1887

Abstract

The movement protein (MP) of tomato mosaic virus (ToMV) was produced in . as a soluble fusion protein with glutathione -transferase. When immobilized on glutathione affinity beads, the recombinant protein was phosphorylated by incubating with cell extracts of and tobacco suspension culture cells (BY-2) in the presence of [γ-P]ATP. Phosphorylation occurred even after washing the beads with a detergent-containing buffer, indicating that the recombinant MP formed a stable complex with some protein kinase(s) during incubation with the cell extract. Phosphoamino acid analysis revealed that the MP was phosphorylated on serine and threonine residues. Phosphorylation of the MP was decreased by addition of kinase inhibitors such as heparin, suramin and quercetin, which are known to be effective for casein kinase II (CK II). The phosphorylation level was not changed by other types of inhibitor. In addition, as shown for animal and plant CK II, [γ-P]GTP was efficiently used as a phosphoryl donor. Phosphorylation was not affected by amino acid replacements at serine-37 and serine-238, but was completely inhibited by deletion of the carboxy-terminal 9 amino acids, including threonine-256, serine-257, serine-261 and serine-263. These results suggest that the MP of ToMV could be phosphorylated in plant cells by a host protein kinase that is closely related to CK II.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-8-2095
2000-08-01
2020-01-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/8/0812095a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-8-2095&mimeType=html&fmt=ahah

