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Article
Nature Structural Biology  3, 771 - 781 (1996)
doi:10.1038/nsb0996-771

Crystal structure of turnip yellow mosaic virus

Mary A. Canady1, Steven B. Larson1, John Day1 & Alexander McPherson1

1Department of Biochemistry, University of California, Riverside, California 92521, USA

The structure of turnip yellow mosaic virus (TYMV) has been solved to 3.2 Å resolution and an R-value of 18.7%. The structure is consistent with models based on low resolution X-ray and electron microscopy studies, with pentameric and hexameric protein aggregates protruding from the surface and forming deep valleys at the quasi three-fold axes. The N-terminal 26 residues of the A-subunit are disordered, while those of the B- and C-subunits are seen to interact around the interior of the quasi six-fold cluster where they form an annulus. The three histidine residues of each protein subunit are located in the interior and accessible for interaction with the RNA genome. The appearance of the interior surface of the virus capsid, along with buried surface area calculations, suggest that a pentameric unit is lost during decapsidation.

REFERENCES
  1. Hirth, L. & Givord, L. Tymoviruses. In The Plant Viruses (ed. R. Koenig) 3, 163−212 (Plenum, New York, 1988).
  2. Morch, M.D., Boyer, J.C. & Haenni, A.L. Overlapping open reading frames revealed by complete nucleotide sequencing of turnip yellow mosaic virus genomic RNA. Nuc. Acids Res. 16, 6157−6173 (1988). | ISI | ChemPort |
  3. Pinck, M., Yot, P., Chapeville, F. & Duranton, H.M. Enzymatic binding of valine to the 3' end of TYMV-RNA Nature 226, 954−956 (1970). | PubMed | ISI | ChemPort |
  4. Haenni, A.L., Prochiantz, A., Bernard, O. & Chapeville, F. TYMV valyl-RNA as an amino-acid donor in protein biosynthesis. Nature new Biol. 241, 166−168 (1973). | PubMed | ISI | ChemPort |
  5. Giége, R., Florentz, C. & Dreher, T.W. The TYMV tRNA-like structure. Biochimie 75, 569−582 (1993). | Article | PubMed | ISI |
  6. Matthews, R.E.F. Plant Virology 231−237 (Academic Press, Inc., New York; 1991).
  7. Mutombo, K., Michels, B., Ott, H., Cerf, R. & Witz, J. The thermal stability and decapsidation mechanism of tymoviruses: A differential calorimetric study. Biochimie 75, 667−674 (1993). | Article | PubMed | ISI | ChemPort |
  8. Klug, A., Longley, W. & Leberman, R. Arrangement of protein subunits and the distribution of nucleic acid in turnip yellow mosiac virus. I. X-ray diffraction studies. J. mol. Biol. 15, 315−343 (1966). | PubMed | ISI | ChemPort |
  9. Finch, J.T. & Klug, A. Arrangement of protein subunits and the distribution of nucleic acid in turnip yellow mosaic virus. II. Electron microscopic studies. J. Mol. Biol. 15, 344−64 (1966). | PubMed | ISI | ChemPort |
  10. Jacrot, B., Chauvin, C. & Witz, J. Comparative neutron small-angle scattering study of small spherical RNA Viruses. Nature 266, 417−421 (1977). | PubMed | ISI | ChemPort |
  11. Rubio-Huertos, M., Vela, A. & Lopez-Abella, D. Crystalline arrays of spherical particles in turnip yellow mosaic virus-infected cells. Virology 32, 438−444 (1967). | PubMed | ChemPort |
  12. Markham, R. & Smith, K.M. Studies on the virus of turnip yellow mosaic. Parasitology 39, 330−343 (1949). | ISI | ChemPort |
  13. Chapman, M.S. & Rossmann, M.G. Comparison of surface properties of picornaviruses: Strategies for hiding the receptor site from immune surveillance. Virology 195, 745−756 (1993). | Article | PubMed | ISI | ChemPort |
  14. Mellema, J.E. & Amos, L.A. Three-dimensional image reconstruction of turnip yellow mosaic virus. J. Mol. Biol. 72, 819−822 (1972). | PubMed | ISI | ChemPort |
  15. Speir, J.A., Munshi, S., Wang, G., Baker, T.S. & Johnson, J.E. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 3, 63−78 (1995). | PubMed | ISI | ChemPort |
