Tobacco Mosaic Virus – a Model for Macromolecular Cell-to-Cell Spread

  • E. WaigmannEmail author
  • M. Curin
  • M. Heinlein
Part of the Plant Cell Monographs book series (CELLMONO, volume 7)


Macromolecular cell-to-cell transport in plants occurs through complex intercellular channels, the plasmodesmata. Plant viruses pirate these natural plant communication channels for their own spread from an infected cell to a neighboring healthy cell. Viral movement proteins are the major agents in promoting this process. Tobacco mosaic virus is the most extensively studied plant virus and can therefore be viewed as a model system for cell-to-cell transport. In this chapter we summarize knowledge about mechanistic properties of the movement protein of Tobacco mosaic virus and discuss the potential involvement of other viral and cellular components in the intercellular transport process.


Tobacco Mosaic Virus Triple Gene Block Brome Mosaic Virus Apple Chlorotic Leaf Spot Virus Virus Movement Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aaziz R, Dinant S, Epel BL (2001) Plasmodesmata and plant cytoskeleton. Trends Plant Sci 6:326–330 PubMedCrossRefGoogle Scholar
  2. Arce-Johnson P, Kahn TW, Reimann-Philipp U, Rivera-Bustamante R, Beachy RN (1995) The amount of movement protein produced in transgenic plants influences the establishment, local movement, and systemic spread of infection by movement protein-deficient tobacco mosaic virus. Mol Plant-Microbe Interact 8:415–423 Google Scholar
  3. Ashby J, Boutant E, Seemanpillai M, Sambade A, Ritzenthaler C, Heinlein M (2006) Tobacco mosaic virus movement protein functions as a structural microtubule-associated protein. J Virol 80:8329–8344 PubMedCrossRefGoogle Scholar
  4. Asurmendi S, Berg R, Koo J, Beachy R (2004) Coat protein regulates formation of replication complexes during tobacco mosaic virus infection. Proc Natl Acad Sci USA 101:1415–1420 PubMedCrossRefGoogle Scholar
  5. Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN (1991) The tobacco mosaic virus 30 K movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol 72:209–211 PubMedGoogle Scholar
  6. Baluska F, Samaj J, Napier R, Volkmann D (1999) Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 19:481–488 PubMedCrossRefGoogle Scholar
  7. Bendahmane M, Fitchen JH, Zhang G, Beachy RN (1997) Studies of coat protein-mediated resistance to tobacco mosaic tobamovirus: correlation between assembly of mutant coat proteins and resistance. J Virol 71:7942–7950 PubMedGoogle Scholar
  8. Bendahmane M, Szecsi J, Chen I, Berg RH, Beachy RN (2002) Characterization of mutant tobacco mosaic virus coat protein that interferes with virus cell-to-cell movement. Proc Natl Acad Sci USA 99:3645–3650 PubMedCrossRefGoogle Scholar
  9. Berna A, Gafny R, Wolf S, Lucas WJ, Holt CA, Beachy RN (1991) The TMV movement protein: role of the C-terminal 73 amino acids in subcellular localization and function. Virology 182:682–689 PubMedCrossRefGoogle Scholar
  10. Bienz K, Egger D, Rasser Y, Bossard W (1994) Characterization of the poliovirus replication complex. Arch Virol (Suppl) 9:147–157 Google Scholar
  11. Blackman L, Harper JDI, Overall RL (1999) Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 78:297–304 PubMedGoogle Scholar
  12. Botha CEJ (1992) Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187:348–358 Google Scholar
  13. Boyko V, Ferralli J, Heinlein M (2000b) Cell-to-cell movement of TMV RNA is temperature-dependent and corresponds to the association of movement protein with microtubuli. Plant J 22:315–325 PubMedCrossRefGoogle Scholar
