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ABSTRACT Environmental stress demands precise coordination among organelles to maintain cellular homeostasis. InArabidopsis, 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 H₂O₂induces mitochondrial elongation, whereas calcium chelation blocks both H₂O₂‐ and HL‐induced responses, demonstrating that chloroplast‐derived H₂O₂activates 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 H₂O₂initiates 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. 

Abstract As a universal second messenger, calcium (Ca2+) transmits specific cellular signals via a spatiotemporal signature generated from its extracellular source and internal stores. Our knowledge of the mechanisms underlying the generation of a Ca2+ signature is hampered by limited tools for simultaneously monitoring dynamic Ca2+ levels in multiple subcellular compartments. To overcome the limitation and to further improve spatiotemporal resolutions, we have assembled a molecular toolset (CamelliA lines) in Arabidopsis (Arabidopsis thaliana) that enables simultaneous and high-resolution monitoring of Ca2+ dynamics in multiple subcellular compartments through imaging different single-colored genetically encoded calcium indicators. We uncovered several Ca2+ signatures in three types of Arabidopsis cells in response to internal and external cues, including rapid oscillations of cytosolic Ca2+ and apical plasma membrane Ca2+ influx in fast-growing Arabidopsis pollen tubes, the spatiotemporal relationship of Ca2+ dynamics in four subcellular compartments of root epidermal cells challenged with salt, and a shockwave-like Ca2+ wave propagating in laser-wounded leaf epidermis. These observations serve as a testimony to the wide applicability of the CamelliA lines for elucidating the subcellular sources contributing to the Ca2+ signatures in plants. 

SUMMARY Plastid‐to‐nucleus communication, crucial for regulating stress‐responsive gene expression, has long intrigued researchers. This study reveals how the plastidial metabolite 2‐C‐methyl‐D‐erythritol‐2,4‐cyclopyrophosphate (MEcPP) orchestrates transcriptional reprogramming by modulating the rapid stress response element (RSRE), a conserved regulatory hub in the plant general stress response network. Yeast one‐hybrid assays identified HAT1, a class II HD‐Zip protein, as a negative regulator of RSRE. Genetic analyses, including HAT1 overexpression and knockdowns, confirmed its role in suppressing RSRE activity. Interaction assays uncovered a suppression network involving HAT1, the co‐repressor TOPLESS (TPL), and the nuclear importin IMPα‐9. Furthermore, HAT1 interacts with calmodulin‐binding transcription activator 3 (CAMTA3), a calcium/calmodulin‐binding transcription factor known to activate RSRE. AlphaFold modeling provided insights into the architecture of the HAT1‐RSRE complex and HAT‐CAMTA3 interaction, supported by conserved domains across plant species. Under stress condition, MEcPP accumulation promotes the 26S proteasomal degradation of TPL and IMPα‐9 while reduces auxin‐dependent HAT1 expression. Additionally, MEcPP enhances Ca²⁺influx, activating CAMTA3 and enabling it to bind RSRE, thereby initiating the transcription of stress response genes. This dual mechanism—dismantling suppressors (HAT1, TPL, and IMPα‐9) and activating CAMTA3—underscores MEcPP's central role in plastid‐to‐nucleus signaling. These findings emphasize MEcPP's pivotal function in dynamically regulating gene expression to maintain cellular homeostasis under environmental stress.