Interplay between antioxidants in response to photooxidative stress in Arabidopsis

Aditya Kumar (1) , Ankush Prasad (1) , Michaela Sedlářová (2) , Brigitte Ksas (3) , Michel Havaux (3, 4) , Pavel Pospíšil (1)

1 CRH - Centre of the Region Haná for Biotechnological and Agricultural Research [Univ Palacký]
2 Department of Botany [Univ Palacký]
3 PPV - Protéines de Protection des Végétaux
4 PEPSS - Plant Environmental Physiology and Stress Signaling

Tocochromanols (tocopherols, tocotrienols and plastochromanol-8), isoprenoid quinone (plastoquinone-9 and plastoquinol-9) and carotenoids (carotenes and 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 analyzed 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 $\alpha$-tocopherol, plastochromanol-8, plastoquinone-9/plastoquinol-9 and zeaxanthin. In the first line of defense (non-radical mechanism), singlet oxygen is either physically or chemically quenched by α-tocopherol; however, when α-tocopherol is consumed, zeaxanthin and plastoquinone-9/plastoquinol-9 can provide alternative protection against singlet oxygen toxicity by functional replacement of $\alpha$-tocopherol either by zeaxanthin for the physical quenching or by plastoquinone-9/plastoquinol-9 for the chemical quenching. When singlet oxygen escapes this first line of defense, it oxidizes lipids and forms lipid hydroperoxides, which are oxidized to lipid peroxyl radicals by ferric iron. In the second line of defense (radical mechanism), lipid peroxyl radicals are scavenged by $\alpha$-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 $\alpha$-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: Antioxidants Arabidopsis thaliana Lipid peroxidation Plastoquinone-9 Photooxidative stress Singlet oxygen Tocochromanol

Domains: Life Sciences [q-bio]

Aditya Kumar, Ankush Prasad, Michaela Sedlářová, Brigitte Ksas, Michel Havaux, et al.. Interplay between antioxidants in response to photooxidative stress in Arabidopsis. Free Radical Biology and Medicine, 2020, 160, pp.894-907. ⟨10.1016/j.freeradbiomed.2020.08.027⟩. ⟨cea-03540812⟩