1887

Abstract

Green fluorescent protein (GFP)-tagging was used to determine the intracellular localization pattern of the proteins encoded by banana bunchy top virus (BBTV) DNA-3, -4 and -6. The protein encoded by BBTV DNA-4, which possesses a hydrophobic N terminus, was found to localize exclusively to the cell periphery while the proteins encoded by BBTV DNA-3 and -6 were found in both the nucleus and the cytoplasm. Co-expression of the DNA-4 protein and the proteins encoded by BBTV DNA-3 and -6 revealed that the DNA-4 protein was able to re-locate the DNA-6 protein, but not the DNA-3 protein, to the cell periphery. The 29 amino acid N-terminal hydrophobic region of the DNA-4 gene product appeared to be essential for specific localization of this protein since deletion of this region abolished its ability to localize to the cell periphery. These results indicate that BBTV may utilize a system analogous to that of the begomoviruses with the BBTV DNA-6 protein acting as a nuclear shuttle protein (NSP) while the DNA-4 protein transports the NSP–DNA complexes to the cell periphery for intercellular transport. The protein encoded by BBTV DNA-5 was found to contain an LXCXE motif and yeast two-hybrid analysis revealed that the DNA-5 protein has retinoblastoma (Rb)-binding activity. This activity was dependent on an intact LXCXE motif since specific mutations to either the C or E residue completely abolished Rb-binding activity. These results indicate that the gene product of BBTV DNA-5 is an Rb-binding-like protein and may play an important role in host-cell cycle manipulation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-1-299
2000-01-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/1/0810299a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-1-299&mimeType=html&fmt=ahah

References

  1. Ach, R. A., Durfee, T., Miller, A. B., Taranto, P., Hanley-Bowdoin, L., Zambryski, P. C. & Gruissem, W. ( 1997; ). RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Molecular and Cellular Biology 17, 5077-5086.
    [Google Scholar]
  2. Acotto, G. P., Mullineaux, P. M., Brown, S. C. & Marie, D. ( 1993; ). Digitaria streak geminivirus replicative forms are abundant in S-phase nuclei of infected cells. Virology 195, 257-259.[CrossRef]
    [Google Scholar]
  3. Bartel, P. L., Chien, C. T., Sternglanz, R. & Fields, S. ( 1993a; ). Using the two hybrid system to detect protein–protein interactions. In Cellular Interactions in Development: A Practical Approach, pp. 153-179. Edited by D. A. Hartley. Oxford: Oxford University Press.
  4. Bartel, P. L., Chien, C. T., Sternglanz, R. & Fields, S. ( 1993b; ). Elimination of false positives that arise in using the two-hybrid system. Biotechniques 14, 920-924.
    [Google Scholar]
  5. Boevink, P., Chu, P. W. G. & Keese, P. ( 1995; ). Sequence of subterranean clover stunt virus DNA: affinities with the geminiviruses. Virology 207, 354-361.[CrossRef]
    [Google Scholar]
  6. Boulton, M. I., Pallaghy, C. K., Chatani, M., MacFarlane, S. & Davies, J. W. ( 1993; ). Replication of maize streak virus mutants in maize protoplasts: evidence for a movement protein. Virology 192, 85-93.[CrossRef]
    [Google Scholar]
  7. Briddon, R. W., Lunness, P., Chamberlain, L. C., Brundish, H., Pinner, M. S. & Markham, P. G. ( 1992; ). The nucleotide sequence of an infectious insect transmissible clone of the geminivirus Panicum streak virus. Journal of General Virology 73, 1041-1047.[CrossRef]
    [Google Scholar]
  8. Brough, C. L., Hayes, R. J., Morgan, A. J., Coutts, R. H. & Buck, K. W. ( 1988; ). Effects of mutagenesis in vitro on the ability of cloned tomato golden mosaic virus DNA to infect Nicotiana benthamiana plants. Journal of General Virology 69, 503-514.[CrossRef]
    [Google Scholar]
  9. Burns, T. M., Harding, R. M. & Dale, J. L. ( 1995; ). The genome organization of banana bunchy top virus: analysis of six ssDNA components. Journal of General Virology 76, 1471-1482.[CrossRef]
    [Google Scholar]
  10. Chiu, W. L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. & Sheen, J. ( 1996; ). Engineered GFP as a vital reporter gene in plants. Current Biology 6, 325-330.[CrossRef]
    [Google Scholar]
  11. Dickinson, V. J., Halder, J. & Woolston, C. J. ( 1996; ). The product of maize streak virus ORF V1 is associated with secondary plasmodesmata and is first detected with the onset of viral lesions. Virology 220, 5159.
