1887

Abstract

Different models have been proposed for the nature of the potexvirus transport form that moves from cell to cell over the infected plant: (i) genomic RNA moves as native virions; or (ii) -assembled non-virion ribonucleoprotein (RNP) complexes consisting of viral RNA, coat protein (CP) and movement protein (MP), termed TGBp1, serve as the transport form . As the structure of these RNPs has not been elucidated, the products assembled from potato virus X (PVX) RNA, CP and TGBp1 were characterized. The complexes appeared as single-tailed particles (STPs) with a helical, head-like structure composed of CP subunits located at the 5′-proximal region of PVX RNA; the TGBp1 was bound to the terminal CP molecules of the head. Remarkably, no particular non-virion RNP complexes were observed. These data suggest that the CP–RNA interactions resulting in head formation prevailed over TGBp1–RNA binding upon STP assembly from RNA, CP and TGBp1. STPs could be assembled from the 5′ end of PVX RNA and CP in the absence of TGBp1. The translational ability of STPs was characterized in a cell-free translation system. STPs lacking TGBp1 were entirely non-translatable; however, they were rendered translatable by binding of TGBp1 to the end of the head. It is suggested that the RNA-mediated assembly of STPs proceeds via two steps. Firstly, non-translatable CP–RNA STPs are produced, due to encapsidation of the 5′-terminal region. Secondly, the TGBp1 molecules bind to the end of a polar head, resulting in conversion of the STPs into a translatable form.

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2006-09-01
2019-11-12
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References