  14. Boyko V, Ferralli J, Ashby J, Schellenbaum P, Heinlein M (2000a) Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2:826–832 PubMedCrossRefGoogle Scholar
  15. Boyko V, van der Laak J, Ferralli J, Suslova E, Kwon M-O, Heinlein M (2000c) Cellular targets of functional and dysfunctional mutants of tobacco mosaic virus movement protein fused to green fluorescent protein. J Virol 74:11339–11346 PubMedCrossRefGoogle Scholar
  16. Boyko V, Ashby JA, Suslova E, Ferralli J, Sterthaus O, Deom CM, Heinlein M (2002) Intramolecular complementing mutations in tobacco mosaic virus movement protein confirm a role for microtubule association in viral RNA transport. J Virol 76:3974–3980 PubMedCrossRefGoogle Scholar
  17. Brill LM, Nunn RS, Kahn TW, Yeager M, Beachy RN (2000) Recombinant tobacco mosaic virus movement protein is an RNA-binding, alpha-helical membrane protein. Proc Natl Acad Sci USA 97:7112–7117 PubMedCrossRefGoogle Scholar
  18. Brill LM, Dechongkit S, DeLaBarre B, Stroebel J, Beachy RN, Yeager M (2004) Dimerization of recombinant tobacco mosaic virus movement protein. J Virol 78:3372–3377 PubMedCrossRefGoogle Scholar
  19. Carrington JC (1999) Reinventing plant virus movement. Trends Microbiol 7:312–313 PubMedCrossRefGoogle Scholar
  20. Chen MH, Tian GW, Gafni Y, Citovsky V (2005) Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 138:1866–1876 PubMedCrossRefGoogle Scholar
  21. Chen MH, Sheng J, Hind G, Handa A, Citovsky V (2000) Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 19:913–920 PubMedCrossRefGoogle Scholar
  22. Citovsky V, Knorr D, Schuster G, Zambryski PC (1990) The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60:637–647 PubMedCrossRefGoogle Scholar
  23. Citovsky V, McLean BG, Zupan J, Zambryski P (1993) Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally-regulated plant cell wall-associated protein kinase. Genes Dev 7:904–910 PubMedGoogle Scholar
  24. Citovsky V, Wong ML, Shaw A, Prasad BVV, Zambryski PC (1992) Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397–411 PubMedCrossRefGoogle Scholar
  25. Cooper B, Lapidot M, Heick JA, Dodds JA, Beachy RN (1995) A defective movement protein of TMV in transgenic plants confers resistance to multiple viruses whereas the functional analog increases susceptibility. Virology 206:307–313 PubMedCrossRefGoogle Scholar
  26. Cowan GH, Lioliopoulou F, Ziegler A, Torrance L (2002) Subcellular localisation, protein interactions, and RNA binding of Potato mop-top virus triple gene block proteins. Virology 298:106–115 PubMedCrossRefGoogle Scholar
  27. Curin M, Ojangu E, Trutnyeva K, Ilau B, Truve E, Waigmann E (2006) MPB2C, a microtubules-associated plant factor, is required for microtubular accumulation of tobacco mosaic virus movement protein in plants. Plant Physiol (in press) doi:10.1104/pp.106.091488 Google Scholar
  28. Deom CM, He XZ (1997) Second-site reversion of a dysfunctional mutation in a conserved region of the tobacco mosaic tobamovirus movement protein. Virology 232(1):13-18 PubMedCrossRefGoogle Scholar
  29. Deom CM, Shaw MJ, Beachy RN (1987) The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 327:389–394 CrossRefGoogle Scholar
  30. Deom CM, Schubert KR, Wolf S, Holt CA, Lucas WJ, Beachy RN (1990) Molecular characterization and biological function of the movement protein of tobacco mosaic virus in transgenic plants. Proc Natl Acad Sci USA 87:3284–3288 PubMedCrossRefGoogle Scholar
  31. Derse D, Heidecker G (2003) Virology. Forced entry - or does HTLV-1 have the key? Science 299:1670–1671 PubMedCrossRefGoogle Scholar
  32. Ding B, Turgeon R, Parthasarathy MV (1992) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41 CrossRefGoogle Scholar
