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Abstract

Capsids of numerous filamentous and rod-shaped plant viruses possess helical symmetry. In positive-stranded RNA viruses, helical capsids are typically composed of many identical subunits of the viral capsid protein (CP), encapsidating a molecule of viral genomic RNA. Current progress in structural studies of helical plant viruses has revealed differences between filamentous and rod-shaped viruses, both in structural folds of their CPs and in the interactions of CP molecules in their capsids. Many filamentous and rod-shaped viruses have functionally similar lateral inter-subunit contacts on the outer virion surface. Additionally, the extreme N-terminal CP region in filamentous viruses is intrinsically disordered. Taken together, the available data establish a link between the structural features of molecular interactions of CP molecules and the physical properties of helical virions ranging from rigidity to flexibility. Overall, the structure of helical plant viruses is significantly more labile than previously thought, often allowing structural transitions, remodelling and the existence of alternative structural forms of virions. These properties of virions are believed to be functionally significant at certain stages of the viral life cycle, such as during translational activation and cell-to-cell transport. In this review, we discuss structural and functional features of filamentous and rod-shaped virions, highlight their shared features and differences, and lay emphasis on the relationships between the molecular structure of viral capsids and their properties including virion shape, lability and capability of structural remodelling.

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2016-08-01
2021-10-24
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References

  1. Agirrezabala X., Méndez-López E., Lasso G., Sánchez-Pina M. A., Aranda M., Valle M. 2015; The near-atomic cryoEM structure of a flexible filamentous plant virus shows homology of its coat protein with nucleoproteins of animal viruses. eLife 4:e11795 [View Article][PubMed]
    [Google Scholar]
  2. Agranovsky A. A., Lesemann D. E., Maiss E., Hull R., Atabekov J. G. 1995; "Rattlesnake" structure of a filamentous plant RNA virus built of two capsid proteins. Proc Natl Acad Sci U S A 92:2470–2473[PubMed] [CrossRef]
    [Google Scholar]
  3. Albertini A. A., Wernimont A. K., Muziol T., Ravelli R. B., Clapier C. R., Schoehn G., Weissenhorn W., Ruigrok R. W. 2006; Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313:360–363 [View Article][PubMed]
    [Google Scholar]
  4. Alzhanova D. V., Hagiwara Y., Peremyslov V. V., Dolja V. V. 2000; Genetic analysis of the cell-to-cell movement of beet yellows closterovirus. Virology 268:192–200 [View Article][PubMed]
    [Google Scholar]
  5. Alzhanova D. V., Napuli A. J., Creamer R., Dolja V. V. 2001; Cell-to-cell movement and assembly of a plant closterovirus: roles for the capsid proteins and Hsp70 homolog. EMBO J 20:6997–7007 [View Article][PubMed]
    [Google Scholar]
  6. Arranz R., Coloma R., Chichón F. J., Conesa J. J., Carrascosa J. L., Valpuesta J. M., Ortín J., Martín-Benito J. 2012; The structure of native influenza virion ribonucleoproteins. Science 338:1634–1637 [View Article][PubMed]
    [Google Scholar]
  7. Atabekov J. G., Rodionova N. P., Karpova O. V., Kozlovsky S. V., Poljakov V. Y. 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 [View Article][PubMed]
    [Google Scholar]
  8. Atabekov J. G., Rodionova N. P., Karpova O. V., Kozlovsky S. V., Novikov V. K., Arkhipenko M. V. 2001; Translational activation of encapsidated potato virus X RNA by coat protein phosphorylation. Virology 286:466–474 [View Article][PubMed]
    [Google Scholar]
  9. Atreya P. L., Atreya C. D., Pirone T. P. 1991; Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc Natl Acad Sci U S A 88:7887–7891[PubMed] [CrossRef]
