1887

Abstract

The intra- and intercellular transport of potexviruses require interactions among viral RNA, coat protein and elements of the triple gene block proteins (TGBps). In this study, the requirement of bamboo mosaic virus (BaMV) TGBps for movement functions and the compatibilities with those of two potexviruses, (PVX) and (FoMV), were examined using a satellite RNA-mediated -complementation assay system. Single or multiple TGBps of BaMV, PVX and FoMV were expressed from BaMV satellite RNA (satBaMV RNA) vectors to complement the functions of green fluorescent protein-tagged, movement-defective BaMV with mutation(s) in the matching gene(s). It was found that individual BaMV TGBps expressed from the satellite vector could function normally , whereas bi-gene BaMV TGBp constructs in which the expression of TGBp3 might be impaired and individual TGBp genes from PVX or FoMV could not complement the movement functions of the defective helper viruses. Furthermore, alterations of the ratio among TGBps by ectopic expression of individual components of TGBps from satBaMV RNA vectors did not affect the cell-to-cell movement capabilities of wild-type BaMV significantly. The results indicate that species-specific interactions among movement proteins are obligatory for the cell-to-cell movement of BaMV and possibly other potexviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81625-0
2006-05-01
2019-09-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/5/1357.html?itemId=/content/journal/jgv/10.1099/vir.0.81625-0&mimeType=html&fmt=ahah