  33. Ding XS, Liu J, Cheng NH, Folimonov A, Hou YM, Bao Y, Katagi C, Carter SA, Nelson RS (2004) The Tobacco mosaic virus 126-kDa protein associated with virus replication and movement suppresses RNA silencing. Mol Plant Microbe Interact 17:583–592 PubMedGoogle Scholar
  34. Dorokhov YL, Makinen K, Frolova OY, Merits A, Saarinen J, Kalkkinen N, Atabekov JG, Saarma M (1999) A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Lett 461:223–228 PubMedCrossRefGoogle Scholar
  35. Doronin SV, Hemenway C (1996) Synthesis of potatovirus X RNAs by membrane-containing extracts. J Virol 70:4795–4799 PubMedGoogle Scholar
  36. Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37:1356–1360 PubMedCrossRefGoogle Scholar
  37. Dunoyer P, Ritzenthaler C, Hemmer O, Michler P, Fritsch C (2002) Intracellular localization of the Peanut clump virus replication complex in tobacco BY-2 protoplasts containing green fluorescent protein labeled endoplasmic reticulum or Golgi apparatus. J Virol 76:865–874 PubMedCrossRefGoogle Scholar
  38. Epel BL, Padgett HS, Heinlein M, Beachy RN (1996a) Plant virus movement protein dynamics probed with a GFP-protein fusion. Gene 173:75–79 PubMedCrossRefGoogle Scholar
  39. Epel BL, Kuchuck B, Kotlizky G, Shurtz S, Erlanger M, Yahalom A (1995) Isolation and characterization of plasmodesmata. Methods Cell Biol 50:237–253 PubMedGoogle Scholar
  40. Epel BL, van Lent JWM, Cohen L, Kotlizky G, Katz A, Yahalom A (1996b) A 41 kDa protein isolated from maize mesocotyl cell walls immunolocalizes to plasmodesmata. Protoplasma 191:70–78 CrossRefGoogle Scholar
  41. Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K (2003) High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15:1507–1523 PubMedCrossRefGoogle Scholar
  42. Ferralli J, Ashby J, Fasler M, Boyko V, Heinlein M (2006) Disruption of microtubule organization and centrosome function by expression of Tobacco mosaic virus movement protein. J Virol 80:5807–5821 PubMedCrossRefGoogle Scholar
  43. Gaffe J, Tiznado ME, Handa AK (1997) Characterization and functional expression of a ubiquitously expressed tomato pectin methylesterase. Plant Physiol 114:1547–1556 PubMedCrossRefGoogle Scholar
  44. Gafny RML, Berna A, Holt CA, Deom CM, Beachy RN (1992) Effects of terminal deletion mutations on function of the movement protein of tobacco mosaic virus. Virology 187:499–507 PubMedCrossRefGoogle Scholar
  45. Gillespie T, Boevink P, Haupt S, Roberts AG, Toth R, Valentine T, Chapman S, Oparka KJ (2002) Functional analysis of a DNA-shuffled movement protein reveals that microtubules are dispensable for the cell-to-cell movement of tobacco mosaic virus. Plant Cell 14:1207–1222 PubMedCrossRefGoogle Scholar
  46. Goelet P, Lomonossoff GP, Butler PJG, Akam ME, Gait MJ, Karn J (1982) Nucleotide sequence of tobacco mosaic virus RNA. Proc Natl Acad Sci USA 79:5818-5822 PubMedCrossRefGoogle Scholar
  47. Goregaoker SP, Lewandowski DJ, Culver JN (2001) Identification and functional analysis of an interaction between domains of the 126/183-kDa replicase-associated proteins of tobacco mosaic virus. Virology 282:320–328 PubMedCrossRefGoogle Scholar
  48. Hacker DL, Petty IT, Wei N, Morris TJ (1992) Turnip crinkle virus genes required for RNA replication and virus movement. Virology 186:1–8 PubMedCrossRefGoogle Scholar
  49. Haley A, Hunter T, Kiberstis P, Zimmern D (1995) Multiple serine phosphorylation sites on the 30 kDa TMV cell-to-cell movement protein synthesized in tobacco protoplasts. Plant J 8:715–724 PubMedCrossRefGoogle Scholar
  50. Haller O, Kochs G (2002) Interferon-induced Mx protein: dynamin-like GTPases with antiviral activity. Traffic 3:710–717 PubMedCrossRefGoogle Scholar
