1887

Abstract

It has been suggested that the beet yellows closterovirus (BYV)-encoded p65 protein, a homologue of HSP70 cell chaperones, plays a role as a virus movement protein (MP). To test this hypothesis, we used two types of complementation experiments with plant viruses containing the triple gene block (TGB) of MP genes. In one, the BYV p65 gene was cloned into a 35S promoter plasmid and introduced into plants by microprojectile bombardment along with the 35S promoter- driven GUS gene-tagged cDNA of a transport- deficient potexvirus mutant. Transient expression of p65 complemented the mutant as visualized by the significant increase in the number of cells expressing the GUS reporter gene in the infection foci. In the other test, the p65 gene was inserted into the infectious cDNA of the hordeivirus RNA component to replace either the 58 kDa MP gene or the whole TGB. Inoculation of and plants with the T7 transcripts of the chimeric RNA/, together with the hordeivirus RNAα and RNA, caused symptomless infection in inoculated leaves detected by hybridization of the total leaf RNA with a specific cDNA probe. The ability of BYV p65 to substitute for the potexvirus or hordeivirus MPs provides direct evidence for its involvement in the cell-to-cell movement of closterovirus infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-79-4-889
1998-04-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/79/4/9568985.html?itemId=/content/journal/jgv/10.1099/0022-1317-79-4-889&mimeType=html&fmt=ahah

References

  1. Agranovsky A. A. 1996; The principles of molecular organization, expression and evolution of closteroviruses: over the barriers. Advances in Virus Research 47:119–158
    [Google Scholar]
  2. Agranovsky A. A., Boyko V. P., Karasev A. V., Koonin E. V., Dolja V. V. 1991a; Putative 65 kDa protein of beet yellows closterovirus is a homologue of HSP70 heat shock proteins. Journal of Molecular Biology 217:603–610
    [Google Scholar]
  3. Agranovsky A. A., Boyko V. P., Karasev A. V., Lunina N. A., Koonin E. V., Dolja V. V. 1991b; Nucleotide sequence of the 3′-terminal half of beet yellows closterovirus RNA genome: unique arrangement of eight virus genes. Journal of General Virology 72:15–23
    [Google Scholar]
  4. Agranovsky A. A., Koonin E. V., Boyko V. P., Maiss E., Frötschl R., Lunina N. A., Atabekov J. G. 1994; Beet yellows closterovirus : complete genome structure and identification of a leader papain-like thiol protease. Virology 198:311–324
    [Google Scholar]
  5. Agranovsky A. A., Lesemann D.-E., Maiss E., Hull R., Atabekov J. G. 1995; ‘Rattlesnake’ structure of a filamentous plant RNA virus built of two capsid proteins. Proceedings ofthe National Academy of Sciences, USA 92:2470–2473
    [Google Scholar]
  6. Agranovsky A. A., Folimonova S. Yu., Folimonov A. S., Denisenko O. N., Zinovkin R. A. 1997; The beet yellows closterovirus p65 homologue of HSP70 chaperones has ATPase activity associated with its conserved N-terminal domain but does not interact with unfolded protein chains. Journal of General Virology 78:535–542
    [Google Scholar]
  7. Angell S. M., Davies C., Baulcombe D. C. 1996; Cell-to-cell movement of potato virus X is associated with a change in the size- exclusion limit of plasmodesmata in trichome cells of Nicotiana clevelandii . Virology 216:197–201
    [Google Scholar]
  8. Atabekov J. G., Novikov V. K. 1989; Barley stripe mosaic virus. AAB Descriptions of Plant Viruses344
    [Google Scholar]
  9. Atabekov J. G., Taliansky M. E. 1990; Expression of a plant virus- coded transport function by different viral genomes. Advances in Virus Research 38:201–248
    [Google Scholar]
  10. Bar-Joseph M., Garnsey S. M., Gonsalves D. 1979; The closteroviruses: a distinct group of elongated plant viruses. Advances in Virus Research 25:93–168
    [Google Scholar]
  11. Beck D. L., Guilford P. J., Voot D. M., Andersen M. T., Forster R. L. S. 1991; Triple gene block proteins of white clover mosaic potexvirus are required for transport. Virology 183:695–702