    [Google Scholar]
  10. Baratova L. A., Grebenshchikov N. I., Dobrov E. N., Gedrovich A. V., Kashirin I. A., Shishkov A. V., Efimov A. V., Järvekülg L., Radavsky Y. L. et al. 1992; The organization of potato virus X coat proteins in virus particles studied by tritium planigraphy and model building. Virology 188:175–180 [View Article][PubMed]
    [Google Scholar]
  11. Baratova L. A., Fedorova N. V., Dobrov E. N., Lukashina E. V., Kharlanov A. N., Nasonov V. V., Serebryakova M. V., Kozlovsky S. V., Zayakina O. V., Rodionova N. P. 2004; N-Terminal segment of potato virus X coat protein subunits is glycosylated and mediates formation of a bound water shell on the virion surface. Eur J Biochem 271:3136–3145 [View Article][PubMed]
    [Google Scholar]
  12. Betti C., Lico C., Maffi D., D'Angeli S., Altamura M. M., Benvenuto E., Faoro F., Baschieri S. 2012; Potato virus X movement in Nicotiana benthamiana: new details revealed by chimeric coat protein variants. Mol Plant Pathol 13:198–203 [View Article][PubMed]
    [Google Scholar]
  13. Bloomer A. C., Champness J. N., Bricogne G., Staden R., Klug A. 1978; Protein disk of tobacco mosaic virus at 2.8 A resolution showing the interactions within and between subunits. Nature 276:362–368 [View Article][PubMed]
    [Google Scholar]
  14. Booth T. F., Rabb M. J., Beniac D. R. 2013; How do filovirus filaments bend without breaking?. Trends Microbiol 21:583–593 [View Article][PubMed]
    [Google Scholar]
  15. Brakke M. K., Ball E. M., Langenberg W. G. 1988; A non-capsid protein associated with unencapsidated virus RNA in barley infected with barley stripe mosaic virus. J Gen Virol 69:481–491 [CrossRef]
    [Google Scholar]
  16. Caspar D. L., Klug A. 1962; Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27:1–24[PubMed] [CrossRef]
    [Google Scholar]
  17. Caspar D. L., Namba K. 1990; Switching in the self-assembly of tobacco mosaic virus. Adv Biophys 26:157–185[PubMed] [CrossRef]
    [Google Scholar]
  18. Champness J. N., Bloomer A. C., Bricogne G., Butler P. G., Klug A. 1976; The structure of the protein disk of tobacco mosaic virus to 5Å resolution. Nature 259:20–24 [View Article][PubMed]
    [Google Scholar]
  19. 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 [View Article][PubMed]
    [Google Scholar]
  20. Chung B. Y., Miller W. A., Atkins J. F., Firth A. E. 2008; An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 105:5897–5902 [View Article][PubMed]
    [Google Scholar]
  21. Citovsky V., Knorr D., Schuster G., Zambryski P. 1990; The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60:637–647 [View Article][PubMed]
    [Google Scholar]
  22. Citovsky V., Wong M. L., Shaw A. L., Prasad B. V., Zambryski P. 1992; Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397–411[PubMed] [CrossRef]
    [Google Scholar]
  23. Clare D. K., Orlova E. V. 2010; 4.6Å Cryo-EM reconstruction of tobacco mosaic virus from images recorded at 300 keV on a 4k × 4k CCD camera. J Struct Biol 171:303–308 [View Article][PubMed]
    [Google Scholar]
  24. Clare D. K., Pechnikova E. V., Skurat E. V., Makarov V. V., Sokolova O. S., Solovyev A. G., Orlova E. V. 2015; Novel inter-subunit contacts in barley stripe mosaic virus revealed by cryo-electron microscopy. Structure 23:1815–1826 [View Article][PubMed]
    [Google Scholar]
  25. DiMaio F., Chen C. C., Yu X., Frenz B., Hsu Y. H., Lin N. S., Egelman E. H. 2015; The molecular basis for flexibility in the flexible filamentous plant viruses. Nat Struct Mol Biol 22:642–644 [View Article][PubMed]
    [Google Scholar]
  26. Dolja V. V., Boyko V. P., Agranovsky A. A., Koonin E. V. 1991; Phylogeny of capsid proteins of rod-shaped and filamentous RNA plant viruses: two families with distinct patterns of sequence and probably structure conservation. Virology 184:79–86 [View Article][PubMed]