References

  1. Agranovsky, A. A., Folimonov, A. S., Folimonova, S. Yu., Morozov, S. Yu., Schiemann, J., Lesemann, D. & Atabekov, J. G. ( 1998; ). Beet yellows closterovirus HSP70-like protein mediates the cell-to-cell movement of a potexvirus transport-deficient mutant and a hordeivirus-based chimeric virus. J Gen Virol 79, 889–895.
    [Google Scholar]
  2. Ajjikuttira, P., Loh, C.-S. & Wong, S.-M. ( 2005; ). Reciprocal function of movement proteins and complementation of long-distance movement of Cymbidium mosaic virus RNA by Odontoglossum ringspot virus coat protein. J Gen Virol 86, 1543–1553.[CrossRef]
    [Google Scholar]
  3. 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.[CrossRef]
    [Google Scholar]
  4. Bayne, E. H., Rakitina, D. V., Morozov, S. Y. & Baulcombe, D. C. ( 2005; ). Cell-to- cell movement of Potato potexvirus X is dependent on suppression of RNA silencing. Plant J 44, 471–482.[CrossRef]
    [Google Scholar]
  5. Bleykasten-Grosshans, C., Guilley, H., Bouzoubaa, S., Richards, K. E. & Jonard, G. ( 1997; ). Independent expression of the first two triple gene block proteins of beet necrotic yellow vein virus complements virus defective in the corresponding gene but expression of the third protein inhibits viral cell-to-cell movement. Mol Plant Microbe Interact 10, 240–246.[CrossRef]
    [Google Scholar]
  6. Chang, B.-Y., Lin, N.-S., Liou, D.-Y., Chen, J.-P., Liou, G.-G. & Hsu, Y.-H. ( 1997; ). Subcellular localization of the 28 kDa protein of the triple-gene-block of bamboo mosaic potexvirus. J Gen Virol 78, 1175–1179.
    [Google Scholar]
  7. Chapman, S., Hills, G., Watts, J. & Baulcombe, D. ( 1992; ). Mutational analysis of the coat protein gene of potato virus X: effects on virion morphology and viral pathogenicity. Virology 191, 223–230.[CrossRef]
    [Google Scholar]
  8. Erhardt, M., Herzog, E., Lauber, E., Fritsch, C., Guilley, H., Jonard, G., Richards, K. & Bouzoubaa, S. ( 1999; ). Transgenic plants expressing the TGB1 protein of peanut clump virus complement movement of TGB1-defective peanut clump virus but not of TGB1-defective beet necrotic yellow vein virus. Plant Cell Rep 18, 614–619.[CrossRef]
    [Google Scholar]
  9. Forster, R. L. S., Beck, D. L., Guilford, P. J., Voot, D. M., van Dolleweerd, C. J. & Andersen, M. T. ( 1992; ). The coat protein of white clover mosaic potexvirus has a role in facilitating cell-to-cell transport in plants. Virology 191, 480–484.[CrossRef]
    [Google Scholar]
  10. 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.[CrossRef]
    [Google Scholar]
  11. Haupt, S., Cowan, G. H., Ziegler, A., Roberts, A. G., Oparka, K. J. & Torrance, L. ( 2005; ). Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 17, 164–181.[CrossRef]
    [Google Scholar]
  12. Hefferon, K. L., Doyle, S. & AbouHaider, M. G. ( 1997; ). Immunological detection of the 8K protein of potato virus X (PVX) in cell walls of PVX-infected tobacco and transgenic potato. Arch Virol 142, 425–433.[CrossRef]
    [Google Scholar]
  13. Herzog, E., Hemmer, O., Hauser, S., Meyer, G., Bouzoubaa, S. & Fritsch, C. ( 1998; ). Identification of genes involved in replication and movement of peanut clump virus. Virology 248, 312–322.[CrossRef]
    [Google Scholar]
  14. Ju, H. J., Samuels, T. D., Wang, Y. S., Blancaflor, E., Payton, M., Mitra, R., Krishnamurthy, K., Nelson, R. S. & Verchot-Lubicz, J. ( 2005; ). The potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiol 138, 1877–1895.[CrossRef]
    [Google Scholar]
  15. Kalinina, N. O., Rakitina, D. V., Solovyev, A. G., Schiemann, J. & Morozov, S. Yu. ( 2002; ). RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296, 321–329.[CrossRef]
    [Google Scholar]
  16. Krishnamurthy, K., Mitra, R., Payton, M. E. & Verchot-Lubicz, J. ( 2002; ). Cell-to-cell movement of the PVX 12K, 8K, or coat proteins may depend on the host, leaf developmental stage, and the PVX 25K protein. Virology 300, 269–281.[CrossRef]
    [Google Scholar]
  17. Krishnamurthy, K., Heppler, M., Mitra, R., Blancaflor, E., Payton, M., Nelson, R. S. & Verchot-Lubicz, J. ( 2003; ). The Potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virology 309, 135–151.[CrossRef]
    [Google Scholar]
