Cryo-EM structure of the spinach chloroplast ribosome reveals the location of plastid-specific ribosomal proteins and extensions

Nucleic Acids Research

Volumn 45, Issue 5, 2017, Pages 2887-2896

  Graf, Michael ^a   Arenz, Stefan ^a   Huter, Paul ^a   Dönhöfer, Alexandra ^a   Nováček, Jiří ^b   Wilson, Daniel N ^a,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b MASARYK UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME PROTEIN; RIBOSOME RNA; CHLOROPLAST PROTEIN;

ARTICLE; BINDING SITE; CHLOROPLAST; COMPUTER MODEL; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; MASS SPECTROMETRY; MOLECULAR MODEL; NONHUMAN; PLASTID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; RIBOSOME; RNA STABILITY; SEQUENCE HOMOLOGY; SPINACH; TRANSMISSION ELECTRON MICROSCOPY; CHEMISTRY; LARGE RIBOSOMAL SUBUNIT; METABOLISM; SMALL RIBOSOMAL SUBUNIT;

BINDING SITES; CHLOROPLAST PROTEINS; CHLOROPLASTS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA STABILITY; RNA, RIBOSOMAL; SPINACIA OLERACEA;

EID: 85018329734     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw1272     Document Type: Article

References (52)

1. Reyes-Prieto, A., Weber, A.P. and Bhattacharya, D. (2007) The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet., 41, 147-168.
2. Tiller, N. and Bock, R. (2014) The translational apparatus of plastids and its role in plant development. Mol. Plant, 7, 1105-1120.
3. Sun, Y. and Zerges, W. (2015) Translational regulation in chloroplasts for development and homeostasis. Biochim. Biophys. Acta, 1847, 809-820.
4. Schmitz-Linneweber, C., Maier, R.M., Alcaraz, J.P., Cottet, A., Herrmann, R.G. and Mache, R. (2001) The plastid chromosome of spinach (Spinacia oleracea): Complete nucleotide sequence and gene organization. Plant Mol. Biol., 45, 307-315.
5. Yamaguchi, K. and Subramanian, A.R. (2000) The plastid ribosomal proteins. Identification of all the proteins in the 50S subunit of an organelle ribosome (chloroplast). J. Biol. Chem., 275, 28466-28482.
6. Yamaguchi, K., von Knoblauch, K. and Subramanian, A.R. (2000) The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). J. Biol. Chem., 275, 28455-28465.
7. Yamaguchi, K. and Subramanian, A.R. (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. Eur. J. Biochem., 270, 190-205.
8. Sharma, M.R., Wilson, D.N., Datta, P.P., Barat, C., Schluenzen, F., Fucini, P. and Agrawal, R.K. (2007) Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc. Natl. Acad. Sci. U.S.A., 104, 19315-19320.
9. Bartsch, M., Kimura, M. and Subramanian, A.R. (1982) Purification, primary structure, and homology relationships of a chloroplast ribosomal protein. Proc. Natl. Acad. Sci. U.S.A., 79, 6871-6875.
10. Grant, T. and Grigorieff, N. (2015) Measuring the optimal exposure for single particle cryo-EM using a 2.6 A reconstruction of rotavirus VP6. Elife, 4, e06980.
11. Rohou, A. and Grigorieff, N. (2015) CTFFIND4: Fast and accurate defocus estimation from electron micrographs. J. Struct. Biol., 192, 216-221.
12. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M. and Leith, A. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol., 116, 190-199.
13. Becker, T., Franckenberg, S., Wickles, S., Shoemaker, C.J., Anger, A.M., Armache, J.P., Sieber, H., Ungewickell, C., Berninghausen, O., Daberkow, I. et al. (2012) Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature, 482, 501-506.
14. Chen, J.Z. and Grigorieff, N. (2007) SIGNATURE: A single-particle selection system for molecular electron microscopy. J. Struct. Biol., 157, 168-173.
15. Arenz, S., Meydan, S., Starosta, A.L., Berninghausen, O., Beckmann, R., Vazquez-Laslop, N. and Wilson, D.N. (2014) Drug sensing by the ribosome induces translational arrest via active site perturbation. Mol. Cell, 56, 446-452.
16. Loerke, J., Giesebrecht, J. and Spahn, C.M. (2010) Multiparticle cryo-EM of ribosomes. Methods Enzymol., 483, 161-177.
17. Grigorieff, N. (2007) FREALIGN: High-resolution refinement of single particle structures. J. Struct. Biol., 157, 117-125.
18. Kucukelbir, A., Sigworth, F.J. and Tagare, H.D. (2014) Quantifying the local resolution of cryo-EM density maps. Nat. Methods, 11, 63-65.
19. Scheres, S.H. (2012) RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol., 180, 519-530.
20. Fischer, N., Neumann, P., Konevega, A.L., Bock, L.V., Ficner, R., Rodnina, M.V. and Stark, H. (2015) Structure of the E. coli ribosome-EF-Tu complex at <3 A resolution by C-corrected cryo-EM. Nature, 520,567-570.
21. Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D'Souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Muller, K.M. et al. (2002) The comparative RNA web (CRW) site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. Biomed Central Bioinformatics, 3 2.
22. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF chimera-A visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
23. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
24. Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis, 18, 2714-2723.
25. Soding, J., Biegert, A. and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res., 33, W244-W248.