    [Google Scholar]
  27. Dolja V. V., Haldeman R., Robertson N. L., Dougherty W. G., Carrington J. C. 1994; Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13:1482–1491[PubMed]
    [Google Scholar]
  28. Dolja V. V., Haldeman-Cahill R., Montgomery A. E., Vandenbosch K. A., Carrington J. C. 1995; Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology 206:1007–1016 [View Article][PubMed]
    [Google Scholar]
  29. Dolja V. V. 2003; Beet yellows virus: the importance of being different. Mol Plant Pathol 4:91–98[PubMed] [CrossRef]
    [Google Scholar]
  30. Dolja V. V., Kreuze J. F., Valkonen J. P. 2006; Comparative and functional genomics of closteroviruses. Virus Res 117:38–51 [View Article][PubMed]
    [Google Scholar]
  31. Duff-Farrier C. R., Bailey A. M., Boonham N., Foster G. D. 2015; A pathogenicity determinant maps to the N-terminal coat protein region of the Pepino mosaic virus genome. Mol Plant Pathol 16:308–315 [View Article][PubMed]
    [Google Scholar]
  32. Esau K., Cronshaw J., Hoefert L. L. 1967; Relation of beet yellows virus to the phloem and to movement in the sieve tube. J Cell Biol 32:71–87[PubMed] [CrossRef]
    [Google Scholar]
  33. Fedorkin O., Solovyev A., Yelina N., Zamyatnin A., Zinovkin R., Mäkinen K., Schiemann J., Morozov S. Y. 2001; Cell-to-cell movement of potato virus X involves distinct functions of the coat protein. J Gen Virol 82:449–458 [View Article][PubMed]
    [Google Scholar]
  34. Fink A. L. 2005; Natively unfolded proteins. Curr Opin Struct Biol 15:35–41 [View Article][PubMed]
    [Google Scholar]
  35. Forster R. L., 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 [View Article][PubMed]
    [Google Scholar]
  36. Gabrenaite-Verkhovskaya R., Andreev I. A., Kalinina N. O., Torrance L., Taliansky M. E., Mäkinen K. 2008; Cylindrical inclusion protein of potato virus A is associated with a subpopulation of particles isolated from infected plants. J Gen Virol 89:829–838 [View Article][PubMed]
    [Google Scholar]
  37. Harrison S. C. 2007; Principles of Virus Structure. In Fields Virology, 5 edn. pp. 59–98 . Edited by Knipe D. M., Howley P. M. Philadelphia: Lippincott Williams & Wilkins;
    [Google Scholar]
  38. Heinlein M. 2015; Plant virus replication and movement. Virology 480:657–671 [View Article]
    [Google Scholar]
  39. Helgstrand C., Munshi S., Johnson J. E., Liljas L. 2004; The refined structure of Nudaurelia capensis ω virus reveals control elements for a T = 4 capsid maturation. Virology 318:192–203 [View Article][PubMed]
    [Google Scholar]
  40. 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 [View Article][PubMed]
    [Google Scholar]
  41. Hoefert L. L., Pinto R. L., Fail G. L. 1988; Ultrastructural effects of lettuce infectious yellows virus in Lactuca sativa L. J Ultrastruct Mol Struct Res 98:243–253 [View Article]
    [Google Scholar]
  42. Holmes K. C., Stubbs G. J., Mandelkow E., Gallwitz U. 1975; Structure of tobacco mosaic virus at 6.7 Å resolution. Nature 254:192–196 [View Article][PubMed]
    [Google Scholar]
  43. Jankowsky E., Gross C. H., Shuman S., Pyle A. M. 2001; Active disruption of an RNA–protein interaction by a DExH/D RNA helicase. Science 291:121–125 [View Article][PubMed]
    [Google Scholar]
  44. Kamtekar S., Hecht M. H. 1995; Protein Motifs. 7. The four-helix bundle: what determines a fold?. FASEB J 9:1013–1022[PubMed]
    [Google Scholar]
  45. Karpova O. V., Arkhipenko M. V., Zaiakina O. V., Nikitin N. A., Kiseleva O. I., Kozlovskiĭ S. V., Rodionova N. P., Atabekov I. G. 2006a; Translational regulation of potato virus X RNA-coat protein complexes: the key role of a coat protein N-terminal peptide. Mol Biol 40:703–710 [CrossRef]
    [Google Scholar]