    [Google Scholar]
  12. Boyko V. P., Karasev A. V., Agranovsky A. A., Koonin E. V., Dolja V. V. 1992; Coat protein gene duplication in a filamentous RNA virus of plants. Proceedings of the National Academy of Sciences, USA 89:9156–9160
    [Google Scholar]
  13. De Jong W., Ahlquist P. 1992; A hybrid plant RNA virus made by transferring the noncapsid movement protein gene from a rod-shaped to an icosahedral virus is competent for systemic infection. Proceedings of the National Academy of Sciences, USA 89:6808–6812
    [Google Scholar]
  14. Dolja V. V., Karasev A. V., Koonin E. V. 1994; Molecular biology and evolution of closteroviruses : sophisticated build-up of large RNA genomes. Annual Review of Phytopathology 32:261–285
    [Google Scholar]
  15. Donald R. G. K., Lawrence D. M., Jackson A. O. 1997; The barley stripe mosaic virus 58-kilodalton βb protein is a multifunctional RNA binding protein. Journal of Virology 71:1538–1546
    [Google Scholar]
  16. Duffus J. E. 1973; The yellowing diseases of beet. Advances in Virus Research 18:347–386
    [Google Scholar]
  17. Febres V. J., Ashoulin L., Mawassi M., Frank A., Bar-Joseph M., Manjunath K. L., Lee R. F., Niblett C. L. 1996; The p27 protein is present at one end of citrus tristeza virus particles. Phytopathology 86:1331–1335
    [Google Scholar]
  18. Giesman-Cookmeyer D., Silver S., Vaewhongs A. A., Lommel S. A., Deom C. M. 1995; Tobamovirus and dianthovirus movement proteins are functionally homologous. Virology 213:38–45
    [Google Scholar]
  19. Heinlein M., Epel B. L., Padget H. S., Beachy R. N. 1995; Interaction of tobamovirus movement proteins with the plant cyto-skeleton. Science 270:1983–1985
    [Google Scholar]
  20. Jelkmann W., Fetchner B., Agranovsky A. A. 1997; Complete genome structure and phylogenetic analysis of little cherry virus, a mealybug-transmissible closterovirus. Journal of General Virology 78:2067–2071
    [Google Scholar]
  21. Kalinina N. O., Fedorkin O. N., Samuilova O. N., Maiss E., Korpela T., Morozov S. Yu., Atabekov J. G. 1996; Expression and biochemical analysis of the recombinant potato virus X 25K movement protein. FEBS Letters 397:75–78
    [Google Scholar]
  22. Kaplan I. B., Shintaku M. H., Li Q., Zhang L., Marsh L. E., Palukaitis P. 1995; Complementation of virus movement in transgenic tobacco expressing the cucumber mosaic virus 3a gene. Virology 209:188–199
    [Google Scholar]
  23. Karasev A. V., Kashina A. S., Gelfand V. I., Dolja V. V. 1992; HSP70-related 65-kDa protein of beet yellows closterovirus is a microtubule-binding protein. FEBS Letters 304:12–14
    [Google Scholar]
  24. Karasev A. V., Boyko V. P., Gowda S., Nikolaeva O. N., Hilf M. E., Koonin E. V., Niblett C. L., Cline K. C., Gumpf D. J., Lee R. F., Garnsey S. M., Lewandowski D. J., Dawson W. O. 1995; Complete sequence of the citrus tristeza virus RNA genome. Virology 208:511–520
    [Google Scholar]
  25. Keese P. K., Gibbs A. 1992; The origin of genes: ‘big bang’ or continuous creation?. Proceedings of the National Academy of Sciences, USA 89:9489–9493
    [Google Scholar]
  26. Klaassen V. A., Boeshore M., Koonin E. V., Falk B. W. 1995; Genome structure and phylogenetic analysis of lettuce infectious yellows virus, a whitefly-transmitted, bipartite closterovirus. Virology 208:99–110
    [Google Scholar]
  27. Koonin E. V., Mushegian A. R., Ryabov E. V., Dolja V. V. 1991; Diverse groups of plant RNA and DNA viruses share related movement proteins that may possess chaperone-like activity. Journal of General Virology 72:2895–2903
    [Google Scholar]
  28. McLean B. G., Zupan J., Zambryski P. 1995; Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7:2101–2114
    [Google Scholar]
  29. Melcher U. 1990; Similarities between putative transport proteins of plant viruses. Journal of General Virology 71:1009–1018
    [Google Scholar]
  30. Mezitt L. A., Lucas W. J. 1996; Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Molecular Biology 32:251–273