    [Google Scholar]
  12. Donson, J., Acotto, G. P., Boulton, M. I., Mullineaux, P. M. & Davies, J. W. ( 1987; ). The nucleotide sequence of a geminivirus from Digitaria sanguinalis. Virology 161, 160-169.[CrossRef]
    [Google Scholar]
  13. Dugdale, B. (1998). Promoter activity associated with the intergenic regions of banana bunchy top virus. PhD thesis, Queensland University of Technology, Australia.
  14. Dugdale, B., Becker, D. K., Harding, R. M. & Dale, J. L. ( 1998; ). Promoter activity associated with the intergenic regions of banana bunchy top virus DNA-1 to -6 in transgenic tobacco and banana cells. Journal of General Virology 79, 2301-2311.
    [Google Scholar]
  15. Feilotter, H. E., Hannon, G. J., Ruddell, C. J. & Beach, D. ( 1994; ). Construction of an improved host strain for two hybrid screening. Nucleic Acids Research 22, 1502-1503.[CrossRef]
    [Google Scholar]
  16. Fields, S. & Song, O. ( 1989; ). A novel genetic system to detect protein–protein interactions. Nature 340, 245-246.[CrossRef]
    [Google Scholar]
  17. Geitz, R. D. & Schiestl, R. H. ( 1995; ). Transforming yeast with DNA. Methods in Molecular and Cellular Biology 5, 255-269.
    [Google Scholar]
  18. Grafi, G. R., Burnett, R. J., Helentjaris, T., Larkins, B. A., DeCaprio, J. A., Sellers, W. R. & Kaelin, W. G. ( 1996; ). A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoduplication. Proceedings of the National Academy of Sciences, USA 93, 8962-8967.[CrossRef]
    [Google Scholar]
  19. Guiterrez, C. ( 1998; ). Retinoblastoma pathway in plant cell cycle and development. Current Opinion in Plant Biology 1, 492-497.[CrossRef]
    [Google Scholar]
  20. Hafner, G. J., Stafford, M. R., Wolter, L. C., Harding, R. M. & Dale, J. L. ( 1997a; ). Nicking and joining activity of banana bunchy top virus replication protein in vitro. Journal of General Virology 78, 1795-1802.
    [Google Scholar]
  21. Hafner, G. J., Harding, R. M. & Dale, J. L. ( 1997b; ). A DNA primer associated with banana bunchy top virus. Journal of General Virology 78, 1795-1799.
    [Google Scholar]
  22. Hannon, G. J., Debetrick, D. & Beach, D. ( 1993; ). Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes & Development 7, 2378-2391.[CrossRef]
    [Google Scholar]
  23. Harding, R. M., Burns, T. M., Hafner, G. J., Dietzgen, R. & Dale, J. L. ( 1993; ). The nucleotide sequence of one segment of the banana bunchy top genome contains a putative replicase gene. Journal of General Virology 74, 323-328.[CrossRef]
    [Google Scholar]
  24. Harper, J. W., Adami, G. R., Wei, N., Kyomarsi, K. & Elledge, S. J. ( 1993; ). The p21 Cdk-interacting protein Cip1 is a potent inhibitor of cyclin-dependent kinases. Cell 75, 805-816.[CrossRef]
    [Google Scholar]
  25. Iwabuchi, K., Li, B., Bartel, P. & Fields, S. ( 1993; ). Use of the two-hybrid system to identify the domain of p53 involved in oligomerisation. Oncogene 8, 1693-1696.
