Journal Article

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

Tissier, Alain, Hur, Manhoi, Zhang, Quanqing, Dehesh, Katayoon, Snyder, Emily, Guo, Jingzhe, Zanini, Andrea A., Angelos, Evan R., Part, Matthew, Ven, Wilhelmina, Balcke, Gerd Ulrich, Burch‐Smith, Tessa M., Choi, Hee‐Seung

2026

Overview

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 Ca2+ flux essential for remodeling. Proteomic and functional studies identify the Ca2+‐binding GTPase MIRO1 as a central integrator of this pathway. MIRO1 overexpression mimics HL‐induced morphodynamics, while mutations disrupting its Ca2+‐binding or acetylation motifs abolish the response, establishing Ca2+‐dependent MIRO1 activity as a prerequisite for remodeling. Together, these findings reveal an epidermis‐specific, light‐responsive network in which chloroplast‐derived H2O2 initiates Ca2+ signaling through MIRO1 to coordinate mitochondrial and ER remodeling—a spatially restricted mechanism of organellar communication and stress adaptation at the plant–environment interface. High light exposure triggers an epidermis‐specific remodeling of mitochondria and ER in Arabidopsis, driven by chloroplast‐derived signals. Live‐cell imaging shows that HL rapidly suppresses mitochondrial motility, followed by fusion‐driven elongation and ER cisternal expansion. MIRO1 emerges as a key mediator, linking chloroplast activity to dynamic interorganellar restructuring at the plant–environment interface.

• Publisher: John Wiley & Sons, Inc,Wiley
• Subject: Arabidopsis - metabolism / Arabidopsis Proteins - genetics / Arabidopsis Proteins - metabolism / Biosynthesis / chloroplast signaling / Chloroplasts / Chloroplasts - metabolism / Communication / Endoplasmic Reticulum - metabolism / Enzymes / epidermal organelle dynamics / high light stress / Homeostasis / Hydrogen Peroxide - metabolism / Influence / Light / Metabolism / Metabolites / Miro1 / Mitochondria / Mitochondria - metabolism / mitochondrial‐ER remodeling / Morphology / organelle plasticity / Phosphorylation / Plant Epidermis - metabolism / Plastids / Proteins / Signal Transduction / Stress, Physiological