  46. Karpova O. V., Zayakina O. V., Arkhipenko M. V., Sheval E. V., Kiselyova O. I., Poljakov V. Y., Yaminsky I. V., Rodionova N. P., Atabekov J. G. 2006b; Potato virus X RNA-mediated assembly of single-tailed ternary ‘coat protein-RNA-movement protein' complexes. J Gen Virol 87:2731–2740 [CrossRef]
    [Google Scholar]
  47. Kempers R., van Bel A. J. E. 1997; Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta 201:195–201 [View Article]
    [Google Scholar]
  48. Kendall A., McDonald M., Bian W., Bowles T., Baumgarten S. C., Shi J., Stewart P. L., Bullitt E., Gore D. et al. 2008; Structure of flexible filamentous plant viruses. J Virol 82:9546–9600 [View Article][PubMed]
    [Google Scholar]
  49. Kendall A., Williams D., Bian W., Stewart P. L., Stubbs G. 2013; Barley stripe mosaic virus: structure and relationship to the tobamoviruses. Virology 443:265–335 [View Article][PubMed]
    [Google Scholar]
  50. King A. M., Adams M. J., Carstens E. B., Lefkowitz E. J. 2012 Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses New York: Academic Press Elsevier;
    [Google Scholar]
  51. 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[PubMed] [CrossRef]
    [Google Scholar]
  52. Kiss Z. A., Medina V., Falk B. W. 2013; Crinivirus replication and host interactions. Front Microbiol 4:99 [View Article][PubMed]
    [Google Scholar]
  53. Lan P., Yeh W. B., Tsai C. W., Lin N. S. 2010; A unique glycine-rich motif at the N-terminal region of Bamboo mosaic virus coat protein is required for symptom expression. Mol Plant-Microbe Interact 23:903–914 [View Article][PubMed]
    [Google Scholar]
  54. Lecours K., Tremblay M. H., Gagné M. E., Gagné S. M., Leclerc D. 2006; Purification and biochemical characterization of a monomeric form of papaya mosaic potexvirus coat protein. Protein Expr Purif 47:273–280 [View Article][PubMed]
    [Google Scholar]
  55. Lee C. C., Ho Y. N., Hu R. H., Yen Y. T., Wang Z. C., Lee Y. C., Hsu Y. H., Meng M. 2011; The interaction between Bamboo mosaic virus replication protein and coat protein is critical for virus movement in plant hosts. J Virol 85:12022–12031 [View Article][PubMed]
    [Google Scholar]
  56. Lico C., Capuano F., Renzone G., Donini M., Marusic C., Scaloni A., Benvenuto E., Baschieri S. 2006; Peptide display on Potato virus X: molecular features of the coat protein-fused peptide affecting cell-to-cell and phloem movement of chimeric virus particles. J Gen Virol 87:3103–3112 [View Article][PubMed]
    [Google Scholar]
  57. Lobert S., Heil P. D., Namba K., Stubbs G. 1987; Preliminary X-ray fiber diffraction studies of cucumber green mottle mosaic virus, watermelon strain. Journal of Molecular Biology 196:935–938 [View Article]
    [Google Scholar]
  58. Longhi S. 2015; Structural disorder within paramyxoviral nucleoproteins. FEBS Lett 589:2649–2659 [View Article][PubMed]
    [Google Scholar]
  59. Lough T. J., Netzler N. E., Emerson S. J., Sutherland P., Carr F., Beck D. L., Lucas W. J., Forster R. L. 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 [View Article][PubMed]
    [Google Scholar]
  60. Lu B., Stubbs G., Culver J. N. 1996; Carboxylate interactions involved in the disassembly of tobacco mosaic tobamovirus. Virology 225:11–20 [View Article][PubMed]
    [Google Scholar]
  61. Lucas W. J. 2006; Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184 [View Article][PubMed]
    [Google Scholar]
  62. Makarov V. V., Skurat E. V., Semenyuk P. I., Abashkin D. A., Kalinina N. O., Arutyunyan A. M., Solovyev A. G., Dobrov E. N. 2013; Structural lability of Barley stripe mosaic virus virions. PLoS One 8:e60942 [View Article][PubMed]
    [Google Scholar]
  63. Martelli G. P., Adams M. J., Kreuze J. F., Dolja V. V. 2007; Family Flexiviridae: a case study in virion and genome plasticity. Annu Rev Phytopathol 45:73–100 [View Article][PubMed]
    [Google Scholar]
  64. Morozov S. Y., Solovyev A. G. 2003; Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366 [View Article][PubMed]
    [Google Scholar]
