1 O 2 (singlet oxygen) is a reactive O 2 species produced from triplet excited chlorophylls in the chloroplasts, especially when plants are exposed to excess light energy. Similarly to other active O 2 species, 1 O 2 has a dual effect: It is toxic, causing oxidation of biomolecules, and it can act as a signal molecule that leads to cell death or to acclimation. Carotenoids are considered to be the main 1 O 2 quenchers in chloroplasts, and we show here that light stress induces the oxidation of the carotenoid β-carotene in Arabidopsis plants, leading to the accumulation of different volatile derivatives. One such compound, β-cyclocitral, was found to induce changes in the expression of a large set of genes that have been identified as 1 O 2 responsive genes. In contrast, β-cyclocitral had little effect on the expression of H 2 O 2 gene markers. β-Cyclocitral–induced reprogramming of gene expression was associated with an increased tolerance to photooxidative stress. The results indicate that β-cyclocitral is a stress signal produced in high light that is able to induce defense mechanisms and represents a likely messenger involved in the 1 O 2 signaling pathway in plants.
Carotenoids are considered to be the first line of defense of plants against singlet oxygen ( 1 O 2 ) toxicity because of their capacity to quench 1 O 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 1 O 2 by a chemical mechanism involving their oxidation. In vitro oxidation of b-carotene, lutein, and zeaxanthin by 1 O 2 generated various aldehydes and endoperoxides. A search for those molecules in Arabidopsis (Arabidopsis thaliana) leaves revealed the presence of 1 O 2 -specific endoperoxides in low-light-grown plants, indicating chronic oxidation of carotenoids by 1 O 2 . b-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 1 O 2 marker genes. The selective accumulation of b-carotene endoperoxide points at the PSII reaction centers, rather than the PSII chlorophyll antennae, as a major site of 1 O 2 accumulation in plants under high-light stress. b-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 1 O 2 production in leaves, the occurrence of which precedes the accumulation of fatty acid oxidation products.
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