Chloroplast Stress Signals Orchestrate Epidermis-Specific Remodeling of Mitochondria and ER Under High Light

Environmental stress demands precise coordination among organelles to maintain cellular homeostasis. In Arabidopsis, high light (HL) exposure triggers chloroplast-dependent remodeling of mitochondrial and endoplasmic reticulum (ER) morphology specifically in adaxial and abaxial epidermal cells, but not in mesophyll cells. Live-cell imaging reveals that HL rapidly suppresses mitochondrial motility, followed by fusion-driven elongation and ER cisternal expansion. Inhibition of photosynthetic, but not mitochondrial, electron transport abolishes these changes, confirming chloroplast activity as the upstream trigger. Pharmacological analyses show that exogenous H₂O₂ induces mitochondrial elongation, whereas calcium chelation blocks both H₂O₂- and HL-induced responses, demonstrating that chloroplast-derived H₂O₂ activates a Ca^{2 +} flux essential for remodeling. Proteomic and functional studies identify the Ca^{2 +}-binding GTPase MIRO1 as a central integrator of this pathway. MIRO1 overexpression mimics HL-induced morphodynamics, while mutations disrupting its Ca^{2 +}-binding or acetylation motifs abolish the response, establishing Ca^{2 +}-dependent MIRO1 activity as a prerequisite for remodeling. Together, these findings reveal an epidermis-specific, light-responsive network in which chloroplast-derived H₂O₂ initiates Ca^{2 +} signaling through MIRO1 to coordinate mitochondrial and ER remodeling-a spatially restricted mechanism of organellar communication and stress adaptation at the plant-environment interface.