References

  1. Aboagye-Kwarteng, T., Ole-Moiyoi, O. K. & Lonsdale-Eccles, J. D. ( 1991; ). Phosphorylation differences among proteins of bloodstream developmental stages of Trypanosoma brucei brucei. Biochemical Journal 275, 7-14.
    [Google Scholar]
  2. Atabekov, J. G. & Dorokhov, Y. L. ( 1984; ). Plant virus-specific transport function and resistance of plants to viruses. Advances in Virus Research 29, 313-364.
    [Google Scholar]
  3. 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]
  4. Atkins, D., Hull, R., Wells, B., Roberts, K., Moore, P. & Beachy, R. N. ( 1991a; ). The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. Journal of General Virology 72, 209-211.[CrossRef]
    [Google Scholar]
  5. Atkins, D., Roberts, K., Hull, R., Prehaud, C. & Bishop, D. H. ( 1991b; ). Expression of the tobacco mosaic virus movement protein using a baculovirus expression vector. Journal of General Virology 72, 2831-2835.[CrossRef]
    [Google Scholar]
  6. Carrington, J. C., Kasschau, K. D., Mahajan, S. K. & Schaad, M. C. ( 1996; ). Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8, 1669-1681.[CrossRef]
    [Google Scholar]
  7. Citovsky, V., Knorr, D., Schuster, G. & Zambryski, P. ( 1990; ). The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60, 637-647.[CrossRef]
    [Google Scholar]
  8. Citovsky, V., McLean, B. G., Zupan, J. R. & Zambryski, P. ( 1993; ). Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes & Development 7, 904-910.[CrossRef]
    [Google Scholar]
  9. Deom, C. M., Oliver, M. J. & Beachy, R. N. ( 1987; ). The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237, 389-394.[CrossRef]
    [Google Scholar]
  10. Deom, C. M., Lapidot, M. & Beachy, R. N. ( 1992; ). Plant virus movement proteins. Cell 69, 221-224.[CrossRef]
    [Google Scholar]
  11. Fenczik, C. A., Padgett, H. S., Holt, C. A., Casper, S. J. & Beachy, R. N. ( 1995; ). Mutational analysis of the movement protein of odontoglossum ringspot virus to identify a host-range determinant. Molecular Plant–Microbe Interactions 8, 666-673.[CrossRef]
    [Google Scholar]
  12. Fujita, M., Mise, K., Kajiura, Y., Dohi, K. & Furusawa, I. ( 1998; ). Nucleic acid-binding properties and subcellular localization of the 3a protein of brome mosaic bromovirus. Journal of General Virology 79, 1273-1280.
    [Google Scholar]
  13. Goelet, P., Lomonossoff, G. P., Butler, P. J., Akam, M. E., Gait, M. J. & Karn, J. ( 1982; ). Nucleotide sequence of tobacco mosaic virus RNA. Proceedings of the National Academy of Sciences, USA 79, 5818-5822.[CrossRef]
    [Google Scholar]
  14. Haley, A., Hunter, T., Kiberstis, P. & Zimmern, D. ( 1995; ). Multiple serine phosphorylation sites on the 30 kDa TMV cell-to-cell movement protein synthesized in tobacco protoplasts. Plant Journal 8, 715-724.[CrossRef]
    [Google Scholar]
  15. Hathaway, G. M. & Traugh, J. A. ( 1983; ). Casein kinase II. Methods in Enzymology 99, 317-331.
    [Google Scholar]
  16. Hathaway, G. M., Lubben, T. H. & Traugh, J. A. ( 1980; ). Inhibition of casein kinase II by heparin. Journal of Biological Chemistry 255, 8038-8041.
    [Google Scholar]
  17. Kaelin, W. G.Jr, Pallas, D. C., DeCaprio, J. A., Kaye, F. J. & Livingston, D. M. ( 1991; ). Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell 64, 521-532.[CrossRef]
    [Google Scholar]
  18. Kamps, M. A. & Sefton, B. M. ( 1989; ). Acid and base hydrolysis of phospho-proteins bound to Immobilon: a rapid technique for the analysis of phosphoamino acids in gel-fractionated proteins. Analytical Biochemistry 176, 22-27.[CrossRef]
    [Google Scholar]
  19. Kawakami, S., Padgett, H. S., Hosokawa, D., Okada, Y., Beachy, R. N. & Watanabe, Y. ( 1999; ). Phosphorylation and/or presence of serine 37 in the movement protein of tomato mosaic tobamovirus is essential for intracellular localization and stability in vivo. Journal of Virology 73, 6831-6840.
    [Google Scholar]
  20. Li, Q. & Palukaitis, P. ( 1996; ). Comparison of the nucleic acid- and NTP-binding of the movement protein of cucumber mosaic cucumovirus and tobacco mosaic tobamovirus. Virology 216, 71-79.[CrossRef]
    [Google Scholar]
  21. Lucas, W. J. & Gilbertson, R. L. ( 1994; ). Plasmodesmata in relation to viral movement within leaf tissues. Annual Review of Phytopathology 32, 387-411.[CrossRef]
    [Google Scholar]
  22. Meshi, T., Watanabe, Y., Saito, T., Sugimoto, A., Maeda, T. & Okada, Y. ( 1987; ). Function of the 30 kd protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO Journal 6, 2557-2563.
    [Google Scholar]
  23. Meshi, T., Motoyoshi, F., Maeda, T., Yoshiwoka, S., Watanabe, H. & Okada, Y. ( 1989; ). Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell 1, 515-522.[CrossRef]
    [Google Scholar]
  24. Meshi, T., Hosokawa, D., Kawagishi, M., Watanabe, Y. & Okada, Y. ( 1992; ). Reinvestigation of intracellular localization of the 30K protein in tobacco protoplasts infected with tobacco mosaic virus RNA. Virology 187, 809-813.[CrossRef]
    [Google Scholar]
  25. Mise, K., Allison, R. F., Janda, M. & Ahlquist, P. ( 1993; ). Bromovirus movement protein genes play a crucial role in host specificity. Journal of Virology 67, 2815-2823.
    [Google Scholar]
  26. Nagata, T., Okada, K., Takebe, I. & Matsui, C. ( 1981; ). Delivery of tobacco mosaic virus RNA into plant protoplasts mediated by reverse-phase evaporation vesicles (liposomes). Molecular and General Genetics 184, 161-165.
    [Google Scholar]
  27. Ohno, T., Aoyagi, M., Yamanashi, Y., Saito, H., Ikawa, S., Meshi, T. & Okada, Y. ( 1984; ). Nucleotide sequence of the tobacco mosaic virus (tomato strain) genome and comparison with the common strain genome. Journal of Biochemistry (Tokyo) 96, 1915-1923.
    [Google Scholar]
  28. Padgett, H. S., Epel, B. L., Kahn, T. W., Heinlein, M., Watanabe, Y. & Beachy, R. N. ( 1996; ). Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection. Plant Journal 10, 1079-1088.[CrossRef]
    [Google Scholar]
  29. Pearson, R. B. & Kemp, B. E. ( 1991; ). Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods in Enzymology 200, 62-81.
    [Google Scholar]
  30. Reichel, C., Mas, P. & Beachy, R. N. ( 1999; ). The role of the ER and cytoskeleton in plant viral trafficking. Trends in Plant Science 4, 458-462.[CrossRef]
    [Google Scholar]
  31. Ruzzene, M., Vianello, F., Donella-Deana, A. & Deana, R. ( 1992; ). Purification and characterization of two casein kinases from ejaculated bovine spermatozoa. Journal of Biochemistry (Tokyo) 112, 768-774.
    [Google Scholar]
  32. Taliansky, M. E., Malyshenko, S. I., Pshennikova, E. S. & Atabekov, J. G. ( 1982; ). Plant virus-specific transport function II: a factor controlling virus host range. Virology 122, 327-331.[CrossRef]
    [Google Scholar]
  33. Tomenius, K., Clapham, D. & Meshi, T. ( 1987; ). Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160, 363-371.[CrossRef]
    [Google Scholar]
  34. Watanabe, Y., Emori, Y., Ooshika, I., Meshi, T., Ohno, T. & Okada, Y. ( 1984; ). Synthesis of TMV-specific RNAs and proteins at the early stage of infection in tobacco protoplasts: transient expression of the 30K protein and its mRNA. Virology 133, 18-24.[CrossRef]
    [Google Scholar]
  35. Watanabe, Y., Ogawa, T. & Okada, Y. ( 1992; ). In vivo phosphorylation of the 30-kDa protein of tobacco mosaic virus. FEBS Letters 313, 181-184.[CrossRef]
    [Google Scholar]
  36. Weber, H. & Pfitzner, A. J. ( 1998; ). Tm-2(2) resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Molecular Plant–Microbe Interactions 11, 498-503.[CrossRef]
    [Google Scholar]
  37. Weber, H., Schultze, S. & Pfitzner, A. J. ( 1993; ). Two amino acid substitutions in the tomato mosaic virus 30-kilodalton movement protein confer the ability to overcome the Tm-2(2) resistance gene in the tomato. Journal of Virology 67, 6432-6438.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-8-2095
Loading
/content/journal/jgv/10.1099/0022-1317-81-8-2095
Loading

Data & Media loading...

Most cited articles

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