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July 1st, 2025
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Instituto de Biologia Molecular y Celular de Rosario, Argentina
plant biology
biorxiv

A canonical chloroplast unfolded protein response triggered by misfolded polypeptides

Cantoia, A.Open in Google Scholar•Bertero, F.Open in Google Scholar•Berrocal, R.Open in Google Scholar•Ceccarelli, E. A.Open in Google Scholar•Blanco, N. E.Open in Google Scholar•Rosano, G. L.Open in Google Scholar

Photosynthetic efficiency and plant viability rely on chloroplast protein homeostasis. While unfolded protein responses (UPRs) in the endoplasmic reticulum and mitochondria have been extensively characterized, the chloroplast UPR (cpUPR) remains less defined, partly due to the off-target effects of traditional stress-inducing methods. In this study, we provide direct evidence for the existence of the cpUPR by expressing engineered, folding-defective variants of ferredoxin-NADP reductase (FNR) in plant chloroplasts. The expression of aggregation-prone proteins inside the organelle triggered a robust upregulation of chloroplast quality control components, including CLPB3, CLPC1/C2, and HSP90C, as revealed by immunodetection and quantitative proteomics. The proteomic response scaled with the severity of the folding defect, with the fully insoluble FNR {Delta}20 variant inducing broader changes than the partially soluble {Delta}3 variant. Network analysis showed that most differentially abundant proteins were chloroplastic and clustered into functional groups related to proteostasis and photosynthesis. Comparative analysis with lincomycin-treated plants highlighted the specificity and advantages of using misfolded proteins to study the cpUPR. Expression of the folding variants conferred tolerance to heat treatment, suggesting that the response can enhance plant fitness. Taken together, our work establishes the cpUPR as a specific stress response in chloroplasts and provides new tools for its characterization.

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