EXECUTER-mediated singlet oxygen signaling in plants: Mechanisms, evolution, and functional diversification

Singlet oxygen (¹O₂) is a highly reactive, chloroplast-derived reactive oxygen species that functions not only as a damaging oxidant but also as a signaling molecule regulating gene expression, stress responses, and development. The EXECUTER (EX) family, comprising EX1 and its paralog EX2, is central to ¹O₂-triggered retrograde signaling in Arabidopsis thaliana. Recent mechanistic advances have revealed that EX1 undergoes post-translational oxidation and proteolytic turnover and that EX1-derived small peptides interact with TOC/TIC translocons to activate signaling cascades. EX1 also has unexpected functions in darkness, during which it modulates auxin-responsive gene networks. Comparative genomic analyses further show that EX-like proteins containing the conserved singlet oxygen sensor domain are present in green algae. By contrast, the complete EX architecture, including both the singlet oxygen sensor and UvrBC-like domains, emerged in charophytes and subsequently diversified across major plant lineages. In this review, we present classical and emerging insights into EX-mediated signaling, highlight evolutionary patterns of EX proteins across the plant kingdom, and discuss how understanding EX1/EX2 dynamics may inform strategies to engineer reactive oxygen species perception, stress tolerance, and crop growth. We propose a unified model of EX-mediated ¹O₂ sensing and outline key unresolved questions to guide future research.