    [Google Scholar]
  31. Milne R. G., Lesemann D.-E. 1984; Immunosorbent electron microscopy in plant virus studies. Methods in Virology 8:85–101
    [Google Scholar]
  32. Morozov S. Yu., Dolja V. V., Atabekov J. G. 1989; Probable reassortment of genomic elements among elongated RNA-containing plant viruses. Journal of Molecular Evolution 29:52–62
    [Google Scholar]
  33. Morozov S. Yu, Fedorkin O. N., Jüttner G., Schiemann J., Baulcombe D. C., Atabekov J. G. 1997; Complementation of a potato virus X mutant mediated by bombardment of plant tissues with cloned viral movement protein genes. Journal of General Virology 78:2077–2083
    [Google Scholar]
  34. Mushegian A. R., Koonin E. V. 1993; Cell-to-cell movement of plant viruses. Insights from amino acid sequence comparisons of movement proteins and from analogies with cellular transport systems. Archives of Virology 133:239–257
    [Google Scholar]
  35. Pappu H. R., Karasev A. V., Anderson E. J., Pappu S. S., Hilf M. E., Febres M. E., Eckloff R. M. G., McCaffery M., Boyko V. P., Gowda S., Dolja V. V., Koonin E. V., Gumpf D. J., Cline K. C., Garnsey S. M., Dawson W. O., Lee R. F., Niblett C. L. 1994; Nucleotide sequence and organization of eight 3′ open reading frames of the citrus tristeza closterovirus genome. Virology 199:35–46
    [Google Scholar]
  36. Petty I. T. D., Jackson A. O. 1990; Mutational analysis of barley stripe mosaic virus RNAb. Virology 179:712–718
    [Google Scholar]
  37. Petty I. T. D., Hunter B. G., Jackson A. O. 1988; A novel strategy for one-step cloning of full-length cDNA and its application to the genome of barley stripe mosaic virus. Gene 74:423–432
    [Google Scholar]
  38. Petty I. T. D., Hunter B. G., Wei N., Jackson A. O. 1989; Infectious barley stripe mosaic virus RNA transcribed from full-length genomic cDNA clones. Virology 171:342–349
    [Google Scholar]
  39. Rouleau M., Smith R. J., Bancroft J. B., Mackie G. A. 1994; Purification, properties, and subcellular location of foxtail mosaic potexvirus 26-kDa protein. Virology 204:254–265
    [Google Scholar]
  40. Saalbach G., Rosso M., Schumann U. 1996; The vacuolar targeting signal of the 2S-albumin from Bertholletia excelsa resides at the C-terminal propeptide as an essential element. Plant Physiology 112:975–985
    [Google Scholar]
  41. Smirnyagina E. V., Morozov S. Yu., Rodionova N. P., Miroshnichenko N. A., Solovyev A. G., Fedorkin O. N., Atabekov J. G. 1991; Translational efficiency and competitive ability of mRNAs with 5′-untranslated αβ-leader of PVX RNA. Biochemie 73:587–598
    [Google Scholar]
  42. Solovyev A. G., Zelenina D. A., Savenkov E. I., Grdzelishvili V. Z., Morozov S. Yu., Lesemann D.-E., Maiss E., Casper R., Atabekov J. G. 1996; Movement of barley stripe mosaic virus chimera with a tobacco mosaic virus movement protein. Virology 217:435–441
    [Google Scholar]
  43. Solovyev A. G., Zelenina D. A., Savenkov E. I., Grdzelishvili V. Z., Morozov S. Yu., Maiss E., Casper R., Atabekov J. G. 1997; Host-controlled cell-to-cell movement of a hybrid barley stripe mosaic virus expressing a dianthovirus movement protein. Intervirology 40:1–6
    [Google Scholar]
  44. Töpfer R., Matzeit V., Groneborn B., Schell J., Steinbiss H.-H. 1987; A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Research 15:5890
    [Google Scholar]
  45. Verwoerd T. C., Dekker B. M. M., Hoekema A. 1989; A small scale procedure for the rapid isolation of plant RNAs. NucleicAcids Research 17:2106
    [Google Scholar]
  46. Zhou H., Jackson A. O. 1996; Expression of barley stripe mosaic virus RNAβ ‘Triple Gene Block’. Virology 216:367–379
    [Google Scholar]
  47. Ziegler-Graf V., Guilford P. J., Baulcombe D. C. 1991; Tobacco rattle virus RNA-1 29K gene product potentiates viral movement and also affects symptom induction in tobacco. Virology 182:145–155
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-79-4-889
Loading
/content/journal/jgv/10.1099/0022-1317-79-4-889
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error