  51. Haupt S, Cowan GH, Ziegler A, Roberts AG, Oparka KJ, Torrance L (2005) Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 17:164–181 PubMedCrossRefGoogle Scholar
  52. Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303-S325 PubMedGoogle Scholar
  53. Heinlein M (2002) Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Curr Opin Plant Biol 5:543–552 PubMedCrossRefGoogle Scholar
  54. Heinlein M (2002a) The spread of tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport. Cell Mol Life Sci 59:58–82 PubMedCrossRefGoogle Scholar
  55. Heinlein M (2005) Systemic RNA silencing. In: Oparka K (ed) Plasmodesmata, vol 18. Blackwell, Oxford, pp 212–240 Google Scholar
  56. Heinlein M, Epel B (2004) Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol 235:93–164 PubMedGoogle Scholar
  57. Heinlein M, Epel BL, Padgett HS, Beachy RN (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270:1983–1985 PubMedCrossRefGoogle Scholar
  58. Heinlein M, Padgett HS, Gens JS, Pickard BG, Caspar SJ, Epel BL, Beachy RN (1998) Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107–1120 PubMedCrossRefGoogle Scholar
  59. Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22:4523–4533 PubMedCrossRefGoogle Scholar
  60. Hirashima K, Watanabe Y (2001) Tobamovirus replicase coding region is involved in cell-to-cell movement. J Virol 75:8831–8836 PubMedCrossRefGoogle Scholar
  61. Hirashima K, Watanabe Y (2003) RNA helicase domain of tobamovirus replicase executes cell-to-cell movement possibly through collaboration with its nonconserved region. J Virol 77:12357–12362 PubMedCrossRefGoogle Scholar
  62. Huang T, Bohlenius H, Eriksson S, Parcy F, Nilsson O (2005) The mRNA of the Arabidopsis gene FT moves from leaf to shoot apex and induces flowering. Science 309:1694–1996 PubMedCrossRefGoogle Scholar
  63. Igakura T, Stinchcombe JC, Goon PK, Taylor GP, Weber JN, Griffiths GM, Tanaka Y, Osame M, Bangham CR (2003) Spread of HTLV-1 between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299:1713–1716 PubMedCrossRefGoogle Scholar
  64. Ishikawa M, Meshi T, Motoyoshi F, Takamatsu N, Okada Y (1986) In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus. Nucleic Acids Res 14:8291–8305 PubMedCrossRefGoogle Scholar
  65. Isogai M, Yoshikawa N (2005) Mapping the RNA-binding domain on the apple chlorotic leaf spot virus movement protein. J Gen Virol 86:225–229 PubMedCrossRefGoogle Scholar
  66. Jackson D (2005) Transcription factor movement through plasmodesmata. In: Oparka K (ed) Plasmodesmata, vol 18. Blackwell, Oxford, pp 113–134 Google Scholar
  67. Kahn TW, Lapidot M, Heinlein M, Reichel C, Cooper B, Gafny R, Beachy RN (1998) Domains of the TMV movement protein involved in subcellular localization. Plant J 15:15–25 PubMedCrossRefGoogle Scholar
  68. Karger EM, Frolova OY, Fedorova NV, Baratova LA, Ovchinnikova TV, Susi P, Makinen K, Ronnstrand L, Dorokhov YL, Atabekov JG (2003) Disfunctionality of TMV movement protein mutant mimicking the threonine 104 phosphorylation. J Gen Virol 84:727–732 PubMedCrossRefGoogle Scholar
  69. Karpova OV, Ivanov KI, Rodionova NP, Dorokhov YL, Atabekhov JG (1997) Nontranslatability and dissimilar behavior in plants and protoplasts of viral RNA and movement protein complexes formed in vitro. Virology 230:11–21 PubMedCrossRefGoogle Scholar
  70. Karpova OV, Rodionova NP, Ivanov KI, Dorokhov YL, Atabekov JG (1999) Phosphorylation of tobacco mosaic virus movement protein abolishes its translation repressing ability. Virology 261:20–24 PubMedCrossRefGoogle Scholar
