Abstract

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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Data availability

Mass spectrometry-based proteomic data have been deposited in the PRIDE partner repository of the ProteomeXchange Consortium with the data set identifiers PXD010730 and PXD013005. All other data are available in the main text or the Supplementary Information.

Additional information

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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Acknowledgements

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).

Author information

Author notes

    • Etienne H. Meyer

    Present address: Martin-Luther-Universität Halle-Wittenberg, Institute of Plant Physiology, Halle, Germany

Affiliations

  1. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam, Germany

    • Guo-Zhang Wu
    • , Etienne H. Meyer
    • , Maja Schuster
    • , Mark A. Schöttler
    • , Dirk Walther
    • , Reimo Zoschke
    •  & Ralph Bock
  2. Institute of Biology/Plant Physiology, Humboldt-Universität zu Berlin, Berlin, Germany

    • Andreas S. Richter
    •  & Bernhard Grimm
  3. Department of Plant Sciences, University of Oxford, Oxford, UK

    • Qihua Ling
    •  & R. Paul Jarvis

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Contributions

R.B. and G.-Z.W. conceived and designed the research. G.-Z.W. performed most of the experiments. E.H.M. performed the mass spectrometry-based proteomics. A.R. and B.G. investigated the import of the TPB enzymes. M.S. performed the ribosome profiling experiments, analysed and discussed the results with G.-Z.W. and R.Z. Q.L. and G.-Z.W. conducted the protein import assays and analysed the results with R.P.J. M.A.S. performed the photosynthesis measurements. D.W. mapped peptides to the transit peptide regions of chloroplast proteins. R.B. and G.-Z.W. wrote the manuscript, with input from the co-authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Ralph Bock.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–29 and Supplementary Tables 1–5.

  2. Reporting Summary

  3. Supplementary Data 1

    Data from array-based ribosome profiling experiments.

  4. Supplementary Data 2

    Mass spectrometry data from co-IP experiments.

  5. Supplementary Data 3

    Mass spectrometry data of proteomic analyses of the wild type, the gun1 and clpc1 single mutants and the gun1clpc1 double mutant.

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https://doi.org/10.1038/s41477-019-0415-y