Chemical Quenching of Singlet Oxygen by Carotenoids in Plants

Abstract

Abstract Carotenoids are considered to be the first line of defense of plants against singlet oxygen (1O2) toxicity because of their capacity to quench 1O2 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 1O2 by a chemical mechanism involving their oxidation. In vitro oxidation of β-carotene, lutein, and zeaxanthin by 1O2 generated various aldehydes and endoperoxides. A search for those molecules in Arabidopsis (Arabidopsis thaliana) leaves revealed the presence of 1O2-specific endoperoxides in low-light-grown plants, indicating chronic oxidation of carotenoids by 1O2. β-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 1O2 marker genes. The selective accumulation of β-carotene endoperoxide points at the PSII reaction centers, rather than the PSII chlorophyll antennae, as a major site of 1O2 accumulation in plants under high-light stress. β-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 1O2 production in leaves, the occurrence of which precedes the accumulation of fatty acid oxidation products.