FtsH2-Dependent Proteolysis of EXECUTER1 Is Essential in Mediating Singlet Oxygen-Triggered Retrograde Signaling in .

Photosystem II reaction center (PSII RC) and light-harvesting complex inevitably generate highly reactive singlet oxygen (O) that can impose photo-oxidative damage, especially when the rate of generation exceeds the rate of detoxification. Besides being toxic, O has also been ascribed to trigger retrograde signaling, which leads to nuclear gene expression changes. Two distinctive molecular components appear to regulate O signaling: a volatile signaling molecule β-cyclocitral (β-CC) generated upon oxidation of β-carotene by O in PSII RC assembled in grana core, and a thylakoid membrane-bound FtsH2 metalloprotease that promotes O-triggered signaling through the proteolysis of EXECUTER1 (EX1) proteins associated with PSII in grana margin. The role of FtsH2 protease in O signaling was established recently in the conditional () mutant of that generates O upon dark-to-light shift. The mutant lacking functional FtsH2 significantly impairs O-triggered and EX1-mediated cell death. In the present study, the role of FtsH2 in the induction of O signaling was further clarified by analyzing the FtsH2-dependent nuclear gene expression changes in the mutant. Genome-wide transcriptome analysis showed that the inactivation of FtsH2 repressed the majority (85%) of the EX1-dependent O-responsive genes (SORGs), providing direct connection between FtsH2-mediated EX1 degradation and O-triggered gene expression changes. Furthermore, the overlap between β-CC-induced genes and EX1-FtsH2-dependent genes was very limited, further supporting the coexistence of two distinctive O signaling pathways.