  18. Lauber, E., Bleykasten-Grosshans, C., Erhardt, M., Bouzoubaa, S., Jonard, G., Richards, K. E. & Guilley, H. ( 1998; ). Cell-to-cell movement of beet necrotic yellow vein virus. I. Heterologous complementation experiments provide evidence for specific interactions among the triple gene block proteins. Mol Plant Microbe Interact 11, 618–625.[CrossRef]
    [Google Scholar]
  19. Lin, N.-S. & Chen, C.-C. ( 1991; ). Association of bamboo mosaic virus (BaMV) and BaMV-specific electron-dense crystalline bodies with chloroplasts. Phytopathology 81, 1551–1555.[CrossRef]
    [Google Scholar]
  20. Lin, N.-S., Lin, B.-Y., Lo, N.-W., Hu, C.-C., Chow, T.-Y. & Hsu, Y.-H. ( 1994; ). Nucleotide sequence of the genomic RNA of bamboo mosaic potexvirus. J Gen Virol 75, 2513–2518.[CrossRef]
    [Google Scholar]
  21. Lin, N.-S., Lee, Y.-S., Lin, B.-Y., Lee, C.-W. & Hsu, Y.-H. ( 1996; ). The open reading frame of bamboo mosaic potexvirus satellite RNA is not essential for its replication and can be replaced with a bacterial gene. Proc Natl Acad Sci U S A 93, 3138–3142.[CrossRef]
    [Google Scholar]
  22. Lin, M.-K., Chang, B.-Y., Liao, J.-T., Lin, N.-S. & Hsu, Y.-H. ( 2004; ). Arg-16 and Arg-21 in the N-terminal region of the triple-gene-block protein 1 of Bamboo mosaic virus are essential for virus movement. J Gen Virol 85, 251–259.[CrossRef]
    [Google Scholar]
  23. Liou, D.-Y., Hsu, Y.-H., Wung, C.-H., Wang, W.-H., Lin, N.-S. & Chang, B.-Y. ( 2000; ). Functional analyses and identification of two arginine residues essential to the ATP-utilizing activity of the triple gene block protein 1 of bamboo mosaic potexvirus. Virology 277, 336–344.[CrossRef]
    [Google Scholar]
  24. Lough, T. J., Shash, K., Xoconostle-Cazares, B., Hofstra, K. R., Beck, D. L., Balmori, E., Forster, R. L. S. & Lucas, W. J. ( 1998; ). Molecular dissection of the mechanism by which potexvirus triplet gene block proteins mediate cell-to-cell transport of infectious RNA. Mol Plant Microbe Interact 11, 801–814.[CrossRef]
    [Google Scholar]
  25. Lough, T. J., Netzler, N. E., Emerson, S. J., Sutherland, P., Carr, F., Beck, D. L., Lucas, W. J. & Forster, R. L. S. ( 2000; ). Cell-to-cell movement of potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Mol Plant Microbe Interact 13, 962–974.[CrossRef]
    [Google Scholar]
  26. Lough, T. J., Emerson, S. J., Lucas, W. J. & Forster, R. L. S. ( 2001; ). Trans-complementation of long-distance movement of White clover mosaic virus triple gene block (TGB) mutants: phloem-associated movement of TGBp1. Virology 288, 18–28.[CrossRef]
    [Google Scholar]
  27. Lucas, W. J. & Lee, J.-Y. ( 2004; ). Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5, 712–726.[CrossRef]
    [Google Scholar]
  28. McGeachy, K. D. & Barker, H. ( 2000; ). Potato mop-top virus RNA can move long distance in the absence of coat protein: evidence from resistant, transgenic plants. Mol Plant Microbe Interact 13, 125–128.[CrossRef]
    [Google Scholar]
  29. Mitra, R., Krishnamurthy, K., Blancaflor, E., Payton, M., Nelson, R. S. & Verchot-Lubicz, J. ( 2003; ). The Potato virus X TGBp2 protein association with the endoplasmic reticulum plays a role in but is not sufficient for viral cell-to-cell movement. Virology 312, 35–48.[CrossRef]
    [Google Scholar]
  30. Morozov, S. Yu. & Solovyev, A. G. ( 2003; ). Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84, 1351–1366.[CrossRef]
    [Google Scholar]
  31. Morozov, S. Yu., Miroshnichenko, N. A., Solovyev, A. G., Fedorkin, O. N., Zelenina, D. A., Lukasheva, L. I., Karasev, A. V., Dolja, V. V. & Atabekov, J. G. ( 1991; ). Expression strategy of the potato virus X triple gene block. J Gen Virol 72, 2039–2042.[CrossRef]
    [Google Scholar]
  32. 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. J Gen Virol 78, 2077–2083.
    [Google Scholar]
  33. Morozov, S. Yu., Solovyev, A. G., Kalinnina, N. O., Fedorkin, O. N., Samuilova, O. V., Schiemann, J. & Atabekov, J. G. ( 1999; ). Evidence for two nonoverlapping functional domains in the potato virus X 25K movement protein. Virology 260, 55–63.[CrossRef]
    [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. Arch Virol 133, 239–257.[CrossRef]
    [Google Scholar]
  35. Petty, I. T. D. & Jackson, A. O. ( 1990; ). Mutational analysis of barley stripe mosaic virus RNA β. Virology 179, 712–718.[CrossRef]
    [Google Scholar]
