The <i>Arabidopsis</i> SAFEGUARD1 suppresses singlet oxygen-induced stress responses by protecting grana margins

Abstract

Singlet oxygen (¹O₂), 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 <i>fluorescent</i> (<i>flu</i>) mutant, its release causes seedling lethality and inhibits mature plant growth. However, these drastic phenotypes are suppressed when EXECUTER1 (EX1) is absent in the <i>flu ex1</i> double mutant. We identified SAFEGUARD1 (SAFE1) in a screen of ethyl methanesulfonate (EMS) mutagenized <i>flu ex1</i> plants for suppressor mutants with a <i>flu</i>-like phenotype. In <i>flu ex1 safe1</i>, all ¹O₂-induced responses, including transcriptional rewiring of nuclear gene expression, return to levels, such as, or even higher than, those in <i>flu</i> Without SAFE1, grana margins (GMs) of chloroplast thylakoids (Thys) are specifically damaged upon ¹O₂ generation and associate with plastoglobules (PGs). SAFE1 is localized in the chloroplast stroma, and release of ¹O₂ induces SAFE1 degradation via chloroplast-originated vesicles. Our paper demonstrates that <i>flu</i>-produced ¹O₂ triggers an EX1-independent signaling pathway and proves that SAFE1 suppresses this signaling pathway by protecting GMs.