1887

Abstract

The genomes of umbraviruses differ from those of most other viruses in that they do not encode a coat protein, and thus no virus particles are formed in infected plants. Protection of umbraviral RNA outside the host plant, during vector transmission, utilizes the coat protein of an assistor luteovirus, but this review focuses on the mechanisms that compensate for the lack of a coat protein in processes within the host plant. As well as an RNA-dependent RNA polymerase, umbravirus genomes encode two other proteins from almost completely overlapping open reading frames. One of these is a cell-to-cell movement protein that can mediate the transport of homologous and heterologous viral RNAs through plasmodesmata without the participation of a coat protein. The other, the ORF3 protein, binds to viral RNA to form filamentous ribonucleoprotein particles that have elements of helical structure. It serves to stabilize the RNA and facilitates its transport through the vascular system of the plant. It may also be involved in protection of the viral RNA from the plant's defensive RNA-silencing response, although it is not a suppressor of silencing. The ORF3 protein also enters the cell nucleus, specifically targeting the nucleolus. Although the function of this localization is unknown, the ORF3 protein may provide a valuable tool for investigating plant nucleolar function.

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2003-08-01
2019-12-07
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References

  1. Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Smith, T. H. & Vance, V. B. ( 1998; ). A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95, 13079–13084.[CrossRef]
    [Google Scholar]
  2. 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 of trichome cells of Nicotiana clevelandii. Virology 216, 197–201.[CrossRef]
    [Google Scholar]
  3. Atkins, D., Hull, R., Wells, B., Roberts, K., Moore, P. & Beachy, R. N. ( 1991; ). The tobacco mosaic virus 30K movement protein in transgenic tobacco is localized to plasmodesmata. J Gen Virol 72, 209–211.[CrossRef]
    [Google Scholar]
  4. Beven, A. F., Lee, R., Razaz, M., Leader, D. J., Brown, J. W. & Shaw, P. J. ( 1996; ). The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J Cell Sci 109, 1241–1251.
    [Google Scholar]
  5. Blok, V. C., Ziegler, A., Robinson, D. J. & Murant, A. F. ( 1994; ). Sequences of ten variants of the satellite-like RNA-3 of groundnut rosette virus. Virology 202, 25–32.[CrossRef]
    [Google Scholar]
  6. Boyko, V., Ferralli, J., Ashby, J., Schellenbaum, P. & Heinlein, M. ( 2000; ). Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2, 826–832.[CrossRef]
    [Google Scholar]
  7. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W. & Baulcombe, D. C. ( 1998; ). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17, 6739–6746.[CrossRef]
    [Google Scholar]
  8. Cadman, C. H. ( 1962; ). Evidence for association of tobacco rattle virus nucleic acid with a cell component. Nature 193, 49–52.[CrossRef]
    [Google Scholar]
  9. Canto, T. & Palukaitis, P. ( 1999; ). Are tubules generated by the 3a protein necessary for cucumber mosaic virus movement? Mol Plant–Microbe Interact 12, 985–993.[CrossRef]
    [Google Scholar]
  10. Canto, T., Prior, D. A. M., Hellwald, K.-H., Oparka, K. J. & Palukaitis, P. ( 1997; ). Characterization of cucumber mosaic virus. IV. Movement protein and coat protein are both essential for cell-to-cell movement of cucumber mosaic virus. Virology 237, 237–248.[CrossRef]
    [Google Scholar]
  11. Carmo-Fonseca, M., Mendes-Soares, L. & Campos, I. ( 2000; ). To be or not to be in the nucleolus. Nat Cell Biol 2, E107–E112.[CrossRef]
    [Google Scholar]
  12. Carrington, J. C. ( 2000; ). RNA silencing: moving targets. Nature 408, 150–151.[CrossRef]
    [Google Scholar]
  13. 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]
  14. Chen, D. & Huang, S. ( 2001; ). Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J Cell Biol 153, 169–176.[CrossRef]
    [Google Scholar]
  15. Chen, H., Wurm, T., Britton, P., Brooks, G. & Hiscox, J. A. ( 2002; ). Interaction of the coronavirus nucleoprotein with nucleolar antigens and the host cell. J Virol 76, 5233–5250.[CrossRef]
    [Google Scholar]
  16. Citovsky, V. & Zambryski, P. ( 1991; ). How do plant virus nucleic acids move through intercellular connections? Bioessays 13, 373–379.[CrossRef]
    [Google Scholar]
  17. Cockbain, A. J., Jones, P. & Woods, R. D. ( 1986; ). Transmission characteristics and some other properties of bean yellow vein-banding virus, and its association with pea enation mosaic virus. Ann Appl Biol 108, 59–69.[CrossRef]
    [Google Scholar]
  18. Cockell, M. M. & Gasser, S. M. ( 1999; ). The nucleolus: nucleolar space for RENT. Curr Biol 9, R575–R576.[CrossRef]
    [Google Scholar]
  19. Demler, S. A., Rucker, D. G. & de Zoeten, G. A. ( 1993; ). The chimeric nature of the genome of pea enation mosaic virus: the independent replication of RNA-2. J Gen Virol 74, 1–14.[CrossRef]
    [Google Scholar]
  20. Demler, S. A., Borkhsenious, O. N., Rucker, D. G. & de Zoeten, G. A. ( 1994; ). Assessment of the autonomy of replicative and structural functions encoded by the luteo-phase of pea enation mosaic virus. J Gen Virol 75, 997–1007.[CrossRef]
    [Google Scholar]
  21. Demler, S. A., Rucker, D. G., de Zoeten, G. A., Ziegler, A., Robinson, D. J. & Murant, A. F. ( 1996a; ). The satellite RNAs associated with the groundnut rosette disease complex and pea enation mosaic virus: sequence similarities and ability of each other's helper virus to support their replication. J Gen Virol 77, 2847–2855.[CrossRef]
    [Google Scholar]
  22. Demler, S. A., de Zoeten, G. A., Adam, G. & Harris, K. F. ( 1996b; ). Pea enation mosaic enamovirus: properties and aphid transmission. In The Plant Viruses, Polyhedral Virions and Bipartite RNA Genomes, vol. 5, pp. 303–344. Edited by B. D. Harrison & A. F. Murant. New York: Plenum Press.
  23. Falk, B. W., Duffus, J. E. & Morris, T. J. ( 1979a; ). Transmission, host range, and serological properties of the viruses that cause lettuce speckles disease. Phytopathology 69, 612–617.[CrossRef]
    [Google Scholar]
  24. Falk, B. W., Morris, T. J. & Duffus, J. E. ( 1979b; ). Unstable infectivity and sedimentable ds-RNA associated with lettuce speckles mottle virus. Virology 96, 239–248.[CrossRef]
    [Google Scholar]
  25. García-Sastre, A. ( 2001; ). Inhibition of interferon-mediated antiviral responses by influenza A virus and other negative strand RNA viruses. Virology 279, 375–384.[CrossRef]
    [Google Scholar]
  26. Gibbs, M. G., Cooper, J. I. & Waterhouse, P. M. ( 1996; ). The genome organization and affinities of an Australian isolate of carrot mottle umbravirus. Virology 224, 310–313.[CrossRef]
    [Google Scholar]
  27. Halk, E. L., Robinson, D. J. & Murant, A. F. ( 1979; ). Molecular weight of the infectious RNA from leaves infected with carrot mottle virus. J Gen Virol 45, 383–388.[CrossRef]
    [Google Scholar]
  28. Heinlein, M., Epel, B. L., Padgett, H. S. & Beachy, R. N. ( 1995; ). Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270, 1983–1985.[CrossRef]
    [Google Scholar]
  29. Hiscox, J. A. ( 2002; ). The nucleolus – a gateway to viral infection? Arch Virol 147, 1077–1089.[CrossRef]
    [Google Scholar]
  30. Jansen, K. A. J., Wolfs, C. J. A. M., Lohuis, H., Goldbach, R. W. & Verduin, B. J. M. ( 1998; ). Characterization of the brome mosaic virus movement protein expressed in E. coli. Virology 242, 387–394.[CrossRef]
    [Google Scholar]
  31. Karpova, O. V., Ivanov, K. I., Rodionova, N. P., Dorokhov, Yu. L. & Atabekov, J. G. ( 1997; ). Nontranslatability and dissimilar behaviour in plants and protoplasts of viral RNA and movement protein complexes formed in vitro. Virology 230, 11–21.[CrossRef]
    [Google Scholar]
  32. Kasschau, K. D. & Carrington, J. C. ( 1998; ). A counterdefensive strategy of plant viruses: suppression of post-transcriptional gene silencing. Cell 95, 461–470.[CrossRef]
    [Google Scholar]
  33. Kasteel, D. T. J., Wellink, J., Goldbach, R. W. & van Lent, J. W. M. ( 1997; ). Isolation and characterization of tubular structures of cowpea mosaic virus. J Gen Virol 78, 3167–3170.
    [Google Scholar]
  34. Koonin, E. V. & Dolja, V. V. ( 1993; ). Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28, 375–430.[CrossRef]
    [Google Scholar]
  35. Lamond, A. I. & Earnshaw, W. C. ( 1998; ). Structure and function in the nucleus. Science 280, 547–553.[CrossRef]
    [Google Scholar]
  36. Langenberg, W. G. & Zhang, L. ( 1997; ). Immunocytology shows the presence of tobacco etch virus P3 protein in nuclear inclusions. J Struct Biol 118, 243–247.[CrossRef]
    [Google Scholar]
  37. 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 triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol Plant–Microbe Interact 11, 801–814.[CrossRef]
    [Google Scholar]
  38. Mackenzie, D. J. & Tremaine, J. H. ( 1988; ). Ultrastructural location of non-structural protein 3A of cucumber mosaic virus in infected tissue using monoclonal antibodies to a cloned chimeric fusion protein. J Gen Virol 69, 2387–2395.[CrossRef]
    [Google Scholar]
  39. McLean, B. G., Zupan, J. & Zambryski, P. ( 1995; ). Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7, 2101–2114.[CrossRef]
    [Google Scholar]
  40. Mo, X.-H., Qin, X.-Y., Wu, J., Yang, C., Wu, J.-Y., Duan, Y.-Q., Li, T.-F. & Chen, H.-R. ( 2003; ). Complete nucleotide sequence and genome organization of a Chinese isolate of tobacco bushy top virus. Arch Virol 148, 389–397.[CrossRef]
    [Google Scholar]
  41. Murant, A. F. ( 1990; ). Dependence of groundnut rosette virus on its satellite RNA as well as on groundnut rosette assistor luteovirus for transmission by Aphis craccivora. J Gen Virol 71, 2163–2166.[CrossRef]
    [Google Scholar]
  42. Murant, A. F. ( 1993; ). Complexes of transmission-dependent and helper viruses. In Diagnosis of Plant Virus Diseases, pp. 333–357. Edited by R. E. F. Matthews. Boca Raton: CRC Press.
  43. Murant, A. F. & Kumar, I. K. ( 1990; ). Different variants of the satellite RNA of groundnut rosette virus are responsible for the chlorotic and green forms of groundnut rosette disease. Ann Appl Biol 117, 85–92.[CrossRef]
    [Google Scholar]
  44. Murant, A. F., Goold, R. A., Roberts, I. M. & Cathro, J. ( 1969; ). Carrot mottle – a persistent aphid-borne virus with unusual properties and particles. J Gen Virol 4, 329–341.[CrossRef]
    [Google Scholar]
  45. Murant, A. F., Roberts, I. M. & Goold, R. A. ( 1973; ). Cytopathological changes and extractable infectivity in Nicotiana clevelandii leaves infected with carrot mottle virus. J Gen Virol 21, 269–283.[CrossRef]
    [Google Scholar]
  46. Murant, A. F., Waterhouse, P. M., Raschké, J. H. & Robinson, D. J. ( 1985; ). Carrot red leaf and carrot mottle viruses: observations on the composition of the particles in single and mixed infections. J Gen Virol 66, 1575–1579.[CrossRef]
    [Google Scholar]
  47. Murant, A. F., Rajeshwari, R., Robinson, D. J. & Raschké, J. H. ( 1988; ). A satellite RNA of groundnut rosette virus that is largely responsible for symptoms of groundnut rosette disease. J Gen Virol 69, 1479–1486.[CrossRef]
    [Google Scholar]
  48. Naidu, R. A., Bottenberg, H., Subrahmanyam, P., Kimmins, F. M., Robinson, D. J. & Thresh, J. M. ( 1998; ). Epidemiology of groundnut rosette virus disease: current status and future research needs. Ann Appl Biol 132, 525–548.[CrossRef]
    [Google Scholar]
  49. Nakielny, S. & Dreyfuss, G. ( 1999; ). Transport of proteins and RNAs in and out of the nucleus. Cell 99, 677–690.[CrossRef]
    [Google Scholar]
  50. Nelson, R. S. & van Bel, A. J. E. ( 1998; ). The mystery of virus trafficking into, through and out of the vascular tissue. Progr Bot 59, 476–533.
    [Google Scholar]
  51. Nurkiyanova, K. M., Ryabov, E. V., Kalinina, N. O., Fan, Y., Andreev, I., Fitzgerald, A. G., Palukaitis, P. & Taliansky, M. E. ( 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]
  52. Olson, M. O. J., Dundr, M. & Szebeni, A. ( 2000; ). The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol 10, 189–196.[CrossRef]
    [Google Scholar]
  53. Oparka, K. J. & Turgeon, R. ( 1999; ). Sieve elements and companion cells – traffic control centers of the phloem. Plant Cell 11, 739–750.
    [Google Scholar]
  54. Pederson, T. ( 1998; ). The plurifunctional nucleolus. Nucleic Acids Res 26, 3871–3876.[CrossRef]
    [Google Scholar]
  55. Perbal, M.-C., Thomas, C. L. & Maule, A. J. ( 1993; ). Cauliflower mosaic virus gene I product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195, 281–285.[CrossRef]
    [Google Scholar]
  56. Portela, A. & Digard, P. ( 2002; ). The influenza virus nucleoprotein: a functional RNA-binding protein pivotal to virus replication. J Gen Virol 83, 723–734.
    [Google Scholar]
  57. Reddy, D. V. R., Murant, A. F., Raschké, J. H., Mayo, M. A. & Ansa, O. A. ( 1985; ). Properties and partial purification of infective material from plants containing groundnut rosette virus. Ann Appl Biol 107, 65–78.[CrossRef]
    [Google Scholar]
  58. Robinson, D. J. & Murant, A. F. ( 1999; ). Umbraviruses. In Encyclopedia of Virology, pp. 1855–1859. Edited by A. Granoff & R. G. Webster. New York: Academic Press.
  59. Robinson, D. J., Ryabov, E. V., Raj, S. K., Roberts, I. M. & Taliansky, M. E. ( 1999; ). Satellite RNA is essential for encapsidation of groundnut rosette umbravirus RNA by groundnut rosette assistor luteovirus coat protein. Virology 254, 105–114.[CrossRef]
    [Google Scholar]
  60. Rojas, M. R., Jiang, H., Salati, R., Xoconostle-Cazares, B., Sudarshana, M. R., Lucas, W. J. & Gilbertson, R. L. ( 2001; ). Functional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus. Virology 291, 110–125.[CrossRef]
    [Google Scholar]
  61. Ryabov, E. V., Oparka, K. J., Santa Cruz, S., Robinson, D. J. & Taliansky, M. E. ( 1998; ). Intracellular location of two groundnut rosette umbravirus proteins delivered by PVX and TMV vectors. Virology 242, 303–313.[CrossRef]
    [Google Scholar]
  62. 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]
  63. 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]
  64. Ryabov, E. V., Robinson, D. J. & Taliansky, M. E. ( 2001; ). Umbravirus-encoded proteins both stabilize heterologous viral RNA and mediate its systemic movement in some plant species. Virology 288, 391–400.[CrossRef]
    [Google Scholar]
  65. Salvatore, M., Basler, C. F., Parisien, J.-P., Horvath, C. M., Bourmakina, S., Zheng, H., Muster, T., Palese, P. & García-Sastre, A. ( 2002; ). Effects of influenza A virus NS1 protein on protein expression: the NS1 protein enhances translation and is not required for shutoff of host protein synthesis. J Virol 76, 1206–1212.[CrossRef]
    [Google Scholar]
  66. Santa Cruz, S. ( 1999; ). Perspective: phloem transport of viruses and macromolecules – what goes in must come out. Trends Microbiol 7, 237–241.[CrossRef]
    [Google Scholar]
  67. 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]
  68. Scholthof, H. B., Scholthof, K.-B. G., Kikkert, M. & Jackson, A. O. ( 1995; ). Tomato bushy stunt virus spread is regulated by two nested genes that function in cell-to-cell movement and host-dependent systemic invasion. Virology 213, 425–438.[CrossRef]
    [Google Scholar]
  69. Smith, K. M. ( 1945; ). Tobacco rosette: a complex virus disease. Parasitology 36, 21–24.
    [Google Scholar]
  70. Swanson, M., Barker, H. & MacFarlane, S. A. ( 2002; ). Rapid vascular movement of tobraviruses does not require coat protein: evidence from mutated and wild-type viruses. Ann Appl Biol 141, 259–266.[CrossRef]
    [Google Scholar]
  71. Taliansky, M. E. & Robinson, D. J. ( 1997; ). Trans-acting untranslated elements of groundnut rosette virus satellite RNA are involved in symptom production. J Gen Virol 78, 1277–1285.
    [Google Scholar]
  72. Taliansky, M. E., Robinson, D. J. & Murant, A. F. ( 1996; ). Complete nucleotide sequence and organization of the RNA genome of groundnut rosette umbravirus. J Gen Virol 77, 2335–2345.[CrossRef]
    [Google Scholar]
  73. Taliansky, M. E., Robinson, D. J. & Murant, A. F. ( 2000; ). Groundnut rosette disease virus complex: biology and molecular biology. Adv Virus Res 55, 357–400.
    [Google Scholar]
  74. Taliansky, M., Roberts, I. M., Kalinina, N., Ryabov, E. V., Raj, S. K., Robinson, D. J. & Oparka, K. J. ( 2003; ). An umbraviral protein, involved in long-distance RNA movement, binds viral RNA and forms unique, protective ribonucleoprotein complexes. J Virol 77, 3031–3040.[CrossRef]
    [Google Scholar]
  75. Vance, V. B. & Vaucheret, H. ( 2001; ). RNA silencing in plants: defense and counterdefense. Science 292, 2277–2280.[CrossRef]
    [Google Scholar]
  76. Van Lent, J., Wellink, J. & Goldbach, R. ( 1990; ). Evidence for the involvement of the 48K and 58K proteins in the intercellular movement of cowpea mosaic virus. J Gen Virol 71, 219–223.[CrossRef]
    [Google Scholar]
  77. Van Lent, J., Storms, M., van der Meer, F., Wellink, J. & Goldbach, R. ( 1991; ). Tubular structures involved in movement of cowpea mosaic virus are also formed in infected cowpea protoplasts. J Gen Virol 72, 2615–2623.[CrossRef]
    [Google Scholar]
  78. Voinnet, O. ( 2001; ). RNA silencing as a plant immune system against viruses. Trends Genet 17, 449–459.[CrossRef]
    [Google Scholar]
  79. Voinnet, O., Pinto, Y. M. & Baulcombe, D. C. ( 1999; ). Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses. Proc Natl Acad Sci U S A 96, 14147–14152.[CrossRef]
    [Google Scholar]
  80. 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]
  81. Waterhouse, P. M. & Murant, A. F. ( 1983; ). Further evidence on the nature of the dependence of carrot mottle virus on carrot red leaf virus for transmission by aphids. Ann Appl Biol 103, 455–464.[CrossRef]
    [Google Scholar]
  82. Wellink, J. & van Kammen, A. ( 1989; ). Cell-to-cell transport of cowpea mosaic virus requires both the 58K/48K proteins and the capsid proteins. J Gen Virol 70, 2279–2286.[CrossRef]
    [Google Scholar]
  83. Wen, W., Meinkoth, J. L., Tsien, R. Y. & Taylor, S. S. ( 1995; ). Identification of a signal for rapid export of proteins from the nucleus. Cell 82, 463–473.[CrossRef]
    [Google Scholar]
  84. Wolf, S., Deom, C. M., Beachy, R. N. & Lucas, W. J. ( 1989; ). Movement protein of tobacco mosaic virus modifies plasmodesmata size exclusion limit. Science 246, 377–379.[CrossRef]
    [Google Scholar]
  85. Wootton, J. C. & Federhen, S. ( 1996; ). Analysis of compositionally biased regions in sequence database. Methods Enzymol 266, 554–571.
    [Google Scholar]
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