  71. Kasteel DT, van der Wel NN, Jansen KA, Goldbach RW, van Lent JW (1997) Tubule-forming capacity of the movement proteins of alfalfa mosaic virus and brome mosaic virus. J Gen Virol 78:2089–2093 PubMedGoogle Scholar
  72. Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complex. Proc Natl Acad Sci USA 101:6291–6296 PubMedCrossRefGoogle Scholar
  73. Kim JY (2005) Regulation of short-distance transport of RNA and protein. Curr Opin Plant Biol 8:45–52 PubMedCrossRefGoogle Scholar
  74. Kiselyova OI, Yaminsky IV, Karger EM, Frolova OY, Dorokhov YL, Atabekov JG (2001) Visualization by atomic force microscopy of tobacco mosaic virus movement protein–RNA complexes formed in vitro. J Gen Virol 82:1503–1508 PubMedGoogle Scholar
  75. Kishi-Kaboshi M, Murata T, Hasebe M, Watanabe Y (2005) An extraction method for tobacco mosaic virus movement protein localizing in plasmodesmata. Protoplasma 225:85–92 PubMedCrossRefGoogle Scholar
  76. Knapp E, Danyluk GM, Achor D, Lewandowski DJ (2005) A bipartite Tobacco mosaic virus-defective RNA (dRNA) system to study the role of the N-terminal methyl transferase domain in cell-to-cell movement of dRNAs. Virology 341:47–58 PubMedCrossRefGoogle Scholar
  77. Koonin EV, Mushegian AR, Ryabov EV, Dolja VV (1991) Diverse groups of plant RNA and DNA viruses share related movement proteins that may possess chaperone-like activity. J Gen Virol 72:2985–2903 Google Scholar
  78. Kotlizky G, Katz A, van der Laak J, Boyko V, Lapidot M, Beachy RN, Heinlein M, Epel BL (2001) A dysfunctional movement protein of tobacco mosaic virus interferes with targeting of wild-type movement protein to microtubules. Mol Plant-Microbe Interact 14:895–904 PubMedGoogle Scholar
  79. Kragler F, Monzer J, Shash K, Xoconostle-Cázares B, Lucas WJ (1998) Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J 15:367–381 CrossRefGoogle Scholar
  80. Kragler F, Curin M, Trutnyeva K, Gansch A, Waigmann E (2003) MPB2C, a microtubule associated plant protein binds to and interferes with cell-to-cell transport of tobacco-mosaic-virus movement protein. Plant Physiol 132:1870–1883 PubMedCrossRefGoogle Scholar
  81. Kubota K, Tsuda S, Tamai A, Meshi T (2003) Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J Virol 77:11016–11026 PubMedCrossRefGoogle Scholar
  82. Lapidot M, Gafny R, Ding B, Wolf S, Lucas WJ, Beachy RN (1993) A dysfunctional movement protein of tobacco mosaic virus that partially modifies the plasmodesmata and limits virus spread in transgenic plants. Plant J 4:959–970 CrossRefGoogle Scholar
  83. Laporte C, Vetter G, Loudes AM, Robinson DG, Hillmer S, Stussi-Garaud C, Ritzenthaler C (2003) Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15:2058–2075 PubMedCrossRefGoogle Scholar
  84. Lee JY, Yoo BC, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–396 PubMedCrossRefGoogle Scholar
  85. Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17:2817–2831 PubMedCrossRefGoogle Scholar
  86. Lewandowski DJ, Dawson WO (2000) Functions of the 126- and 183-kDa proteins of tobacco mosaic virus. Virology 271:90–98 PubMedCrossRefGoogle Scholar
  87. Li A, Schuermann D, Gallego F, Kovalchuk I, Tinland B (2002) Repair of damaged DNA by Arabidopsis cell extract. Plant Cell 14:263–273 PubMedCrossRefGoogle Scholar
  88. Li WZ, Qu F, Morris TJ (1998) Cell-to-cell movement of turnip crinkle virus is controlled by two small open reading frames that function in trans. Virology 244:405–416 PubMedCrossRefGoogle Scholar
  89. Liu J-Z, Blancaflor EB, Nelson RS (2005) The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol 138:1853–1865 PubMedCrossRefGoogle Scholar
  90. Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726 PubMedCrossRefGoogle Scholar
