Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1999 Mar 29;354(1383):551–557. doi: 10.1098/rstb.1999.0406

Tobacco mosaic virus particle structure and the initiation of disassembly.

G Stubbs 1
PMCID: PMC1692545  PMID: 10212934

Abstract

The structure of an intact tobacco mosaic virus (TMV) particle was determined at 2.9 A resolution using fibre diffraction methods. All residues of the coat protein and the three nucleotides of RNA that are bound to each protein subunit were visible in the electron density map. Examination of the structures of TMV, cucumber green mottle mosaic virus and ribgrass mosaic virus, and site-directed mutagenesis experiments in which carboxylate groups were changed to the corresponding amides, showed that initial stages of disassembly are driven by complex electrostatic interactions involving at least seven carboxylate side-chains and a phosphate group. The locations of these interactions can drift during evolution, allowing the viruses to evade plant defensive responses that depend on recognition of the viral coat protein surface.

Full Text

The Full Text of this article is available as a PDF (242.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barrett A. N., Leigh J. B., Holmes K. C., Leberman R., Mandelkow E., von Sengbusch P. An electron-density map of tobacco mosaic virus at 10 Angstrom resolution. Cold Spring Harb Symp Quant Biol. 1972;36:433–448. doi: 10.1101/sqb.1972.036.01.056. [DOI] [PubMed] [Google Scholar]
  2. Butler P. J., Durham A. C. Structures and roles of the polymorphic forms of tobacco mosaic virus. V. Conservation of the abnormally titrating groups in tobacco mosaic virus. J Mol Biol. 1972 Dec 14;72(1):19–24. doi: 10.1016/0022-2836(72)90064-2. [DOI] [PubMed] [Google Scholar]
  3. CASPAR D. L. ASSEMBLY AND STABILITY OF THE TOBACCO MOSAIC VIRUS PARTICLE. Adv Protein Chem. 1963;18:37–121. doi: 10.1016/s0065-3233(08)60268-5. [DOI] [PubMed] [Google Scholar]
  4. Culver J. N., Dawson W. O., Plonk K., Stubbs G. Site-directed mutagenesis confirms the involvement of carboxylate groups in the disassembly of tobacco mosaic virus. Virology. 1995 Jan 10;206(1):724–730. doi: 10.1016/s0042-6822(95)80096-4. [DOI] [PubMed] [Google Scholar]
  5. Culver J. N., Stubbs G., Dawson W. O. Structure-function relationship between tobacco mosaic virus coat protein and hypersensitivity in Nicotiana sylvestris. J Mol Biol. 1994 Sep 16;242(2):130–138. doi: 10.1006/jmbi.1994.1564. [DOI] [PubMed] [Google Scholar]
  6. FRASER R. D. B. Infra-red dichroism of tobacco mosaic virus nucleoprotein. Nature. 1952 Sep 20;170(4325):491–491. doi: 10.1038/170491a0. [DOI] [PubMed] [Google Scholar]
  7. Gallagher W. H., Lauffer M. A. Calcium ion binding by tobacco mosaic virus. J Mol Biol. 1983 Nov 15;170(4):905–919. doi: 10.1016/s0022-2836(83)80194-6. [DOI] [PubMed] [Google Scholar]
  8. Goelet P., Lomonossoff G. P., Butler P. J., Akam M. E., Gait M. J., Karn J. Nucleotide sequence of tobacco mosaic virus RNA. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5818–5822. doi: 10.1073/pnas.79.19.5818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Holmes K. C., Stubbs G. J., Mandelkow E., Gallwitz U. Structure of tobacco mosaic virus at 6.7 å resolution. Nature. 1975 Mar 20;254(5497):192–196. doi: 10.1038/254192a0. [DOI] [PubMed] [Google Scholar]
  10. Lobert S., Stubbs G. Fiber diffraction analysis of cucumber green mottle mosaic virus using limited numbers of heavy-atom derivatives. Acta Crystallogr A. 1990 Dec 1;46(Pt 12):993–997. doi: 10.1107/s0108767390008844. [DOI] [PubMed] [Google Scholar]
  11. Lu B., Stubbs G., Culver J. N. Carboxylate interactions involved in the disassembly of tobacco mosaic tobamovirus. Virology. 1996 Nov 1;225(1):11–20. doi: 10.1006/viro.1996.0570. [DOI] [PubMed] [Google Scholar]
  12. Mundry K. W., Watkins P. A., Ashfield T., Plaskitt K. A., Eisele-Walter S., Wilson T. M. Complete uncoating of the 5' leader sequence of tobacco mosaic virus RNA occurs rapidly and is required to initiate cotranslational virus disassembly in vitro. J Gen Virol. 1991 Apr;72(Pt 4):769–777. doi: 10.1099/0022-1317-72-4-769. [DOI] [PubMed] [Google Scholar]
  13. Namba K., Caspar D. L., Stubbs G. J. Computer graphics representation of levels of organization in tobacco mosaic virus structure. Science. 1985 Feb 15;227(4688):773–776. doi: 10.1126/science.3994790. [DOI] [PubMed] [Google Scholar]
  14. Namba K., Pattanayek R., Stubbs G. Visualization of protein-nucleic acid interactions in a virus. Refined structure of intact tobacco mosaic virus at 2.9 A resolution by X-ray fiber diffraction. J Mol Biol. 1989 Jul 20;208(2):307–325. doi: 10.1016/0022-2836(89)90391-4. [DOI] [PubMed] [Google Scholar]
  15. Namba K., Stubbs G. Structure of tobacco mosaic virus at 3.6 A resolution: implications for assembly. Science. 1986 Mar 21;231(4744):1401–1406. doi: 10.1126/science.3952490. [DOI] [PubMed] [Google Scholar]
  16. PAULING L., COREY R. B., BRANSON H. R. The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci U S A. 1951 Apr;37(4):205–211. doi: 10.1073/pnas.37.4.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pattanayek R., Stubbs G. Structure of the U2 strain of tobacco mosaic virus refined at 3.5 A resolution using X-ray fiber diffraction. J Mol Biol. 1992 Nov 20;228(2):516–528. doi: 10.1016/0022-2836(92)90839-c. [DOI] [PubMed] [Google Scholar]
  18. Stubbs G., Namba K., Makowski L. Application of restrained least-squares refinement to fiber diffraction from macromolecular assemblies. Biophys J. 1986 Jan;49(1):58–60. doi: 10.1016/S0006-3495(86)83592-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Stubbs G., Stauffacher C. Structure of the RNA in tobacco mosaic virus. J Mol Biol. 1981 Oct 25;152(2):387–396. doi: 10.1016/0022-2836(81)90249-7. [DOI] [PubMed] [Google Scholar]
  20. Stubbs G. The probability distributions of X-ray intensities in fiber diffraction: largest likely values for fiber diffraction R factors. Acta Crystallogr A. 1989 Mar 1;45(Pt 3):254–258. doi: 10.1107/s0108767388010864. [DOI] [PubMed] [Google Scholar]
  21. Stubbs G., Warren S., Holmes K. Structure of RNA and RNA binding site in tobacco mosaic virus from 4-A map calculated from X-ray fibre diagrams. Nature. 1977 May 19;267(5608):216–221. doi: 10.1038/267216a0. [DOI] [PubMed] [Google Scholar]
  22. WATSON J. D. The structure of tobacco mosaic virus. I. X-ray evidence of a helical arrangement of sub-units around the longitudinal axis. Biochim Biophys Acta. 1954 Jan;13(1):10–19. doi: 10.1016/0006-3002(54)90265-6. [DOI] [PubMed] [Google Scholar]
  23. Wang H., Culver J. N., Stubbs G. Structure of ribgrass mosaic virus at 2.9 A resolution: evolution and taxonomy of tobamoviruses. J Mol Biol. 1997 Jun 27;269(5):769–779. doi: 10.1006/jmbi.1997.1048. [DOI] [PubMed] [Google Scholar]
  24. Wang H., Planchart A., Stubbs G. Caspar carboxylates: the structural basis of tobamovirus disassembly. Biophys J. 1998 Jan;74(1):633–638. doi: 10.1016/S0006-3495(98)77822-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wang H., Stubbs G. Molecular dynamics in refinement against fiber diffraction data. Acta Crystallogr A. 1993 May 1;49(3):504–513. doi: 10.1107/s0108767392011255. [DOI] [PubMed] [Google Scholar]
  26. Wang H., Stubbs G. Structure determination of cucumber green mottle mosaic virus by X-ray fiber diffraction. Significance for the evolution of tobamoviruses. J Mol Biol. 1994 Jun 10;239(3):371–384. doi: 10.1006/jmbi.1994.1379. [DOI] [PubMed] [Google Scholar]
  27. Zimmern D. The nucleotide sequence at the origin for assembly on tobacco mosaic virus RNA. Cell. 1977 Jul;11(3):463–482. doi: 10.1016/0092-8674(77)90065-4. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES