1887

Abstract

Complementation of movement and coat proteins of the orchid-infecting potexvirus (CymMV) and tobamovirus (ORSV) was investigated. , which is susceptible to both CymMV and ORSV, was used as a model system. Four transgenic lines, each harbouring one of the movement protein (MP) or coat protein (CP) genes of CymMV or ORSV, were constructed. The MP of CymMV consists of three overlapping open reading frames, together called the triple-gene block (TGB). CymMV and ORSV mutants, each carrying an inactivated MP or CP, were generated from the respective biologically active full-length cDNA clones. Complementation was studied by infecting transgenic plants with transcripts generated from these mutants. The cell-to-cell movement of a movement-deficient CymMV was restored in transgenic plants carrying the ORSV MP transgene. Similarly, CymMV TGB1 transgenic plants were able to rescue the cell-to-cell movement of a movement-deficient ORSV mutant. ORSV CP transgenic plants supported systemic movement of a CymMV CP-deficient mutant. However, in these plants, neither encapsidation of CymMV RNA with ORSV CP nor CymMV CP expression was detected. Long-distance movement of an ORSV CP-deficient mutant was not supported by CymMV CP. The complementation of MPs and CPs of CymMV and ORSV facilitates movement of these viruses in plants, except for long-distance movement of ORSV RNA by CymMV CP.

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2005-05-01
2019-10-20
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References