  1. AbouHaidar, M. G. & Erickson, J. W. ( 1985; ). Structure and in vitro assembly of papaya mosaic virus. In Molecular Plant Virology, vol. 1, pp. 85–121. Edited by J. W. Davies. Boca Raton, FL: CRC Press.
  2. Allison, A. V. & Shalla, T. A. ( 1974; ). The ultrastructure of local lesions induced by potato virus X: a sequence of cytological events in the course of infection. Phytopathology 64, 784–793.[CrossRef]
    [Google Scholar]
  3. Atabekov, J. G., Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V. & Poljakov, V. Yu. ( 2000; ). The movement protein-triggered in situ conversion of potato virus X virion RNA from a nontranslatable into a translatable form. Virology 271, 259–263.[CrossRef]
    [Google Scholar]
  4. Batten, J. S., Yoshinari, S. & Hemenway, C. ( 2003; ). Potato virus X: a model system for virus replication, movement and gene expression. Mol Plant Pathol 4, 125–131.[CrossRef]
    [Google Scholar]
  5. 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]
  6. Dementjeva, S. P., Novikov, V. K. & Atabekov, J. G. ( 1970; ). Immunochemical studies of potato virus X protein. Biologicheskie nauki 8, 92–101 (in Russian).
    [Google Scholar]
  7. Goodman, R. M., Horne, R. W. & Hobart, J. M. ( 1975; ). Reconstitution of potato virus X in vitro. II. Characterization of the reconstituted product. Virology 68, 299–308.[CrossRef]
    [Google Scholar]
  8. Howard, A. R., Heppler, M. L., Ju, H.-J., Krishnamurthy, K., Payton, M. E. & Verchot-Lubicz, J. ( 2004; ). Potato virus X TGBp1 induces plasmodesmata gating and moves between cells in several host species whereas CP moves only in N. benthamiana leaves. Virology 328, 185–197.[CrossRef]
    [Google Scholar]
  9. Huisman, M. J., Linthorst, H. J. M., Ju, H.-J., Bol, J. F. & Cornelissen, B. J. C. ( 1988; ). The complete nucleotide sequence of potato virus X and its homologies at the amino acid level with various plus-stranded RNA viruses. J Gen Virol 69, 1789–1798.[CrossRef]
    [Google Scholar]
  10. 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]
  11. Kaftanova, A. S., Kiselev, N. A., Novikov, V. K. & Atabekov, J. G. ( 1975; ). Structure of products of protein reassembly and reconstruction of potato virus X. Virology 67, 283–287.[CrossRef]
    [Google Scholar]
  12. Kalinina, N. O., Fedorkin, O. V., Samuilova, O. V., Maiss, E., Korpela, T., Morozov, S. Yu. & Atabekov, J. G. ( 1996; ). Expression and biochemical analyses of the recombinant potato virus X 25K movement protein. FEBS Lett 397, 75–78.[CrossRef]
    [Google Scholar]
  13. Kalinina, N. O., Rakitina, D. A., 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]
  14. Karpova, O. V., Ivanov, K. I., Rodionova, N. P., Dorokhov, Yu. L. & Atabekov, J. G. ( 1997; ). Nontranslatability and dissimilar behavior in plants and protoplasts of viral RNA and movement protein complexes formed in vitro. Virology 230, 11–21.[CrossRef]
    [Google Scholar]
  15. Kim, S. H., Kalinina, N. O., Andreev, I., Ryabov, E. V., Fitzgerald, A. G., Taliansky, M. E. & Palukaitis, P. ( 2004; ). The C-terminal 33 amino acids of the cucumber mosaic virus 3a protein affect virus movement, RNA binding and inhibition of infection and translation. J Gen Virol 85, 221–230.[CrossRef]
    [Google Scholar]
  16. Kiselyova, O. I., Yaminsky, I. V., Karger, E. M., Frolova, O. Yu., Dorokhov, Y. L. & Atabekov, J. G. ( 2001; ). Visualization by atomic force microscopy of tobacco mosaic virus protein–RNA complexes formed in vitro. J Gen Virol 82, 1503–1508.
    [Google Scholar]
  17. Kiselyova, O. I., Yaminsky, I. V., Karpova, O. V., Rodionova, N. P., Kozlovsky, S. V., Arkhipenko, M. V. & Atabekov, J. G. ( 2003; ). AFM study of potato virus X disassembly induced by movement protein. J Mol Biol 332, 321–325.[CrossRef]
    [Google Scholar]
  18. Koenig, R., Stegemann, M. E., Franksen, H. & Paul, H. L. ( 1970; ). Protein subunits in the potato virus X group. Determination of the molecular weights by polyacrylamide electrophoresis. Biochem Biophys Acta 207, 184–189.
    [Google Scholar]
  19. Kuznetsov, Y. G., Daijogo, S., Zhou, J., Semler, B. L. & McPherson, A. ( 2005; ). Atomic force microscopy analysis of icosahedral virus RNA. J Mol Biol 347, 41–52.[CrossRef]
    [Google Scholar]
  20. Kwon, S.-J., Park, M.-R., Kim, K.-W., Plante, C. A., Hemenway, C. L. & Kim, K.-H. ( 2005; ). cis-Acting sequences required for coat protein binding and in vitro assembly of Potato virus X. Virology 334, 83–97.[CrossRef]
    [Google Scholar]
  21. Lok, S. & AbouHaidar, M. G. ( 1986; ). The nucleotide sequence of the 5′ end of papaya mosaic virus RNA: site of in vitro assembly initiation. Virology 153, 289–296.[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. 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]
  25. Miki, T. & Knight, C. A. ( 1968; ). The protein subunit of potato virus X. Virology 36, 168–173.[CrossRef]
    [Google Scholar]
  26. 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]
  27. Morozov, S. Yu., Solovyev, A. G., Kalinina, N. O., Fedorkin, O. N., Samuilova, O. V., Schiemann, J. & Atabekov, J. G. ( 1999; ). Evidence for two nonoverlapping functional domains in potato virus X 25K movement protein. Virology 260, 55–63.[CrossRef]
    [Google Scholar]
  28. Novikov, V. K., Kimaev, V. Z. & Atabekov, J. G. ( 1972; ). Reconstitution of the nucleoprotein of potato virus X. Dokl Akad Nauk SSSR 204, 1259–1262 (in Russian).
    [Google Scholar]
  29. Nurkiyanova, K. M., Ryabov, E. V., Kalinina, N. O., Fan, Y., Andreev, I., Fitzgerald, A. G., Palukaitis, P. & Taliansky, M. ( 2001; ). Umbravirus-encoded movement protein induces tubule formation on the surface of protoplasts and binds RNA incompletely and non-cooperatively. J Gen Virol 82, 2579–2588.
    [Google Scholar]
  30. Oparka, K. J., Roberts, A. G., Roberts, I. M., Prior, D. A. M. & Santa Cruz, S. ( 1996; ). Viral coat protein is targeted to, but does not gate, plasmodesmata during cell-to-cell movement of potato virus X. Plant J 10, 805–813.[CrossRef]
    [Google Scholar]
  31. Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V., Zayakina, O. V., Arkhipenko, M. V. & Atabekov, J. G. ( 2003; ). Linear remodeling of helical virus by movement protein binding. J Mol Biol 333, 565–572.[CrossRef]
    [Google Scholar]
  32. Santa Cruz, S., Roberts, A. G., Prior, D. A. M., Chapman, S. & Oparka, K. J. ( 1998; ). Cell-to-cell and phloem-mediated transport of potato virus X: the role of virions. Plant Cell 10, 495–510.[CrossRef]
    [Google Scholar]
  33. Shlyakhtenko, L. S., Potaman, V. N., Sinden, R. R. & Lyubchenko, Y. L. ( 1998; ). Structure and dynamics of supercoil-stabilized DNA cruciforms. J Mol Biol 280, 61–72.[CrossRef]
    [Google Scholar]
  34. Sit, T. L., Leclerc, D. & AbouHaidar, M. G. ( 1994; ). A minimal 5′ sequence for in vitro initiation of papaya mosaic potexvirus assembly. Virology 199, 238–242.[CrossRef]
    [Google Scholar]
  35. Skryabin, K. G., Morozov, S. Yu., Kraev, A. S., Rozanov, M. M., Chernov, B. K., Lukasheva, L. I. & Atabekov, J. G. ( 1988; ). Conserved and variable elements in RNA genomes of potexviruses. FEBS Lett 240, 33–40.[CrossRef]
    [Google Scholar]
  36. Tollin, P. & Wilson, H. R. ( 1988; ). Particle structure. In The Plant Viruses: the Filamentous Plant Viruses, vol. 4, pp. 51–83. Edited by R. C. Milne. New York: Plenum.
  37. 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]
  38. Verchot-Lubicz, J. ( 2005; ). A new cell-to-cell transport model for potexviruses. Mol Plant Microbe Interact 18, 283–290.[CrossRef]
    [Google Scholar]
  39. 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]
  40. 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]
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