  36. Rouleau, M., Smith, R. J., Bancroft, J. B. & Mackie, G. A. ( 1994; ). Purification, properties, and subcellular localization of foxtail mosaic potexvirus 26-kDa protein. Virology 204, 254–265.[CrossRef]
    [Google Scholar]
  37. Sambrook, T., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  38. Schepetilnikov, M. V., Manske, U., Solovyev, A. G., Zamyatnin, A. A., Jr, Schiemann, J. & Morozov, S. Yu. ( 2005; ). The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J Gen Virol 86, 2379–2391.[CrossRef]
    [Google Scholar]
  39. Schmitt, C., Balmori, E., Jonard, G., Richards, K. E. & Guilley, H. ( 1992; ). In vitro mutagenesis of biologically active transcripts of beet necrotic yellow vein virus RNA 2: evidence that a domain of the 75-kDa readthrough protein is important for efficient virus assembly. Proc Natl Acad Sci U S A 89, 5715–5719.[CrossRef]
    [Google Scholar]
  40. Sit, T. L. & Abouhaidar, M. G. ( 1993; ). Infectious RNA transcripts derived from cloned cDNA of papaya mosaic virus: effect of mutations to the capsid and polymerase proteins. J Gen Virol 74, 1113–1140.
    [Google Scholar]
  41. Solovyev, A. G., Savenkov, E. I., Agranovsky, A. A. & Morozov, S. Yu. ( 1996; ). Comparisons of the genomic cis-elements and coding regions in RNAβ components of the hordeiviruses barley stripe mosaic virus, lychnis ringspot virus, and poa semilatent virus. Virology 219, 9–18.[CrossRef]
    [Google Scholar]
  42. Solovyev, A. G., Savenkov, E. I., Grdzelishvili, V. Z., Kalinina, N. O., Morozov, S. Yu., Schiemann, J. & Atabekov, J. G. ( 1999; ). Movement of hordeivirus hybrids with exchanges in the triple gene block. Virology 253, 278–287.[CrossRef]
    [Google Scholar]
  43. Solovyev, A. G., Stroganova, T. A., Zamyatnin, A. A., Jr, Fedorkin, O. N., Schiemann, J. & Morozov, S. Yu. ( 2000; ). Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269, 113–127.[CrossRef]
    [Google Scholar]
  44. Tamai, A. & Meshi, T. ( 2001; ). Cell-to-cell movement of potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Mol Plant Microbe Interact 14, 1158–1167.[CrossRef]
    [Google Scholar]
  45. Tamai, A., Kubota, K., Nagano, H., Yoshii, M., Ishikawa, M., Mise, K. & Meshi, T. ( 2003; ). Cucumovirus- and bromovirus-encoded movement functions potentiate cell-to-cell movement of tobamo- and potexviruses. Virology 315, 56–67.[CrossRef]
    [Google Scholar]
  46. Verchot, J., Angell, S. M. & Baulcombe, D. C. ( 1998; ). In vivo translation of the triple gene block of potato virus X requires two subgenomic mRNAs. J Virol 72, 8316–8320.
    [Google Scholar]
  47. Verchot-Lubicz, J. ( 2005; ). A new cell-to-cell transport model for potexviruses. Mol Plant Microbe Interact 18, 283–290.[CrossRef]
    [Google Scholar]
  48. Voinnet, O., Lederer, C. & Baulcombe, D. C. ( 2000; ). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157–167.[CrossRef]
    [Google Scholar]
  49. Wong, S.-M., Lee, K.-C., Yu, H.-H. & Leong, W.-F. ( 1998; ). Phylogenetic analysis of triple gene block viruses based on the TGB 1 homolog gene indicates a convergent evolution. Virus Genes 16, 295–302.[CrossRef]
    [Google Scholar]
  50. Wung, C.-H., Hsu, Y.-H., Liou, D.-Y., Hung, W.-C., Lin, N.-S. & Chang, B.-Y. ( 1999; ). Identification of the RNA-binding sites of the triple gene block protein 1 of bamboo mosaic potexvirus. J Gen Virol 80, 1119–1126.
    [Google Scholar]
  51. Yang, Y., Ding, B., Baulcombe, D. C. & Verchot, J. ( 2000; ). Cell-to-cell movement of the 25K protein of potato virus X is regulated by three other viral proteins. Mol Plant Microbe Interact 13, 599–605.[CrossRef]
    [Google Scholar]
  52. Zamyatnin, A. A., Jr, Solovyev, A. G., Savenkov, E. I., Germundsson, A., Sandgren, M., Valkonen, J. P. T. & Morozov, S. Y. ( 2004; ). Transient coexpression of individual genes encoded by the triple gene block of Potato mop-top virus reveals requirements for TGBp1 trafficking. Mol Plant Microbe Interact 17, 921–930.[CrossRef]
    [Google Scholar]
  53. Zhou, H. & Jackson, A. O. ( 1996; ). Expression of the barley stripe mosaic virus RNAβ “triple gene block”. Virology 216, 367–379.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81625-0
Loading
/content/journal/jgv/10.1099/vir.0.81625-0
Loading

Data & Media loading...

Most Cited This Month

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