  91. Lucas WJ, Yoo BC, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2:849–857 PubMedCrossRefGoogle Scholar
  92. Mas P, Beachy RN (1999) Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J Cell Biol 147:945–958 PubMedCrossRefGoogle Scholar
  93. Mas P, Beachy RN (2000) Role of microtubules in the intracellular distribution of tobacco mosaic virus movement protein. Proc Natl Acad Sci USA 97:12345–12349 PubMedCrossRefGoogle Scholar
  94. McLean BG, Zupan J, Zambryski PC (1995) Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7:2101–2114 PubMedCrossRefGoogle Scholar
  95. Melcher U (1990) Similarities between putative transport proteins of plant viruses. J Gen Virol 71:1009–1018 PubMedGoogle Scholar
  96. Melcher U (2000) The “30K” superfamily of viral movement proteins. J Gen Virol 81:257–266 PubMedGoogle Scholar
  97. Meshi T, Hosokawa D, Kawagishi M, Watanabe Y, Okada Y (1992) Reinvestigation of intracellular localization of the 30K protein in tobacco protoplasts infected with tobacco mosaic virus RNA. Virology 2:807–819 Google Scholar
  98. Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, Okada Y (1987) Function of the 30 kdprotein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6:2557–2563 PubMedGoogle Scholar
  99. Moore PJ, Fenczik CA, Beachy RN (1992) Developmental changes in plasmodesmata in transgenic plants expressing the movement protein of tobacco mosaic virus. Protoplasma 170:115–127 CrossRefGoogle Scholar
  100. Morozov SY, Solovyev AG (2003) Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366 PubMedCrossRefGoogle Scholar
  101. Moser O, Gagey M-J, Godefroy-Colburn T, Stussi-Garaud C, Ellwart-Tschürtz M, Nitschko H, Mundry K-W (1988) The fate of the transport protein of tobacco mosaic virus in systemic and hypersensitive tobacco hosts. J Gen Virol 69:1367–1373 Google Scholar
  102. Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S, Nagata T, Horio T, Hasebe M (2005) Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat Cell Biol Google Scholar
  103. Nairn CJ, Lewandowski DJ, Burns JK (1998) Genetics and expression of two pectinesterase genes in Valencia orange. Physiol Plant 102:226–235 CrossRefGoogle Scholar
  104. Nguyen L, Lucas WJ, Ding B, Zaitlin M (1996) Viral RNA trafficking is inhibited in replicase-mediated resistant transgenic tobacco plants. Proc Natl Acad Sci USA 93:12643–12647 PubMedCrossRefGoogle Scholar
  105. Nilsson-Tillgren T, Kielland-Brandt MC, Bekke B (1974) Studies on the biosynthesis of tobacco mosaic virus. VI. On the subcellular localization of double-stranded viral RNA. Mol Gen Genet 128:157–169 PubMedGoogle Scholar
  106. Nogales E, Whittaker M, Milligan RA, Downing KH (1999) High-resolution model of the microtubule. Cell 96:70–88 CrossRefGoogle Scholar
  107. Olesen P (1979) The neck constriction in plasmodesmata: evidence for a peripheral sphincter-like structure revealed by fixation with tannic acid. Planta 144:349–358 CrossRefGoogle Scholar
  108. Oparka K (2005) Plasmodesmata, vol 18. Blackwell, Oxford Google Scholar
  109. Oparka KJ, Prior DAM, Santa-Cruz S, Padgett HS, Beachy RN (1997) Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus. Plant J 12:781–789 PubMedCrossRefGoogle Scholar
  110. Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts I, Pradel KS, Imlau A, Kotlizky G, Sauer N, Epel B (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754 PubMedCrossRefGoogle Scholar
  111. Osman TA, Buck KW (1996) Complete replication in vitro of tobacco mosaic virus RNA by a template-dependent, membrane-bound RNA polymerase. J Virol 70:6227–6234 PubMedGoogle Scholar