  65. Mundry K. W., Watkins P. A., Ashfield T., Plaskitt K. A., Eisele-Walter S., Wilson T. M. 1991; Complete uncoating of the 5′ leader sequence of tobacco mosaic virus RNA occurs rapidly and is required to initiate cotranslational virus disassembly in vitro . J Gen Virol 72:769–777 [View Article][PubMed]
    [Google Scholar]
  66. Namba K., Pattanayek R., Stubbs G. 1989; Visualization of protein-nucleic acid interactions in a virus. Refined structure of intact tobacco mosaic virus at 2.9 Å resolution by X-ray fiber diffraction. J Mol Biol 208:307–325[PubMed] [CrossRef]
    [Google Scholar]
  67. Napuli A. J., Falk B. W., Dolja V. V. 2000; Interaction between HSP70 homolog and filamentous virions of the Beet yellows virus. Virology 274:232–239 [View Article][PubMed]
    [Google Scholar]
  68. Napuli A. J., Alzhanova D. V., Doneanu C. E., Barofsky D. F., Koonin E. V., Dolja V. V. 2003; The 64-kilodalton capsid protein homolog of Beet yellows virus is required for assembly of virion tails. J Virol 77:2377–2384[PubMed] [CrossRef]
    [Google Scholar]
  69. Nemykh M. A., Efimov A. V., Novikov V. K., Orlov V. N., Arutyunyan A. M., Drachev V. A., Lukashina E. V., Baratova L. A., Dobrov E. N. 2008; One more probable structural transition in potato virus X virions and a revised model of the virus coat protein structure. Virology 373:61–71 [View Article][PubMed]
    [Google Scholar]
  70. Oparka K. J., Cruz S. S. 2000; The great escape: phloem transport and unloading of macromolecules. Annu Rev Plant Physiol Plant Mol Biol 51:323–347 [CrossRef]
    [Google Scholar]
  71. Ozeki J., Hashimoto M., Komatsu K., Maejima K., Himeno M., Senshu H., Kawanishi T., Kagiwada S., Yamaji Y., Namba S. 2009; The N-terminal region of the Plantago asiatica mosaic virus coat protein is required for cell-to-cell movement but is dispensable for virion assembly. Mol Plant Microbe Interact 22:677–685 [View Article][PubMed]
    [Google Scholar]
  72. Parker L., Kendall A., Stubbs G. 2002; Surface features of potato virus X from fiber diffraction. Virology 300:291–295 [View Article][PubMed]
    [Google Scholar]
  73. Pattanayek R., Stubbs G. 1992; Structure of the U2 strain of tobacco mosaic virus refined at 3.5 A resolution using X-ray fiber diffraction. J Mol Biol 228:516–528[PubMed] [CrossRef]
    [Google Scholar]
  74. Peremyslov V. V., Hagiwara Y., Dolja V. V. 1999; HSP70 homolog functions in cell-to-cell movement of a plant virus. Proc Natl Acad Sci U S A 96:14771–14776[PubMed] [CrossRef]
    [Google Scholar]
  75. Peremyslov V. V., Andreev I. A., Prokhnevsky A. I., Duncan G. H., Taliansky M. E., Dolja V. V. 2004; Complex molecular architecture of beet yellows virus particles. Proc Natl Acad Sci U S A 101:5030–5035 [View Article][PubMed]
    [Google Scholar]
  76. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., Meng E. C., Ferrin T. E. 2004; UCSF Chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612 [View Article][PubMed]
    [Google Scholar]
  77. Petty I. T., Jackson A. O. 1990; Two forms of the major barley stripe mosaic virus nonstructural protein are synthesized in vivo from alternative initiation codons. Virology 177:829–832 [View Article][PubMed]
    [Google Scholar]
  78. Planchart, A. 1995; X-ray fiber diffraction studies of odontoglossum ringspot virus: lessons on how nature produces a virus with a different host specificity. Thesis Vanderbilt University:
    [Google Scholar]
  79. Prilusky J., Felder C. E., Zeev-Ben-Mordehai T., Rydberg E. H., Man O., Beckmann J. S., Silman I., Sussman J. L. 2005; FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21:3435–3438 [View Article][PubMed]
    [Google Scholar]
  80. Prokhnevsky A. I., Peremyslov V. V., Napuli A. J., Dolja V. V. 2002; Interaction between long-distance transport factor and Hsp70-related movement protein of Beet yellows virus . J Virol 76:11003–11011[PubMed] [CrossRef]
    [Google Scholar]
  81. Prokhnevsky A. I., Peremyslov V. V., Dolja V. V. 2005; Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79:14421–14429 [View Article][PubMed]
    [Google Scholar]
  82. Raymond D. D., Piper M. E., Gerrard S. R., Smith J. L. 2010; Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc Natl Acad Sci U S A 107:11769–11843 [View Article][PubMed]
    [Google Scholar]
  83. Raymond D. D., Piper M. E., Gerrard S. R., Skiniotis G., Smith J. L. 2012; Phleboviruses encapsidate their genomes by sequestering RNA bases. Proc Natl Acad Sci U S A 109:19208–19213 [View Article][PubMed]
    [Google Scholar]
  84. Revers F., García J. A. 2015; Molecular biology of potyviruses. Adv Virus Res 92:101–199 [View Article][PubMed]
    [Google Scholar]
  85. Roberts I. M., Wang D., Findlay K., Maule A. J. 1998; Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (Cls) show that the Cl protein acts transiently in aiding virus movement. Virology 245:173–181 [View Article][PubMed]
    [Google Scholar]
  86. Rodríguez-Cerezo E., Findlay K., Shaw J. G., Lomonossoff G. P., Qiu S. G., Linstead P., Shanks M., Risco C. 1997; The coat and cylindrical inclusion proteins of a potyvirus are associated with connections between plant cells. Virology 236:296–306 [View Article][PubMed]
    [Google Scholar]
  87. Ruigrok R. W., Crépin T., Kolakofsky D. 2011; Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr Opin Microbiol 14:504–510 [View Article][PubMed]
    [Google Scholar]
  88. Russel M., Linderoth N. A., Sali A. 1997; Filamentous phage assembly: variation on a protein export theme. Gene 192:23–32 [View Article][PubMed]
    [Google Scholar]
  89. Saito T., Yamanaka K., Okada Y. 1990; Long-distance movement and viral assembly of tobacco mosaic virus mutants. Virology 176:329–336 [View Article][PubMed]
    [Google Scholar]
  90. Santa Cruz S., Roberts A. G., Prior D. A., 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[PubMed] [CrossRef]
    [Google Scholar]
  91. Satyanarayana T., Gowda S., Ayllón M. A., Dawson W. O. 2004; Closterovirus bipolar virion: evidence for initiation of assembly by minor coat protein and its restriction to the genomic RNA 5′ region. Proc Natl Acad Sci U S A 101:799–804 [View Article][PubMed]
    [Google Scholar]
  92. Savenkov E. I., Germundsson A., Zamyatnin A. A., Sandgren M., Valkonen J. P. 2003; Potato mop-top virus: the coat protein-encoding RNA and the gene for cysteine-rich protein are dispensable for systemic virus movement in Nicotiana benthamiana . J Gen Virol 84:1001–1005 [View Article][PubMed]
    [Google Scholar]
  93. 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[PubMed] [CrossRef]
    [Google Scholar]
  94. Seo J. K., Vo Phan M. S., Kang S. H., Choi H. S., Kim K. H. 2013; The charged residues in the surface-exposed C-terminus of the Soybean mosaic virus coat protein are critical for cell-to-cell movement. Virology 446:95–101 [View Article][PubMed]
    [Google Scholar]
  95. Solovyev A. G., Kalinina N. O., Morozov S. Y. 2012; Recent advances in research of plant virus movement mediated by triple gene block. Front Plant Sci 3: 276. [View Article][PubMed]
    [Google Scholar]
  96. Stubbs G. 1999; Tobacco mosaic virus particle structure and the initiation of disassembly. Philos Trans R Soc Lond B Biol Sci 354:551–557 [View Article][PubMed]
    [Google Scholar]
  97. Stubbs G., Warren S., Holmes K. 1977; Structure of RNA and RNA binding site in tobacco mosaic virus from 4-Å map calculated from X-ray fibre diagrams. Nature 267:216–221 [View Article][PubMed]
    [Google Scholar]
  98. Stubbs G., Kendall A. 2012; Helical viruses. Adv Exp Med Biol 726:631–658 [View Article][PubMed]
    [Google Scholar]
  99. Tamada T., Schmitt C., Saito M., Guilley H., Richards K., Jonard G. 1996; High resolution analysis of the readthrough domain of beet necrotic yellow vein virus readthrough protein: a KTER motif is important for efficient transmission of the virus by Polymyxa betae . J Gen Virol 77:1359–1367 [View Article][PubMed]
