Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1997 Mar;71(3):2270–2276. doi: 10.1128/jvi.71.3.2270-2276.1997

Deletion of the C-terminal 33 amino acids of cucumber mosaic virus movement protein enables a chimeric brome mosaic virus to move from cell to cell.

H Nagano 1, T Okuno 1, K Mise 1, I Furusawa 1
PMCID: PMC191335  PMID: 9032362

Abstract

The movement protein (MP) gene of brome mosaic virus (BMV) was precisely replaced with that of cucumber mosaic virus (CMV). Infectivity tests of the chimeric BMV on Chenopodium quinoa, a permissive host for cell-to-cell movement of both BMV and CMV, showed that the chimeric BMV failed to move from cell to cell even though it replicated in protoplasts. A spontaneous mutant of the chimeric BMV that displayed cell-to-cell movement was subsequently obtained from a local lesion during one of the experiments. A cloned cDNA representing the genomic RNA encoding the MP of the chimeric BMV mutant was analyzed and found to contain a mutation in the CMV MP gene resulting in deletion of the C-terminal 33 amino acids of the MP. Directed mutagenesis of the CMV MP gene showed that the C-terminal deletion was responsible for the movement capability of the mutant. When the mutation was introduced into CMV, the CMV mutant moved from cell to cell in C. quinoa, though the movement was less efficient than that of the wild-type CMV. These results indicate that the CMV MP, except the C-terminal 33 amino acids, potentiates cell-to-cell movement of both BMV and CMV in C. quinoa. In addition, since C. quinoa is a common host for both BMV and CMV, these results suggest that the CMV MP has specificity for the viral genomes during cell-to-cell movement of the virus and that the C-terminal 33 amino acids of the CMV MP are involved in that specificity.

Full Text

The Full Text of this article is available as a PDF (512.6 KB).

