Interplay between antioxidants in response to photooxidative stress in Arabidopsis

Tocochromanols (tocopherols and plastochromanol-8), isoprenoid quinone (plastoquinone-9 and plastoquinol-9) and carotenoids (xanthophylls), are lipid-soluble antioxidants in the chloroplasts, which play an important defensive role against photooxidative stress in plants. In this study, the interplay between the antioxidant activities of those compounds in excess light stress was analysed in wild-type (WT) Arabidopsis thaliana and in a tocopherol cyclase mutant (vte1), a homogentisate phytyl transferase mutant (vte2) and a tocopherol cyclase overexpressor (VTE1oex). The results reveal a strategy of cooperation and replacement between α-tocopherol, plastochromanol-8, plastoquinone-9 and zeaxanthin. In the first line of defence (non-radical mechanism), singlet oxygen is either physically or chemically quenched by α-tocopherol; however, when α-tocopherol is absent or consumed, zeaxanthin and plastoquinone-9/plastoquinol-9 can provide an alternative protection against singlet oxygen toxicity either by functional replacement of α-tocopherol by zeaxanthin for the physical quenching or by functional replacement of α-tocopherol by plastoquinone-9 for the chemical quenching. When singlet oxygen escapes this first line of defence, it oxidizes lipids and forms lipid hydroperoxides, which are oxidized to lipid peroxyl radicals by ferric iron. In the second line of defence (radical mechanism), lipid peroxyl radicals are scavenged by α-tocopherol. After its consumption, plastochromanol-8 overtakes this function. We provide a comprehensive description of the reaction pathways underlying the non-radical and radical antioxidant activities of α-tocopherol, carotenoids, plastoquinone-9/plastoquinol-9 and plastochromanol-8. The interplay between the different plastid lipid-soluble antioxidants in the non-radical and the radical mechanism provides step by step insights into protection against photooxidative stress in higher plants.

Keywords: Arabidopsis thaliana; antioxidants; lipid peroxidation; photooxidative stress; plastoquinone-9; singlet oxygen; tocochromanols.