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Structure of the chloroplast ribosome with chl-RRF and hibernation-promoting factor

Nature Plants volume 4, pages 212–217 (2018)Cite this article

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A Publisher Correction to this article was published on 23 July 2018

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Abstract

Oxygenic photosynthesis produces oxygen and builds a variety of organic compounds, changing the chemistry of the air, the sea and fuelling the food chain on our planet. The photochemical reactions underpinning this process in plants take place in the chloroplast. Chloroplasts evolved ~1.2 billion years ago from an engulfed primordial diazotrophic cyanobacterium, and chlororibosomes are responsible for synthesis of the core proteins driving photochemical reactions. Chlororibosomal activity is spatiotemporally coupled to the synthesis and incorporation of functionally essential co-factors, implying the presence of chloroplast-specific regulatory mechanisms and structural adaptation of the chlororibosome1,2. Despite recent structural information3,4,5,6, some of these aspects remained elusive. To provide new insights into the structural specialities and evolution, we report a comprehensive analysis of the 2.9–3.1 Å resolution electron cryo-microscopy structure of the spinach chlororibosome in complex with its recycling factor and hibernation-promoting factor. The model reveals a prominent channel extending from the exit tunnel to the chlororibosome exterior, structural re-arrangements that lead to increased surface area for translocon binding, and experimental evidence for parallel and convergent evolution of chloro- and mitoribosomes.

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Fig. 1: The structure of the chlororibosome.
Fig. 2: The exit tunnel.
Fig. 3: Implications for the chl-SSU.
Fig. 4: Chl-RRF and PSRP1 bound to the chlororibosome.

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Change history

  • 23 July 2018

    In the version of this Article originally published, the name of co-author Annemarie Perez Boerema was coded wrongly, resulting in it being incorrect when exported to citation databases. This has been corrected, though no visible changes will be apparent.

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Acknowledgements

The data were collected at the UK national electron bio-imaging centre (eBIC, proposal EM15290-2) and the Swedish national cryo-EM facility, funded by the Knut and Alice Wallenberg, and the Family Erling Persson foundations. We thank A. Siebert, D. Clare, M. Carroni and J. Conrad for help with data collection, S. Fleischmann for computing support and A. Petrov for help with the analysis of rRNA. This work was supported by the Swedish Foundation for Strategic Research (Future Leaders Grant FFL15:0325), Ragnar Söderberg Foundation (Fellowship in Medicine M44/16), Swedish Research Council (NT_2015-04107, NT-2013-5901), Raymond & Beverly Sackler Foundation, Swedish e-Science Center FEBS Long-Term Fellowship (SA), Lawski Scholarship (BOF) and Erasmus Mundus Programme (BP).

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Author notes

  1. Bijoya Paul

    Present address: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

  2. These authors contributed equally: Annemarie Perez Boerema and Shintaro Aibara.

Authors and Affiliations

  1. Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, Sweden

    Annemarie Perez Boerema, Shintaro Aibara, Bijoya Paul, Victor Tobiasson, Dari Kimanius, Björn O. Forsberg, Karin Wallden, Erik Lindahl & A. Amunts

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Contributions

A.P.B. and A.A. designed the study. A.P.B., B.P. and A.A. purified chlororibosomes. A.P.B., S.A., B.P. and A.A. prepared cryosamples, optimized conditions and collected data. A.P.B. and S.A. processed data. A.P.B., S.A., B.P., V.T., D.K., B.O.F. and K.W. built the model. A.P.B., S.A. and A.A. wrote the manuscript. All authors discussed and commented on the final manuscript.

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Correspondence to A. Amunts.

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Supplementary Tables 1–4 and References, and Supplementary Figures 1–10.

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Perez Boerema, A., Aibara, S., Paul, B. et al. Structure of the chloroplast ribosome with chl-RRF and hibernation-promoting factor. Nature Plants 4, 212–217 (2018). https://doi.org/10.1038/s41477-018-0129-6

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