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Wang, Liangsheng; Leister, Dario; Guan, Li; Zheng, Yi; Schneider, Katja; Lehmann, Martin; Apel, Klaus and Kleine, Tatjana (2020): The Arabidopsis SAFEGUARD1 suppresses singlet oxygen-induced stress responses by protecting grana margins. In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, No. 12: pp. 6918-6927

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Singlet oxygen (O-1(2)), the major reactive oxygen species (ROS) produced in chloroplasts, has been demonstrated recently to be a highly versatile signal that induces various stress responses. In the fluorescent (flu) mutant, its release causes seedling lethality and inhibits mature plant growth. However, these drastic phenotypes are suppressed when EXECUTER1 (EX1) is absent in the flu ex1 double mutant. We identified SAFEGUARD1 (SAFE1) in a screen of ethyl methanesulfonate (EMS) mutagenized flu ex1 plants for suppressor mutants with a flu-like phenotype. In flu ex1 safe1, all O-1(2)-induced responses, including transcriptional rewiring of nuclear gene expression, return to levels, such as, or even higher than, those in flu. Without SAFE1, grana margins (GMs) of chloroplast thylakoids (Thys) are specifically damaged upon O-1(2) generation and associate with plastoglobules (PGs). SAFE1 is localized in the chloroplast stroma, and release of O-1(2) induces SAFE1 degradation via chloroplast-originated vesicles. Our paper demonstrates that flu-produced O-1(2) triggers an EX1-independent signaling pathway and proves that SAFE1 suppresses this signaling pathway by protecting GMs.

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