26. Buchan, D., Minneci, F., Nugent, T., Bryson, K. and Jones, D. (2013) Scalable web services for the PSIPRED Protein Analysis Workbench. Nucleic Acids Res., 41 W340-W348.
27. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
28. Vagin, A.A., Steiner, R.A., Lebedev, A.A., Potterton, L., McNicholas, S., Long, F. and Murshudov, G.N. (2004) REFMAC5 dictionary: Organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr., 60, 2184-2195.
29. Brown, A., Long, F., Nicholls, R.A., Toots, J., Emsley, P. and Murshudov, G. (2015) Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions. Acta Crystallogr. D Biol. Crystallogr., 71, 136-153.
30. Amunts, A., Brown, A., Bai, X.C., Llacer, J.L., Hussain, T., Emsley, P., Long, F., Murshudov, G., Scheres, S.H. and Ramakrishnan, V. (2014) Structure of the yeast mitochondrial large ribosomal subunit. Science, 343, 1485-1489.
31. Chen, V.B., Arendall, W.B. 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr., 66, 12-21.
32. Noeske, J., Wasserman, M.R., Terry, D.S., Altman, R.B., Blanchard, S.C. and Cate, J.H. (2015) High-resolution structure of the Escherichia coli ribosome. Nat. Struct. Mol. Biol., 22, 336-341.
33. Llacer, J.L., Hussain, T., Marler, L., Aitken, C.E., Thakur, A., Lorsch, J.R., Hinnebusch, A.G. and Ramakrishnan, V. (2015) Conformational differences between open and closed states of the eukaryotic translation initiation complex. Mol. Cell, 59, 399-412.
34. Hussain, T., Llacer, J.L., Wimberly, B.T., Kieft, J.S. and Ramakrishnan, V. (2016) Large-scale movements of IF3 and tRNA during bacterial translation initiation. Cell, 167, 133-144.
35. Wimberly, B.T., Brodersen, D.E., Clemons, W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T. and Ramakrishnan, V. (2000) Structure of the 30S ribosomal subunit. Nature, 407, 327-339.
36. Sharma, M.R., Donhofer, A., Barat, C., Marquez, V., Datta, P.P., Fucini, P., Wilson, D.N. and Agrawal, R.K. (2010) PSRP1 is not a ribosomal protein, but a ribosome-binding factor that is recycled by the ribosome-recycling factor (RRF) and elongation factor G (EF-G). J. Biol. Chem., 285, 4006-4014.
37. Yoshida, H. and Wada, A. (2014) The 100S ribosome: Ribosomal hibernation induced by stress. Wiley interdisciplin. Rev. RNA, 5, 723-732.
38. Vila-Sanjurjo, A., Schuwirth, B.S., Hau, C.W. and Cate, J.H.D. (2004) Structural basis for the control of translational initiation during stress. Nat. Struct. Mol. Biol., 11, 1054-1059.
39. Polikanov, Y.S., Blaha, G.M. and Steitz, T.A. (2012) How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science, 336, 915-918.
40. Puri, P., Eckhardt, T.H., Franken, L.E., Fusetti, F., Stuart, M.C., Boekema, E.J., Kuipers, O.P., Kok, J. and Poolman, B. (2014) Lactococcus lactis YfiA is necessary and sufficient for ribosome dimerization. Mol. Microbiol., 91, 394-407.
41. Basu, A. and Yap, M.N. (2016) Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res., 44, 4881-4893.
42. Wilson, D.N., Schluenzen, F., Harms, J.M., Yoshida, T., Ohkubo, T., Albrecht, R., Buerger, J., Kobayashi, Y. and Fucini, P. (2005) X-ray crystallography study on ribosome recycling: The mechanism of binding and action of RRF on the 50S ribosomal subunit. EMBO J., 24, 251-260.
43. Weixlbaumer, A., Petry, S., Dunham, C.M., Selmer, M., Kelley, A.C. and Ramakrishnan, V. (2007) Crystal structure of the ribosome recycling factor bound to the ribosome. Nat. Struct. Mol. Biol., 14, 733-737.
44. Amunts, A., Brown, A., Toots, J., Scheres, S.H. and Ramakrishnan, V. (2015) Ribosome. The structure of the human mitochondrial ribosome. Science, 348, 95-98.
45. Greber, B.J., Bieri, P., Leibundgut, M., Leitner, A., Aebersold, R., Boehringer, D. and Ban, N. (2015) Ribosome. The complete structure of the 55S mammalian mitochondrial ribosome. Science, 348, 303-308.
46. Ban, N., Nissen, P., Hansen, J., Moore, P.B. and Steitz, T.A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science, 289, 905-920.
47. Ben-Shem, A., Garreau de Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G. and Yusupov, M. (2011) The structure of the eukaryotic ribosome at 3.0 A resolution. Science, 334, 1524-1529.
48. Anger, A.M., Armache, J.P., Berninghausen, O., Habeck, M., Subklewe, M., Wilson, D.N. and Beckmann, R. (2013) Structures of the human and Drosophila 80S ribosome. Nature, 497, 80-85.
49. Halic, M., Blau, M., Becker, T., Mielke, T., Pool, M.R., Wild, K., Sinning, I. and Beckmann, R. (2006) Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature, 444, 507-511.
50. Jomaa, A., Boehringer, D., Leibundgut, M. and Ban, N. (2016) Structures of the E. coli translating ribosome with SRP and its receptor and with the translocon. Nat. Commun., 7, 10471.
51. Ahmed, T., Yin, Z. and Bhushan, S. (2016) Cryo-EM structure of the large subunit of the spinach chloroplast ribosome. Sci. Rep., 6, 35793.
52. Wilson, D.N. and Beckmann, R. (2011) The ribosomal tunnel as a functional environment for nascent polypeptide folding and translational stalling. Curr. Opin. Struct. Biol., 21, 1-10.