  16. Sheriff, S., Hendrickson, W.A. & Smith, J.L. Structure of myohemerythrin in the azidomet state at 1.7/1.3 Å resolution. J. Mol. Biol. 197, 273−296 (1987). | PubMed | ISI | ChemPort |
  17. Kaper, J.M. The Chemical basis of virus structure, dissociation, and assembly (North-Holland Publishing Company, Amsterdam; 1975).
  18. Peter, R., Stehelin, D., Reinbolt, J., Collot, D. & Duranton, H. Primary structure of turnip yellow mosaic virus coat protein. Virology 49, 615−617 (1972). | PubMed | ISI | ChemPort |
  19. Chelvanayagam, G., Heringa, J. & Argos, P. Anatomy and evolution of proteins displaying the viral capsid jellyroll topology. J. Mol. Biol. 228 220−242 (1992). | PubMed | ISI | ChemPort |
  20. Nicholls, A., Sharp, K. & Honig, B. Protein folding and association—insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281−296 (1991). | PubMed | ISI | ChemPort |
  21. Witz, J., Timmins, P.A. & Adrian, M. Organization of turnip yellow mosaic virus investigated by neutron small angle scattering at 80 K: An intermediate state preceding decapsidation of the virion? Proteins 17, 223−231 (1993). | PubMed | ISI | ChemPort |
  22. Pleij, C.W., Eecen, H.G., Bosch, L. & Mandel, M. The formation of fast-sedimenting turnip yellow mosaic virus RNA: Structural rearrangement inside the capsid. Virology 76, 781−786 (1977). | Article | PubMed | ISI | ChemPort |
  23. Virudachalam, R., Low, P.S., Argos, P. & Markley, J.L. Turnip yellow mosaic virus and its capsid have thermal stabilities with opposite pH dependence: Studies by differential scanning calorimetry and 31P nuclear magnetic resonance spectroscopy. Virology 146, 213−220 (1985). | Article | PubMed | ISI | ChemPort |
  24. Rohozinski, J. & Hancock, J.M. Do light-induced pH changes within the chloroplast drive turnip yellow mosaic virus assembly? J. Gen. Virol. 77, 163−165 (1996). | PubMed | ISI | ChemPort |
  25. Matthews, R.E.F. & Witz, J. Uncoating of turnip yellow mosaic virus RNA in vivo. Virology 144, 318−327 (1985). | Article | ISI | ChemPort |
  26. Adrian, M., Timmins, P.A. & Witz, J. In vitro decapsidation of turnip yellow mosaic virus investigated by cryo-electron microscopy: a model for the decapsidation of a small isometric virus. J. Gen. Virol. 73, 2079−2083 (1992). | PubMed | ISI | ChemPort |
  27. Keeling, J. & Matthews, R.E.F. Mechanism for release of RNA from turnip yellow mosaic virus at high pH. Virology 119, 214−218 (1982). | Article | ISI | ChemPort |
  28. Katouzian-Safadi, M. & Berthet-Colominas, C. Evidence for the presence of a hole in the capsid of turnip yellow mosaic virus after RNA release by freezing and thawing. Eur. J. Biochem. 137, 47−55 (1983). | PubMed | ChemPort |
  29. Quesniaux, V., Jaegle, M. & Van Regenmortel, M.H.V. Immunochemical studies of turnip yellow mosaic virus III. Localization of two viral epitopes in residues 57−64 and 183−189 of the coat protein. Bioch. et Bioph. Acta 743, 226−231 (1983). | Article | ISI | ChemPort |
  30. Quesniaux, V., Briand, J.P. & Van Regenmortel, M.H.V. Immunochemical studies of turnip yellow mosaic virus—II. Localization of a viral epitope in the N-terminal residues of the coat protein. Molec. Immun. 20, 179−185 (1983). | Article | PubMed | ISI | ChemPort |
  31. Roivainen, M., Piirainen, L., Rysä, T., Närvänen, A. & Hovi, T. An immunodominant N-terminal region of VP1 protein of poliovirion that is buried in crystal structure can be exposed in solution. Virology 195, 762−765 (1993). | Article | PubMed | ISI | ChemPort |
  32. Yafal, A.G., Kaplan, G., Racaniello, V.R. & Hogle, J.M. Characterization of poliovirus conformational alteration mediated by soluble cell receptors. Virology 197, 501−515 (1993). | Article | PubMed | ISI |
