Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1981 Jul;78(7):4231–4235. doi: 10.1073/pnas.78.7.4231

Correlation between particle multiplicity and location on virion RNA of the assembly initiation site for viruses of the tobacco mosaic virus group

Megumi Fukuda *, Tetsuo Meshi *, Yoshimi Okada *, Yoshiaki Otsuki †, Itaru Takebe ‡
PMCID: PMC319763  PMID: 16593057

Abstract

The initiation site for reconstitution on genome RNA was determined by electron microscopic serology for a watermelon strain of cucumber green mottle mosaic virus (CGMMV-W), which is chemically and serologically related to tobacco mosaic virus (TMV). The initiation site was located at the same position as that of the cowpea strain, a virus that produces short rods of encapsidated subgenomic messenger RNA for the coat protein (a two-component TMV), being about 320 nucleotides away from the 3′ terminus, and hence within the coat protein cistron. Although CGMMV-W was until now believed to be a single-component TMV, the location of the initiation site indicated the presence of short rods containing coat protein messenger RNA in CGMMV-W-infected tissue, as in the case for the cowpea strain. We found such short rods in CGMMV-W-infected tissue. The results confirmed our previous hypothesis that the site of the initiation region for reconstitution determines the rod multiplicity of TMV. The finding of the second two-component TMV, CGMMV, indicates that the cowpea strain of TMV is not unique in being a two-component virus and that the location of the assembly initiation site on the genome RNA can be a criterion for grouping of viruses.

