Communication between organelles and the nucleus is essential for fitness and survival. Retrograde signals are cues emitted from the organelles to regulate nuclear gene expression. GENOMES UNCOUPLED1 (GUN1), a protein of unknown function, has emerged as a central integrator, participating in multiple retrograde signalling pathways that collectively regulate the nuclear transcriptome. Here, we show that GUN1 regulates chloroplast protein import through interaction with the import-related chaperone cpHSC70-1. We demonstrated that overaccumulation of unimported precursor proteins (preproteins) in the cytosol causes a GUN phenotype in the wild-type background and enhances the GUN phenotype of the gun1 mutant. Furthermore, we identified the cytosolic HSP90 chaperone complex, induced by overaccumulated preproteins, as a central regulator of photosynthetic gene expression that determines the expression of the GUN phenotype. Taken together, our results suggest a model in which protein import capacity, folding stress and the cytosolic HSP90 complex control retrograde communication.
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We thank the MPI-MP GreenTeam for help with plant transformation. We are grateful to D. Leister (Ludwig-Maximilians-University Munich) for providing the gun1-102 seeds, Å. Strand (Umeå University, Umeå, Sweden) for providing seeds of the HSP90 RNAi lines, A. Clarke (Gothenburg University) for providing antibodies against Clp proteins and M. Gorka from MPI-MP for running the mass spectrometry samples to quantify the TOC–TIC subunits. This research was financed by the Max Planck Society, grants from the Deutsche Forschungsgemeinschaft to R.B. (FOR 804; SFB-TRR 175 A04), R.Z. (ZO 302/4-1; SFB-TRR 175 A04) and B.G. (SFB-TRR 175 C04), and grants from the Biotechnology and Biological Sciences Research Council (BBSRC) to R.P.J. (research grant numbers BB/N006372/1 and BB/R009333/1).
The authors declare no competing interests.
Journal peer review information: Nature Plants thanks Chanhong Kim, Thomas Pfannschmidt and Jin-Zheng Wang for their contribution to the peer review of this work.
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Supplementary Figures 1–29 and Supplementary Tables 1–5.
Data from array-based ribosome profiling experiments.
Mass spectrometry data from co-IP experiments.
Mass spectrometry data of proteomic analyses of the wild type, the gun1 and clpc1 single mutants and the gun1 clpc1 double mutant.
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Wu, GZ., Meyer, E.H., Richter, A.S. et al. Control of retrograde signalling by protein import and cytosolic folding stress. Nat. Plants 5, 525–538 (2019). https://doi.org/10.1038/s41477-019-0415-y