  1. 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]
  2. Atabekov, J. G., Malyshenko, S. I., Morozov, Yu. S., Taliansky, M. E., Solovyev, A. G., Agranovsky, A. A. & Shapka, N. A. ( 1999; ). Identification and study of tobacco mosaic virus movement function by complementation tests. Philos Trans R Soc Lond B Biol Sci 354, 629–635.[CrossRef]
    [Google Scholar]
  3. Baulcombe, D. C., Chapman, S. & Santa Cruz, S. ( 1995; ). Jellyfish green fluorescent protein as a reporter for virus infections. Plant J 7, 1045–1053.[CrossRef]
    [Google Scholar]
  4. 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.[CrossRef]
    [Google Scholar]
  5. 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]
  6. Cassab, G. I. & Varner, J. E. ( 1987; ). Immunocytolocalization of extensin in developing soybean seed coats by immunogold-silver staining and by tissue printing on nitrocellulose paper. J Cell Biol 105, 2581–2588.[CrossRef]
    [Google Scholar]
  7. Chapman, S., Hills, G., Watts, J. & Baulcombe, D. ( 1992; ). Mutational analysis of the coat protein gene of potato virus X: effects of virion morphology and viral pathogenicity. Virology 191, 223–230.[CrossRef]
    [Google Scholar]
  8. Chilton, M.-D., Currier, T. C., Farrand, S. K., Bendich, A. J., Gordon, M. P. & Nester, E. W. ( 1974; ). Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc Natl Acad Sci U S A 71, 3672–3676.[CrossRef]
    [Google Scholar]
  9. Christie, S. R., Purcifull, D. E., Crawford, W. E. & Ahmed, N. A. ( 1987; ). Electron microscopy of negatively stained clarified viral concentrates obtained from small tissue samples with appendices on negative staining techniques. Bulletin of the Agricultural Experimental Station, vol. 872, p. 44. Gainesville, FL: University of Florida.
  10. Cooper, B., Schmitz, I., Rao, A. L. N., Beachy, R. N. & Dodds, A. J. ( 1996; ). Cell-to-cell transport of movement-defective cucumber mosaic and tobacco mosaic viruses in transgenic plants expressing heterologous movement protein genes. Virology 216, 208–213.[CrossRef]
    [Google Scholar]
  11. 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]
  12. Fedorkin, O. N., Merits, A., Lucchesi, J., Solovyev, A. G., Saarma, M., Morozov, S. Yu. & Mäkinen, K. ( 2000; ). Complementation of the movement-deficient mutations in potato virus X: potyvirus coat protein mediates cell-to-cell trafficking of C-terminal truncation but not deletion mutant of potexvirus coat protein. Virology 270, 31–42.[CrossRef]
    [Google Scholar]
  13. Fedorkin, O. N., Solovyev, A. G., Yelina, N. E., Zamayatnin, A. A., Jr, Zinovkin, R. A., Mäkinen, K., Schiemann, J. & Morozov, S. Yu. ( 2001; ). Cell-to-cell movement of potato virus X involves distinct functions of the coat protein. J Gen Virol 82, 449–458.
    [Google Scholar]
  14. 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]
  15. Fuentes, A. L. & Hamilton, R. I. ( 1991; ). Sunn-hemp mosaic virus facilitates cell-to-cell spread of southern bean mosaic virus in a nonpermissive host. Phytopathology 81, 1302–1305.[CrossRef]
    [Google Scholar]
  16. Giesman-Cookmeyer, D., Siver, 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]
  17. Hamilton, R. I. & Dodds, J. A. ( 1970; ). Infection of barley by tobacco mosaic virus in single and mixed infection. Virology 42, 266–268.[CrossRef]
    [Google Scholar]
  18. Hu, W.-W., Wong, S.-M., Loh, C.-S. & Goh, C.-J. ( 1998; ). Synergism in replication of cymbidium mosaic potexvirus (CymMV) and odontoglossum ringspot tobamovirus (ORSV) RNA in orchid protoplasts. Arch Virol 143, 1265–1275.[CrossRef]
    [Google Scholar]
  19. Kawakami, S., Watanabe, Y. & Beachy, R. N. ( 2004; ). Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci U S A 101, 6291–6296.[CrossRef]
    [Google Scholar]
  20. 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]
  21. Lee, J.-Y., Yoo, B.-C., Rojas, M. R., Gomez-Ospina, N., Staehelin, L. A. & Lucas, W. J. ( 2003; ). Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299, 392–396.[CrossRef]
    [Google Scholar]
  22. Lough, T. J., Shash, K., Xoconostle-Cázares, 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 triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol Plant Microbe Interact 11, 801–814.[CrossRef]
    [Google Scholar]
  23. 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]
  24. Malyshenko, S. I., Kondakova, O. A., Taliansky, M. E. & Atabekov, J. G. ( 1989; ). Plant virus transport function: complementation by helper viruses is non-specific. J Gen Virol 70, 2751–2757.[CrossRef]
    [Google Scholar]
  25. Mansky, L. M., Andrews, R. E., Jr, Durand, D. P. & Hill, J. H. ( 1990; ). Plant virus location in leaf tissue by press blotting. Plant Mol Biol Rep ISPMB 8, 13–17.[CrossRef]
    [Google Scholar]
  26. 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 J 6, 2557–2563.
    [Google Scholar]
  27. 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]
  28. Morozov, S. Yu., Dolja, V. V. & Atabekov, J. G. ( 1989; ). Probable reassortment of genomic elements among elongated RNA-containing plant viruses. J Mol Evol 29, 52–62.[CrossRef]
    [Google Scholar]
  29. Morozov, S. Y., 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]
  30. Murashige, T. & Skoog, F. ( 1962; ). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15, 473–497.[CrossRef]