Keywords: cucumber green mottle mosaic virus, virus encapsidation

Full text

PDF
4231

Images in this article

4232Image
on p.4232
4234Image
on p.4234
4234Image
on p.4234

Selected References

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

  1. Anderer F. A., Wittmann-Liebold B., Wittmann H. G. Weitere Untersuchungen zur Aminosäuresequenz des Proteins im Tabakmosaikvirus. Z Naturforsch B. 1965 Dec;20(12):1203–1213. [PubMed] [Google Scholar]
  2. Bruening G., Beachy R. N., Scalla R., Zaitlin M. In vitro and in vivo translation of the ribonucleic acids of a cowpea strain of tobacco mosaic virus. Virology. 1976 Jun;71(2):498–517. doi: 10.1016/0042-6822(76)90377-9. [DOI] [PubMed] [Google Scholar]
  3. Butler P. J., Klug A. Assembly of the particle of tobacco mosaic virus from RNA and disks of protein. Nat New Biol. 1971 Jan 13;229(2):47–50. doi: 10.1038/newbio229047a0. [DOI] [PubMed] [Google Scholar]
  4. Chamberlain J. P. Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate. Anal Biochem. 1979 Sep 15;98(1):132–135. doi: 10.1016/0003-2697(79)90716-4. [DOI] [PubMed] [Google Scholar]
  5. FRAENKEL-CONRAT H. Degradation of tobacco mosaic virus with acetic acid. Virology. 1957 Aug;4(1):1–4. doi: 10.1016/0042-6822(57)90038-7. [DOI] [PubMed] [Google Scholar]
  6. FRAENKEL-CONRAT H., SINGER B., TSUGITA A. Purification of viral RNA by means of bentonite. Virology. 1961 May;14:54–58. doi: 10.1016/0042-6822(61)90131-3. [DOI] [PubMed] [Google Scholar]
  7. Fraenkel-Conrat H., Williams R. C. RECONSTITUTION OF ACTIVE TOBACCO MOSAIC VIRUS FROM ITS INACTIVE PROTEIN AND NUCLEIC ACID COMPONENTS. Proc Natl Acad Sci U S A. 1955 Oct 15;41(10):690–698. doi: 10.1073/pnas.41.10.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fukuda M., Ohno T., Okada Y., Otsuki Y., Takebe I. Kinetics of biphasic reconstitution of tobacco mosaic virus in vitro. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1727–1730. doi: 10.1073/pnas.75.4.1727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Graham J., Butler P. J. Binding of oligonucleotides to the disk of tobacco-mosaic-virus protein. Eur J Biochem. 1979 Jan 15;93(2):333–337. doi: 10.1111/j.1432-1033.1979.tb12827.x. [DOI] [PubMed] [Google Scholar]
  10. Guilley H., Jonard G., Kukla B., Richards K. E. Sequence of 1000 nucleotides at the 3' end of tobacco mosaic virus RNA. Nucleic Acids Res. 1979 Apr;6(4):1287–1308. doi: 10.1093/nar/6.4.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guilley H., Jonard G., Richards K. E., Hirth L. Observations concerning the sequence of two additional specifically encapsidated RNA fragments originating from the tobacco-mosaic-virus coat-protein cistron. Eur J Biochem. 1975 May;54(1):145–153. doi: 10.1111/j.1432-1033.1975.tb04123.x. [DOI] [PubMed] [Google Scholar]
  12. Guilley H., Jonard G., Richards K. E., Hirth L. Sequence of a specifically encapsidated RNA fragment originating from the tobacco-mosaic-virus coat-protein cistron. Eur J Biochem. 1975 May;54(1):135–144. doi: 10.1111/j.1432-1033.1975.tb04122.x. [DOI] [PubMed] [Google Scholar]
  13. Higgins T. J., Goodwin P. B., Whitfeld P. R. Occurrence of short particles in beans infected with the cowpea strain of TMV. II. Evidence that short particles contain the cistron for coat-protein. Virology. 1976 Jun;71(2):486–497. doi: 10.1016/0042-6822(76)90376-7. [DOI] [PubMed] [Google Scholar]
  14. Hunter T. R., Hunt T., Knowland J., Zimmern D. Messenger RNA for the coat protein of tobacco mosaic virus. Nature. 1976 Apr 29;260(5554):759–764. doi: 10.1038/260759a0. [DOI] [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  17. Lebeurier G., Nicolaieff A., Richards K. E. Inside-out model for self-assembly of tobacco mosaic virus. Proc Natl Acad Sci U S A. 1977 Jan;74(1):149–153. doi: 10.1073/pnas.74.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Marcu K., Dudock B. Characterization of a highly efficient protein synthesizing system derived from commercial wheat germ. Nucleic Acids Res. 1974 Nov;1(11):1385–1397. doi: 10.1093/nar/1.11.1385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nozu Y., Okada Y. Amino acid sequence of a common Japanese strain of tobacco mosaic virus. J Mol Biol. 1968 Aug 14;35(3):643–646. doi: 10.1016/s0022-2836(68)80021-x. [DOI] [PubMed] [Google Scholar]
  20. Nozu Y., Tochihara H., Komuro Y., Okada Y. Chemical and immunological characterization of cucumber green mottle mosaic virus (watermelon strain) protein. Virology. 1971 Sep;45(3):577–585. doi: 10.1016/0042-6822(71)90173-5. [DOI] [PubMed] [Google Scholar]
  21. Ohno T., Sumita M., Okada Y. Location of the initiation site on tobacco mosaic virus RNA involved in assembly of the virus in vitro. Virology. 1977 May 15;78(2):407–414. doi: 10.1016/0042-6822(77)90117-9. [DOI] [PubMed] [Google Scholar]
  22. Ono T., Nozu Y., Okada Y. Polar reconstitution of tobacco mosaic virus (TMV). Virology. 1971 Jun;44(3):510–516. doi: 10.1016/0042-6822(71)90364-3. [DOI] [PubMed] [Google Scholar]
  23. Otsuki Y., Takebe I. Fluorescent antibody staining of tobacco mosaic virus antigen in tobacco mesophyll protoplasts. Virology. 1969 Jul;38(3):497–499. doi: 10.1016/0042-6822(69)90167-6. [DOI] [PubMed] [Google Scholar]
  24. Otsuki Y., Takebe I., Ohno T., Fukuda M., Okada Y. Reconstitution of tobacco mosaic virus rods occurs bidirectionally from an internal initiation region: demonstration by electron microscopic serology. Proc Natl Acad Sci U S A. 1977 May;74(5):1913–1917. doi: 10.1073/pnas.74.5.1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rees M. W., Short M. N. The amino acid sequence of the cowpea strain of tobacco mosaic virus protein. Biochim Biophys Acta. 1975 May 30;393(1):15–23. doi: 10.1016/0005-2795(75)90211-1. [DOI] [PubMed] [Google Scholar]
  26. Richards K. E., Williams R. C. Assembly of tobacco mosaic virus in vitro: effect of state of polymerization of the protein component. Proc Natl Acad Sci U S A. 1972 May;69(5):1121–1124. doi: 10.1073/pnas.69.5.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Siegel A., Hari V., Montgomery I., Kolacz K. A messenger RNA for capsid protein isolated from tobacco mosaic virus-infected tissue. Virology. 1976 Sep;73(2):363–371. doi: 10.1016/0042-6822(76)90397-4. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Studier F. W. Analysis of bacteriophage T7 early RNAs and proteins on slab gels. J Mol Biol. 1973 Sep 15;79(2):237–248. doi: 10.1016/0022-2836(73)90003-x. [DOI] [PubMed] [Google Scholar]
  30. Thouvenel J. -C., Guilley H., Stussi C., Hirth L. Evidence for polar reconstitution of TMV. FEBS Lett. 1971 Aug 15;16(3):204–206. doi: 10.1016/0014-5793(71)80134-5. [DOI] [PubMed] [Google Scholar]
  31. Whitfeld P. R., Higgins T. J. Occurrence of short particles in beans infected with the cowpea strain of TMV. I. Purification and characterization of short particles. Virology. 1976 Jun;71(2):471–485. doi: 10.1016/0042-6822(76)90375-5. [DOI] [PubMed] [Google Scholar]
  32. Wittmann H. G. Die primäre Proteinstruktur von Stämmen des Tabakmosaikvirus. IV: Aminosäuresequenzen (1 bis 61 und 135 bis 158) des Proteins des Tabakmosaikvirus-Stammes U2. Z Naturforsch B. 1965 Dec;20(12):1213–1223. [PubMed] [Google Scholar]
  33. Wittmann H. G., Hindennach I., Wittmann-Liebold B. Die primäre Proteinstruktur von Stämmen des Tabakmosaikvirus. VI. Aminosäurensequenz (Positionen 62-156) des Proteins des Tabakmosaikvirusstammes Holmes rib grass. Z Naturforsch B. 1969 Jul;24(7):877–885. [PubMed] [Google Scholar]
  34. 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 Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES