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

ABSTRACT 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 H ₂ O ₂ induces mitochondrial elongation, whereas calcium chelation blocks both H ₂ O ₂ ‐ and HL‐induced responses, demonstrating that chloroplast‐derived H ₂ O ₂ 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 H ₂ O ₂ 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.