    [Google Scholar]
  100. Tian T., Rubio L., Yeh H. H., Crawford B., Falk B. W. 1999; Lettuce infectious yellows virus: in vitro acquisition analysis using partially purified virions and the whitefly Bemisia tabaci . J Gen Virol 80:1111–1117 [View Article][PubMed]
    [Google Scholar]
  101. Tilsner J., Linnik O., Louveaux M., Roberts I. M., Chapman S. N., Oparka K. J. 2013; Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. J Cell Biol 201:981–995 [View Article][PubMed]
    [Google Scholar]
  102. Tilsner J., Taliansky M. E., Torrance L. 2014; Plant virus movement. In eLS Chichester: John Wiley & Sons Ltd;
    [Google Scholar]
  103. Torrance L., Andreev I. A., Gabrenaite-Verhovskaya R., Cowan G., Mäkinen K., Taliansky M. E. 2006; An unusual structure at one end of potato potyvirus particles. J Mol Biol 357:1–8 [View Article][PubMed]
    [Google Scholar]
  104. Uversky V. N. 2011; Intrinsically disordered proteins from A to Z. IntJ Biochem Biol 43:1090–1103 [CrossRef]
    [Google Scholar]
  105. van der Lee R., Lang B., Kruse K., Gsponer J., Sánchez de Groot N., Huynen M. A., Matouschek A., Fuxreiter M., Babu M. M. 2014; Intrinsically disordered segments affect protein half-life in the cell and during evolution. Cell Rep 8:1832–1844 [View Article][PubMed]
    [Google Scholar]
  106. Verchot-Lubicz J., Torrance L., Solovyev A. G., Morozov S. Y., Jackson A. O., Gilmer D. 2010; Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23:1231–1247 [View Article][PubMed]
    [Google Scholar]
  107. Vijayapalani P., Maeshima M., Nagasaki-Takekuchi N., Miller W. A. 2012; Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. PLoS Pathogen 8:e1002639 [View Article]
    [Google Scholar]
  108. Wang H., Culver J. N., Stubbs G. 1997; Structure of ribgrass mosaic virus at 2.9 Å resolution: evolution and taxonomy of tobamoviruses. J Mol Biol 269:769–779 [View Article][PubMed]
    [Google Scholar]
  109. Wang H., Planchart A., Stubbs G. 1998; Caspar carboxylates: the structural basis of tobamovirus disassembly. Biophys J 74:633–638 [CrossRef]
    [Google Scholar]
  110. Ward J. J., Sodhi J. S., McGuffin L. J., Buxton B. F., Jones D. T. 2004; Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337:635–645 [View Article][PubMed]
    [Google Scholar]
  111. Wilson T., Shaw J. G. 1987; Cotranslational disassembly of filamentous plant virus nucleocapsids in vitro and in vivo. In Positive Strand RNA Viruses, UCLA Symposia on Molecular and Cellular Biology, New Series 50 pp 159–181 Edited by Brinton M. A., Rueckert R. R. New York: Alan R. Liss;
    [Google Scholar]
  112. Wolf S., Deom C. M., Beachy R. N., Lucas W. J. 1989; Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379 [View Article][PubMed]
    [Google Scholar]
  113. Yang S., Wang T., Bohon J., Gagné M. È., Bolduc M., Leclerc D., Li H. 2012; Crystal structure of the coat protein of the flexible filamentous papaya mosaic virus. J Mol Biol 422:263–273 [View Article][PubMed]
    [Google Scholar]
  114. Zayakina O., Arkhipenko M., Kozlovsky S., Nikitin N., Smirnov A., Susi P., Rodionova N., Karpova O., Atabekov J. 2008; Mutagenic analysis of Potato Virus X movement protein (TGBp1) and the coat protein (CP): in vitro TGBp1-CP binding and viral RNA translation activation. Mol Plant Pathol 9:37–44 [View Article][PubMed]
    [Google Scholar]
  115. Zhou H., Sun Y., Guo Y., Lou Z. 2013; Structural perspective on the formation of ribonucleoprotein complex in negative-sense single-stranded RNA viruses. Trends Microbiol 21:475–484 [View Article][PubMed]
    [Google Scholar]
  116. 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[PubMed] [CrossRef]
    [Google Scholar]
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