  112. Osman TAM, Buck KW (1997) The tobacco mosaic virus RNA polymerase complex contains a plant protein related to the RNA-binding subunit of yeast eIF-3. J Virol 71:6075–6082 PubMedGoogle Scholar
  113. Overall RL, Blackman LM (1996) A model for the macromolecular structure of plasmodesmata. Trends Plant Sci 1:307–311 Google Scholar
  114. Overall RL, White RG, Blackman LM, Radford JE (2000) Actin and myosin in plasmodesmata. In: Staiger CJ, Baluska F, Volkmann D, Barlow PW (eds) Actin: A Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic, Dordrecht, pp 1–19 Google Scholar
  115. Padgett HS, Epel BL, Kahn TW, Heinlein M, Watanabe Y, Beachy RN (1996) Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection. Plant J 10:1079–1088 PubMedCrossRefGoogle Scholar
  116. Powell-Abel P, Nelson RS, De B, Hoffmann N, Rogers SG, Fraley RT, Beachy RN (1986) Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738–743 CrossRefGoogle Scholar
  117. Pressey R (1984) Role of pectinesterase in pH-dependent interactions between pea cell wall polymers. Plant Physiol 76:547–549 PubMedCrossRefGoogle Scholar
  118. Ralph RK, Bullivant S, Wojcik SJ (1971) Cytoplasmic membranes as a possible site of tobacco mosaic virus RNA replication. Virology 43:713–716 PubMedCrossRefGoogle Scholar
  119. Reichel C, Beachy RN (1998) Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA 95:11169–11174 PubMedCrossRefGoogle Scholar
  120. Reichel C, Beachy RN (1999) The role of the ER and cytoskeleton in plant viral trafficking. Trends Plant Sci 4:458–462 PubMedCrossRefGoogle Scholar
  121. Reichel C, Beachy RN (2000) Degradation of tobacco mosaic virus movement protein by the 26S proteasome. J Virol 74:3330–3337 PubMedCrossRefGoogle Scholar
  122. Reichelt S, Knight AE, Hodge PT, Baluska F, Samaj J, Volkmann D, Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19:555–567 PubMedCrossRefGoogle Scholar
  123. Restrepo-Hartwig MA, Ahlquist P (1996) Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral synthesis. J Virol 70:8908–8916 PubMedGoogle Scholar
  124. Ritzenthaler C, Laporte C, Gaire F, Dunoyer P, Schmitt C, Duval S, Piéquet A, Loudes AM, Rohfritsch O, Stussi-Garaud C, Pfeiffer P (2002) Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J Virol 76:8808–8819 PubMedCrossRefGoogle Scholar
  125. Sacristan S, Malpica JM, Fraile A, Garcia-Arenal F (2003) Estimation of population bottlenecks during systemic movement of tobacco mosaic virus in tobacco plants. J Virol 77:9906–9911 PubMedCrossRefGoogle Scholar
  126. Sagi G, Katz A, Guenoune-Gelbart D, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the golgi apparatus. Plant Cell 17:1788–1800 PubMedCrossRefGoogle Scholar
  127. Sauri A, Saksena S, Salgado J, Johnson AE, Mingarro I (2005) Double-spanning plant viral movement protein integration into the ER membrane is SRP-dependent, translocon-mediated, and concerted. J Biol Chem 280:25907–25912 PubMedCrossRefGoogle Scholar
  128. Schaad MC, Jensen PE, Carrington JC (1997) Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J 16:4049–4059 PubMedCrossRefGoogle Scholar
  129. Schmit AC (2002) Acentrosomal microtubule nucleation in higher plants. Int Rev Cytol 220:257–289 PubMedGoogle Scholar
  130. Seemanpillai M, Elamawi R, Ritzenthaler C, Heinlein M (2006) Challenging the role of microtubules in Tobacco mosaic virus movement by drug treatments is disputable. J Virol 80:6712–6715 PubMedCrossRefGoogle Scholar
  131. Seltzer V, Pawlowski T, Campagne S, Canaday J, Erhardt M, Evrard JL, Herzog E, Schmit AC (2003) Multiple microtubule nucleation sites in higher plants. Cell Biol Int 27:267–269 PubMedCrossRefGoogle Scholar