  33. Cheng, R.H. et al. Functional implications of quasi-equivalence in a T=3 icosahedral animal virus established by cryo-electron microscopy and X-ray crystallography. Structure 2, 271−282 (1994). | PubMed | ISI | ChemPort |
  34. Tsao, J. et al. & Parrish, C.R. Three dimensional structure of canine parvovirus and its functional implications. Science 251, 1456−1464 (1991). | PubMed | ISI | ChemPort |
  35. Langeveld, J.P.M. et al. B-cell epitopes of canine parvovirus: Distribution on the primary structure and exposure on the viral surface. J. Virol. 68, 4506−4513 (1994). | PubMed | ISI | ChemPort |
  36. Ehresmann, B., Briand, J.P., Reinbolt, J. & Witz, J. Identification of binding sites of turnip yellow mosaic virus protein and RNA induced in situ. Eur. J. Biochem. 108, 123−129 (1980). | PubMed | ISI | ChemPort |
  37. Chen, Z. et al. & Johnson, J.E. Protein-RNA interactions in an icosahedral virus at 3.0 Å resolution. Science 245, 154−159 (1989). | PubMed | ISI | ChemPort |
  38. Larson, S.B. et al. Double helical RNA in satellite tobacco mosaic virus. Nature 361, 179−182 (1993). | Article | PubMed | ISI | ChemPort |
  39. Fisher, A.J. & Johnson, J.E. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature 361, 176−179 (1993). | Article | PubMed | ISI | ChemPort |
  40. Wery, J.P., Reddy, V.S., Hosur, M.V. & Johnson, J.E. The refined three-dimensional structure of an insect virus at 2.8 Å resolution. J. mol. Biol. 235, 565−586 (1994). | Article | PubMed | ISI | ChemPort |
  41. Bottcher, B. & Crowther, R.A. Difference imaging reveals ordered regions of RNA in turnip yellow mosaic virus. Structure 4, 387−394 (1996). | PubMed | ISI | ChemPort |
  42. Hanna, M. & Szostak, J.W. Suppression of mutations in the core of the Tetrahymena ribozyme by spermidine, ethanol and by substrate stabilization. Nuc. Acids Res. 22, 5326−5331 (1994). | ISI | ChemPort |
  43. Canady, M.A., Day, J. & McPherson, A. Preliminary X-ray diffraction analysis of crystals of turnip yellow mosaic virus (TYMV). Proteins 21, 78−81 (1995). | PubMed | ISI | ChemPort |
  44. McPherson, A. The growth and preliminary investigation of protein and nucleic acid crystals for X-ray diffraction. In Methods of Biochemical analysis (ed. D. Glick) 249−345 (John Wiley & Sons, New York, 1976). | ChemPort |
  45. Otwinowski, Z.. Oscillation Data Reduction program. In Proceedings of the CCP4 Study Weekend: Data Collection and Processing, 29−30 January, (L. Sawyer, N. Isaacs & S. Bailey, compl.) 56−62 (SERC Daresbury Laboratory, England, 1993).
  46. Minor, W. XDISPLAYF Program (Purdue University, West Lafayette, Indiana, 1993).
  47. Brünger, A.T. X-PLOR Version 3.1. A system for X-ray Crystallography and NMR (Yale University Press, New Haven, 1992).
  48. Larson, S.B. et al. Three dimensional structure of satellite tobacco mosaic virus at 2.9 Å resolution. J. Mol. Biol. 21, 375−391 (1993). | Article |
  49. Bricogne, G. Methods and programs for direct-space exploitation of geometrical redundancies. Acta Crystallogr. A 32, 832−846 (1976). | Article | ISI |
  50. Furey, W. Abstract, American Crystallographic Association, Series 2 (18) 73 (1990).
  51. Jones, A.T. & Kjeldgaard, M. "O" Manual, version 5.4 (Uppsala University, Sweden and Aarhus University, Denmark, 1990).
  52. Kraulis, P.J. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. appl. Cryst. 24, 946−950 (1991). | Article | ISI |
  53. Evans, S.V. SETOR: hardware lighted three-dimensional solid model representations of macromolecules. J. Molec. Graphics 11, 134−138 (1993). | Article | ISI | ChemPort |
  54. Laskowski, R.A., Macarthur, M.W., Moss, D.S. & Thornton, J.M. Procheck—A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283−291 (1993). | Article | ISI | ChemPort |
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