Selected References

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

  1. Allison R., Thompson C., Ahlquist P. Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1820–1824. doi: 10.1073/pnas.87.5.1820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Atabekov J. G., Taliansky M. E. Expression of a plant virus-coded transport function by different viral genomes. Adv Virus Res. 1990;38:201–248. doi: 10.1016/s0065-3527(08)60863-5. [DOI] [PubMed] [Google Scholar]
  3. Boccard F., Baulcombe D. Mutational analysis of cis-acting sequences and gene function in RNA3 of cucumber mosaic virus. Virology. 1993 Apr;193(2):563–578. doi: 10.1006/viro.1993.1165. [DOI] [PubMed] [Google Scholar]
  4. Citovsky V. Probing Plasmodesmal Transport with Plant Viruses. Plant Physiol. 1993 Aug;102(4):1071–1076. doi: 10.1104/pp.102.4.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cooper B., Dodds J. A. Differences in the subcellular localization of tobacco mosaic virus and cucumber mosaic virus movement proteins in infected and transgenic plants. J Gen Virol. 1995 Dec;76(Pt 12):3217–3221. doi: 10.1099/0022-1317-76-12-3217. [DOI] [PubMed] [Google Scholar]
  6. Cooper B., Schmitz I., Rao A. L., Beachy R. N., Dodds J. A. Cell-to-cell transport of movement-defective cucumber mosaic and tobacco mosaic viruses in transgenic plants expressing heterologous movement protein genes. Virology. 1996 Feb 1;216(1):208–213. doi: 10.1006/viro.1996.0048. [DOI] [PubMed] [Google Scholar]
  7. Davies C., Symons R. H. Further implications for the evolutionary relationships between tripartite plant viruses based on cucumber mosaic virus RNA 3. Virology. 1988 Jul;165(1):216–224. doi: 10.1016/0042-6822(88)90675-7. [DOI] [PubMed] [Google Scholar]
  8. De Jong W., Ahlquist P. A hybrid plant RNA virus made by transferring the noncapsid movement protein from a rod-shaped to an icosahedral virus is competent for systemic infection. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6808–6812. doi: 10.1073/pnas.89.15.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. De Jong W., Chu A., Ahlquist P. Coding changes in the 3a cell-to-cell movement gene can extend the host range of brome mosaic virus systemic infection. Virology. 1995 Dec 20;214(2):464–474. doi: 10.1006/viro.1995.0057. [DOI] [PubMed] [Google Scholar]
  10. Deom C. M., He X. Z., Beachy R. N., Weissinger A. K. Influence of heterologous tobamovirus movement protein and chimeric-movement protein genes on cell-to-cell and long-distance movement. Virology. 1994 Nov 15;205(1):198–209. doi: 10.1006/viro.1994.1635. [DOI] [PubMed] [Google Scholar]
  11. Deom C. M., Lapidot M., Beachy R. N. Plant virus movement proteins. Cell. 1992 Apr 17;69(2):221–224. doi: 10.1016/0092-8674(92)90403-y. [DOI] [PubMed] [Google Scholar]
  12. Ding B., Li Q., Nguyen L., Palukaitis P., Lucas W. J. Cucumber mosaic virus 3a protein potentiates cell-to-cell trafficking of CMV RNA in tobacco plants. Virology. 1995 Mar 10;207(2):345–353. doi: 10.1006/viro.1995.1093. [DOI] [PubMed] [Google Scholar]
  13. Ding S. W., Anderson B. J., Haase H. R., Symons R. H. New overlapping gene encoded by the cucumber mosaic virus genome. Virology. 1994 Feb;198(2):593–601. doi: 10.1006/viro.1994.1071. [DOI] [PubMed] [Google Scholar]
  14. Ding S. W., Li W. X., Symons R. H. A novel naturally occurring hybrid gene encoded by a plant RNA virus facilitates long distance virus movement. EMBO J. 1995 Dec 1;14(23):5762–5772. doi: 10.1002/j.1460-2075.1995.tb00265.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fujita Y., Mise K., Okuno T., Ahlquist P., Furusawa I. A single codon change in a conserved motif of a bromovirus movement protein gene confers compatibility with a new host. Virology. 1996 Sep 15;223(2):283–291. doi: 10.1006/viro.1996.0480. [DOI] [PubMed] [Google Scholar]
  16. Gal-On A., Kaplan I., Roossinck M. J., Palukaitis P. The kinetics of infection of zucchini squash by cucumber mosaic virus indicate a function for RNA 1 in virus movement. Virology. 1994 Nov 15;205(1):280–289. doi: 10.1006/viro.1994.1644. [DOI] [PubMed] [Google Scholar]
  17. Giesman-Cookmeyer D., Silver S., Vaewhongs A. A., Lommel S. A., Deom C. M. Tobamovirus and dianthovirus movement proteins are functionally homologous. Virology. 1995 Oct 20;213(1):38–45. doi: 10.1006/viro.1995.1544. [DOI] [PubMed] [Google Scholar]
  18. Ito W., Ishiguro H., Kurosawa Y. A general method for introducing a series of mutations into cloned DNA using the polymerase chain reaction. Gene. 1991 Jun 15;102(1):67–70. doi: 10.1016/0378-1119(91)90539-n. [DOI] [PubMed] [Google Scholar]
  19. Kaido M., Mori M., Mise K., Okuno T., Furusawa I. Inhibition of brome mosaic virus (BMV) amplification in protoplasts from transgenic tobacco plants expressing replicable BMV RNAs. J Gen Virol. 1995 Nov;76(Pt 11):2827–2833. doi: 10.1099/0022-1317-76-11-2827. [DOI] [PubMed] [Google Scholar]
  20. Kaplan I. B., Shintaku M. H., Li Q., Zhang L., Marsh L. E., Palukaitis P. Complementation of virus movement in transgenic tobacco expressing the cucumber mosaic virus 3a gene. Virology. 1995 May 10;209(1):188–199. doi: 10.1006/viro.1995.1242. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Li Q., Palukaitis P. Comparison of the nucleic acid- and NTP-binding properties of the movement protein of cucumber mosaic cucumovirus and tobacco mosaic tobamovirus. Virology. 1996 Feb 1;216(1):71–79. doi: 10.1006/viro.1996.0035. [DOI] [PubMed] [Google Scholar]
  23. Melcher U. Similarities between putative transport proteins of plant viruses. J Gen Virol. 1990 May;71(Pt 5):1009–1018. doi: 10.1099/0022-1317-71-5-1009. [DOI] [PubMed] [Google Scholar]
  24. Mise K., Allison R. F., Janda M., Ahlquist P. Bromovirus movement protein genes play a crucial role in host specificity. J Virol. 1993 May;67(5):2815–2823. doi: 10.1128/jvi.67.5.2815-2823.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mise K., Tsuge S., Nagao K., Okuno T., Furusawa I. Nucleotide sequence responsible for the synthesis of a truncated coat protein of brome mosaic virus strain ATCC66. J Gen Virol. 1992 Oct;73(Pt 10):2543–2551. doi: 10.1099/0022-1317-73-10-2543. [DOI] [PubMed] [Google Scholar]
  26. Mori M., Mise K., Kobayashi K., Okuno T., Furusawa I. Infectivity of plasmids containing brome mosaic virus cDNA linked to the cauliflower mosaic virus 35S RNA promoter. J Gen Virol. 1991 Feb;72(Pt 2):243–246. doi: 10.1099/0022-1317-72-2-243. [DOI] [PubMed] [Google Scholar]
  27. Mori M., Zhang G. H., Kaido M., Okuno T., Furusawa I. Efficient production of human gamma interferon in tobacco protoplasts by genetically engineered brome mosaic virus RNAs. J Gen Virol. 1993 Jul;74(Pt 7):1255–1260. doi: 10.1099/0022-1317-74-7-1255. [DOI] [PubMed] [Google Scholar]
  28. Mushegian A. R., Koonin E. V. Cell-to-cell movement of plant viruses. Insights from amino acid sequence comparisons of movement proteins and from analogies with cellular transport systems. Arch Virol. 1993;133(3-4):239–257. doi: 10.1007/BF01313766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nejidat A., Cellier F., Holt C. A., Gafny R., Eggenberger A. L., Beachy R. N. Transfer of the movement protein gene between two tobamoviruses: influence on local lesion development. Virology. 1991 Jan;180(1):318–326. doi: 10.1016/0042-6822(91)90036-b. [DOI] [PubMed] [Google Scholar]
  30. Palukaitis P., Roossinck M. J., Dietzgen R. G., Francki R. I. Cucumber mosaic virus. Adv Virus Res. 1992;41:281–348. doi: 10.1016/s0065-3527(08)60039-1. [DOI] [PubMed] [Google Scholar]
  31. Rao A. L., Grantham G. L. Biological significance of the seven amino-terminal basic residues of brome mosaic virus coat protein. Virology. 1995 Aug 1;211(1):42–52. doi: 10.1006/viro.1995.1377. [DOI] [PubMed] [Google Scholar]
  32. Suzuki M., Kuwata S., Kataoka J., Masuta C., Nitta N., Takanami Y. Functional analysis of deletion mutants of cucumber mosaic virus RNA3 using an in vitro transcription system. Virology. 1991 Jul;183(1):106–113. doi: 10.1016/0042-6822(91)90123-s. [DOI] [PubMed] [Google Scholar]
  33. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Traynor P., Young B. M., Ahlquist P. Deletion analysis of brome mosaic virus 2a protein: effects on RNA replication and systemic spread. J Virol. 1991 Jun;65(6):2807–2815. doi: 10.1128/jvi.65.6.2807-2815.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES