EXECUTER2 modulates the EXECUTER1 signalosome through its singlet oxygen-dependent oxidation
2022
Dogra, Vivek | Singh, Rahul Mohan | Li, Mengping | Li, Mingyue | Singh, Somesh | Kim, Chanhong
Oxidative post-translational modifications of specific chloroplast proteins contribute to the initiation of retrograde signaling. The Arabidopsis thaliana EXECUTER1 (EX1) protein, a chloroplast-localized singlet oxygen (¹O₂) sensor, undergoes tryptophan (Trp) 643 oxidation by ¹O₂, a chloroplast-derived and light-dependent reactive oxygen species. The indole side chain of Trp is vulnerable to ¹O₂, leading to the generation of oxidized Trp variants and priming EX1 for degradation by a membrane-bound FtsH protease. The perception of ¹O₂ via Trp643 oxidation and subsequent EX1 proteolysis facilitate chloroplast-to-nucleus retrograde signaling. In this study, we discovered that the EX1-like protein EX2 also undergoes ¹O₂-dependent Trp530 oxidation and FtsH-dependent turnover, which attenuates ¹O₂ signaling by decelerating EX1-Trp643 oxidation and subsequent EX1 degradation. Consistent with this finding, the loss of EX2 function reinforces EX1-dependent retrograde signaling by accelerating EX1-Trp643 oxidation and subsequent EX1 proteolysis, whereas overexpression of EX2 produces molecular phenotypes opposite to those observed in the loss–of- function mutants of EX2. Intriguingly, phylogenetic analysis suggests that EX2 may have emerged evolutionarily to attenuate the sensitivity of EX1 toward ¹O₂. Collectively, these results suggest that EX2 functions as a negative regulator of the EX1 signalosome through its own ¹O₂-dependent oxidation, providing a new mechanistic insight into the regulation of EX1-mediated ¹O₂ signaling.
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