    [Google Scholar]
  26. Katul, L., Maiss, E., Morozov, S. Y. & Vetten, H. J. ( 1997; ). Analysis of six DNA components of faba bean necrotic yellows virus genome and their structural affinity to related plant virus genomes. Virology 233, 247-259.[CrossRef]
    [Google Scholar]
  27. Katul, L., Timchenko, T., Gronenborn, B. & Vetten, H. J. ( 1998; ). Ten distinct circular ssDNA components, four of which encode putative replication-associated proteins, are associated with the faba bean necrotic yellows virus genome. Journal of General Virology 79, 3101-3109.
    [Google Scholar]
  28. Li, B. & Fields, S. ( 1993; ). Identification of mutations in p53 that affect its binding to SV40 T antigen by using the yeast two hybrid system. FASEB Journal 7, 957-963.
    [Google Scholar]
  29. Li, L., Saunders, K., Thomas, C. L, Davies, J. W. & Stanley, J. ( 1999; ). Bean yellow dwarf virus RepA, but not Rep, binds to maize retinoblastoma protein, and the virus tolerates mutations in the consensus binding motif. Virology 256, 270-279.[CrossRef]
    [Google Scholar]
  30. Liu, H., Boulton, M. I. & Davies, J. W. ( 1997; ). Maize streak virus coat protein binds single- and double-stranded DNA in vitro. Journal of General Virology 78, 1265-1270.
    [Google Scholar]
  31. Morris, B. A. M., Richardson, K. A., Haley, A., Zhan, X. & Thomas, J. E. ( 1992; ). The nucleotide sequence of the infectious cloned DNA component of tobacco yellow dwarf virus reveals features of geminiviruses infecting monocotyledonous plants. Virology 187, 633-642.[CrossRef]
    [Google Scholar]
  32. Mullineaux, P. M., Donson, J., Morris-Krsinich, B. A. M., Boulton, M. I. & Davies, J. W. ( 1984; ). The nucleotide sequence of maize streak virus DNA. EMBO Journal 3, 3063-3068.
    [Google Scholar]
  33. Nagar, S., Pedersen, T. J., Carrick, K. M., Hanley-Bowdoin, L. & Robertson, D. ( 1995; ). A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells. Plant Cell 7, 705-719.[CrossRef]
    [Google Scholar]
  34. Noueiry, A. O., Lucas, W. J. & Gilbertson, R. L. ( 1994; ). Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76, 925-932.[CrossRef]
    [Google Scholar]
  35. Rohde, W., Randles, J. W., Langridge, P. & Hanold, D. ( 1990; ). Nucleotide sequence of a circular single-stranded DNA associated with coconut foliar decay virus. Virology 176, 648-651.[CrossRef]
    [Google Scholar]
  36. Sanderfoot, A. A. & Lazarowitz, S. G. ( 1995; ). Cooperation in viral movement: the geminivirus BL1 movement protein interacts with BR1 and redirects it from the nucleus to the cell periphery. Plant Cell 7, 1185-1194.[CrossRef]
    [Google Scholar]
  37. Sano, Y., Wada, M., Hashimoto, Y., Matsumoto, T. & Kojima, M. ( 1998; ). Sequences of ten circular ssDNA components associated with the milk vetch dwarf virus genome. Journal of General Virology 79, 3111-3118.
    [Google Scholar]
  38. Sudarshana, M. R., Wang, H. L., Lucas, W. J. & Gilbertson, R. L. ( 1998; ). Dynamics of bean dwarf mosaic geminivirus cell-to-cell and long-distance movement in Phaseolus vulgaris revealed, using the green fluorescent protein. Molecular Plant–Microbe Interactions 11, 277-291.[CrossRef]
    [Google Scholar]
  39. Wanitchakorn, R., Harding, R. M. & Dale, J. L. ( 1997; ). Banana bunchy top virus DNA-3 encodes the viral coat protein. Archives of Virology 142, 1673-1680.[CrossRef]
    [Google Scholar]
  40. Xie, Q., Suarez-Lopez, P. & Gutierrez, C. ( 1995; ). Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. EMBO Journal 14, 4073-4082.
    [Google Scholar]
  41. Xie, Q., Sanz-Burgos, A. P., Hannon, G. J. & Gutierrez, C. ( 1996; ). Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO Journal 15, 4900-4908.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-1-299
Loading
/content/journal/jgv/10.1099/0022-1317-81-1-299
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