Chemical Quenching of Singlet Oxygen by Carotenoids in Plants

Carotenoids are considered to be the first line of defense of plants against singlet oxygen (O-1(2)) toxicity because of their capacity to quench O-1(2) as well as triplet chlorophylls through a physical mechanism involving transfer of excitation energy followed by thermal deactivation. Here, we show that leaf carotenoids are also able to quench O-1(2) by a chemical mechanism involving their oxidation. In vitro oxidation of beta-carotene, lutein, and zeaxanthin by O-1(2) generated various aldehydes and endoperoxides. A search for those molecules in Arabidopsis (Arabidopsis thaliana) leaves revealed the presence of O-1(2)-specific endoperoxides in low-light-grown plants, indicating chronic oxidation of carotenoids by O-1(2). beta-Carotene endoperoxide, but not xanthophyll endoperoxide, rapidly accumulated during high-light stress, and this accumulation was correlated with the extent of photosystem (PS) II photoinhibition and the expression of various O-1(2) marker genes. The selective accumulation of beta-carotene endoperoxide points at the PSII reaction centers, rather than the PSII chlorophyll antennae, as a major site of O-1(2) accumulation in plants under high-light stress. beta-Carotene endoperoxide was found to have a relatively fast turnover, decaying in the dark with a half time of about 6 h. This carotenoid metabolite provides an early index of O-1(2) production in leaves, the occurrence of which precedes the accumulation of fatty acid oxidation products.