Xanthophylls - metabolism; Zeaxanthins
• ISSN: 0021-9258; 1083-351X
• DOI: 10.1074/jbc.M702831200

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 β-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.