Chloroplast precursor protein preClpD overaccumulation triggers multilevel reprogramming of gene expression and a heat shock-like response

Zheng-Hui Hong, Liyu Zhu, Lin-Lin Gao, Zhe Zhu, Tong Su, Leonard Krall, Xu-Na Wu, Ralph Bock and Guo-Zhang Wu ()
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Zheng-Hui Hong: Shanghai Jiao Tong University
Liyu Zhu: Shanghai Jiao Tong University
Lin-Lin Gao: Shanghai Jiao Tong University
Zhe Zhu: Yunnan University
Tong Su: Shanghai Jiao Tong University
Leonard Krall: Yunnan University
Xu-Na Wu: Yunnan University
Ralph Bock: Max-Planck-Institut für Molekulare Pflanzenphysiologie
Guo-Zhang Wu: Shanghai Jiao Tong University

Nature Communications, 2025, vol. 16, issue 1, 1-20

Abstract: Abstract Thousands of nucleus-encoded chloroplast proteins are synthesized as precursors on cytosolic ribosomes and posttranslationally imported into chloroplasts. Cytosolic accumulation of unfolded chloroplast precursor proteins (e.g., under stress conditions) is hazardous to the cell. The global cellular responses and regulatory pathways involved in triggering appropriate responses are largely unknown. Here, by inducible and constitutive overexpression of ClpD-GFP to result in precursor protein overaccumulation, we present a comprehensive picture of multilevel reprogramming of gene expression in response to chloroplast precursor overaccumulation stress (cPOS), reveal a critical role of translational activation in the expression of cytosolic chaperones (heat-shock proteins, HSPs), and demonstrate that chloroplast-derived reactive oxygen species act as retrograde signal for the transcriptional activation of small HSPs. Furthermore, we reveal an important role of the chaperone ClpB1/HOT1 in maintaining cellular proteostasis upon cPOS. Together, our observations uncover a cytosolic heat shock-like response to cPOS and provide insights into the underlying molecular mechanisms.

Date: 2025
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DOI: 10.1038/s41467-025-59043-3

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