    [Google Scholar]
  31. Petty, I. T. D. & Jackson, A. O. ( 1989; ). Mutational analysis of barley stripe mosaic virus RNA β. Virology 179, 712–718.
    [Google Scholar]
  32. Petty, I. T. D., French, R., Jones, R. W. & Jackson, A. O. ( 1990; ). Identification of barley stripe mosaic virus genes involved in viral RNA replication and systemic movement. EMBO J 9, 3453–3457.
    [Google Scholar]
  33. Power, J. B. & Chapman, J. V. ( 1985; ). Isolation, culture and genetic manipulation of plant protoplasts. In Plant Cell Culture, pp. 37–66. Edited by R. A. Dixon. Oxford: ICR Press.
  34. Pringle, C. R. ( 1997; ). Virus taxonomy 1997. Arch Virol 142, 1727–1733.
    [Google Scholar]
  35. Quillet, L., Guilley, H., Jonard, G. & Richards, K. ( 1989; ). In vitro synthesis of biologically active beet necrotic yellow vein virus RNA. Virology 172, 293–301.[CrossRef]
    [Google Scholar]
  36. Rao, A. L. N., Cooper, B. & Deom, C. M. ( 1998; ). Defective movement of viruses in the family Bromoviridae is differentially complemented in Nicotiana benthamiana expressing tobamovirus or dianthovirus movement proteins. Phytopathology 88, 666–672.[CrossRef]
    [Google Scholar]
  37. Richins, R. D., Donson, J., Lewandowsky, D. J., Ducasse, D. A., Dawson, W. O. & Shepherd, R. J. ( 1993; ). Temperature-dependent complementation of movement-deficient mutants of tobacco mosaic virus by gene I of peanut chlorotic streak caulimovirus. Phytopathology 83, 1349.
    [Google Scholar]
  38. Ryabov, E. V., Roberts, I. M., Palukaitis, P. & Taliansky, M. ( 1999a; ). Host-specific cell-to-cell and long-distance movements of cucumber mosaic virus are facilitated by the movement protein of groundnut rosette virus. Virology 260, 98–108.[CrossRef]
    [Google Scholar]
  39. Ryabov, E. V., Robinson, D. J. & Taliansky, M. E. ( 1999b; ). A plant virus-encoded protein facilitates long-distance movement of heterologous viral RNA. Proc Natl Acad Sci U S A 96, 1212–1217.[CrossRef]
    [Google Scholar]
  40. Ryu, K. H. & Park, W. M. ( 1995; ). The complete nucleotide sequence and genome organization of odontoglossum ringspot tobamovirus RNA. Arch Virol 140, 1577–1587.[CrossRef]
    [Google Scholar]
  41. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Soh, Y. M. M. ( 2000; ). Investigation of viral movement in plants. MSc thesis, Department of Biological Sciences, National University of Singapore.
  43. 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.[CrossRef]
    [Google Scholar]
  44. Spirin, A. S. ( 1994; ). Storage of messenger RNA in eukaryotes: envelopment with protein, translational barrier at 5′ side, or conformational masking by 3′ side? Mol Reprod Dev 38, 107–117.[CrossRef]
    [Google Scholar]
  45. Spitsin, S., Steplewski, K., Fleysh, N., Belanger, H., Mikheeva, T., Shivprasad, S., Dawson, W., Koprowski, H. & Yusibov, V. ( 1999; ). Expression of alfalfa mosaic virus coat protein in tobacco mosaic virus (TMV) deficient in the production of its native coat protein supports long-distance movement of a chimeric TMV. Proc Natl Acad Sci U S A 96, 2549–2553.[CrossRef]
    [Google Scholar]
  46. Taliansky, M. E., de Jager, C. P., Wellink, J., van Lent, J. W. M. & Goldbach, R. W. ( 1993; ). Defective cell-to-cell movement of cowpea mosaic virus mutant N123 is efficiently complemented by sunn-hemp mosaic virus. J Gen Virol 74, 1895–1901.[CrossRef]
    [Google Scholar]
  47. 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]
  48. Verchot-Lubicz, J. ( 2005; ). A new cell-to-cell transport model for potexviruses. Mol Plant Microbe Interact 18, 283–290.[CrossRef]
    [Google Scholar]
  49. Verwoerd, T. C., Dekker, B. M. M. & Hoekema, A. ( 1989; ). A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17, 2362–2364.[CrossRef]
    [Google Scholar]
  50. Wong, S. M., Chng, C. G., Lee, Y. H., Tan, K. & Zettler, F. W. ( 1994; ). Incidence of cymbidium mosaic and odontoglossum ringspot viruses and their significance in orchid cultivation in Singapore. Crop Prot 13, 235–239.[CrossRef]
    [Google Scholar]
  51. Wong, S. M., Mahtani, P. H., Lee, K. C., Yu, H. H., Tan, Y., Neo, K. K., Chan, Y., Wu, M. & Chng, C. G. ( 1997; ). Cymbidium mosaic potexvirus RNA: complete nucleotide sequence and phylogenetic analysis. Arch Virol 142, 383–391.[CrossRef]
    [Google Scholar]
  52. Yu, H. H. ( 1999; ). Molecular manipulation of two orchid viruses. PhD thesis, Department of Biological Sciences, National University of Singapore.
  53. Yu, H. H. & Wong, S. M. ( 1998a; ). A DNA clone encoding the full-length infectious genome of odontoglossum ringspot tobamovirus and mutagenesis of its coat protein gene. Arch Virol 143, 163–171.[CrossRef]
    [Google Scholar]
  54. Yu, H. H. & Wong, S. M. ( 1998b; ). Synthesis of biologically active cDNA clones of cymbidium mosaic potexvirus using a population cloning strategy. Arch Virol 143, 1617–1620.[CrossRef]
    [Google Scholar]
  55. Ziegler-Graff, 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.[CrossRef]
    [Google Scholar]
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vol. , part 5, pp. 1543 – 1553

Screening and confirmation of putative transgenic lines expressing CymMV TGB1 and CymMV CP, ORSV MP and ORSV CP [PDF](977 KB)



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