  132. Siegel A, Zaitlin M, Sehgal OP (1962) The isolation of defective tobacco mosaic virus strains. Proc Natl Acad Sci USA 48:1845–1851 PubMedCrossRefGoogle Scholar
  133. Solovyev AG, Stroganova TA, Zamyatnin AA Jr, Fedorkin ON, Schiemann J, Morozov SY (2000) Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virol 269:113–127 CrossRefGoogle Scholar
  134. Szécsi J, Ding XS, Lim CO, Bendahmane M, Cho MJ, Nelson RS, Beachy RN (1999) Development of tobacco mosaic virus infection sites in Nicothiana benthamiana. Mol Plant Microbe Interact 2:143–152 Google Scholar
  135. Takamatsu N, Ishiakwa M, Meshi T, Okada Y (1987) Expression of bacterial chloramphenicol acetyltransferase gene in tobacco plants infected by TMV-RNA. EMBO J 6:307–311 PubMedGoogle Scholar
  136. Tomenius K, Clapham D, Meshi T (1987) Localization by immunogold cytochemistry of the virus coded 30 K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363–371 CrossRefPubMedGoogle Scholar
  137. Trutnyeva K, Bachmaier R, Waigmann E (2005) Mimicking carboxyterminal phosphorylation differentially effects subcellular distribution and cell-to-cell movement of Tobacco mosaic virus movement protein. Virology 332:563–577 PubMedCrossRefGoogle Scholar
  138. Turner A, Wells B, Roberts K (1994) Plasmodesmata of maize root tips: structure and composition. J Cell Sci 107:3351–3361 PubMedGoogle Scholar
  139. Tzfira T, Rhee Y, Chen M-H, Citovsky V (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Ann Rev Microbiol 54:187–219 CrossRefGoogle Scholar
  140. 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 PubMedCrossRefGoogle Scholar
  141. Vilar M, Sauri A, Monne M, Marcos JF, Von Heijne G, Perez-Paya E, Mingarro I (2002) Insertion and topology of a plant viral movement protein in the endoplasmic reticulum membrane. J Biol Chem 277:23447–23452 PubMedCrossRefGoogle Scholar
  142. Waigmann E, Zambryski P (1995) Tobacco mosaic virus movement protein-mediated protein transport between trichome cells. Plant Cell 7:2069–2079 PubMedCrossRefGoogle Scholar
  143. Waigmann E, Lucas W, Citovsky V, Zambryski P (1994) Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc Natl Acad Sci USA 91:1433–1437 PubMedCrossRefGoogle Scholar
  144. Waigmann E, Ueki S, Trutnyeva K, Citovsky V (2004) The ins and outs of non-destructive cell-to-cell and systemic movement of plant viruses. Crit Rev Plant Sci 23:195–250 CrossRefGoogle Scholar
  145. Waigmann E, Chen M-H, Bachmaier R, Goshroy S, Citovsky V (2000) Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J 19:4875–4884 PubMedCrossRefGoogle Scholar
  146. Watanabe T, Honda A, Iwata A, Ueda S, Hibi T, Ishihama A (1999) Isolation from tobacco mosaic virus-infected tobacco of a solubilized template-specific RNA-dependent RNA polymerase containing a 126K/183K protein heterodimer. J Virol 73:2633–2640 PubMedGoogle Scholar
  147. Watanabe Y, Okada Y (1986) In vitro viral RNA synthesis by a subcellular fraction of TMV-inoculated tobacco protoplasts. Virology 149:73–74 CrossRefGoogle Scholar
  148. Watanabe Y, Ogawa T, Okada Y (1992) In vivo phosphorylation of the 30-kDa protein of tobacco mosaic virus. FEBS Lett 313:181–184 PubMedCrossRefGoogle Scholar
  149. Wellink J, van Lent JWM, Verver J, Sijen T, Goldbach RW, van Kammen A (1993) The cowpea mosaic virus M RNA-encoded 48-kilodalton protein is responsible for induction of tubular structures in protoplasts. J Virol 67:3660–3664 PubMedGoogle Scholar
  150. White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180:169–184 CrossRefGoogle Scholar
  151. Wright KM, Wood NT, Roberts AG, Chapman S, Boeving P, MacKenzie KM, Oparka KJ (2007) Targeting of TMV Movement Protein to Plasmodesmata Requires the Actin/ER Network; Evidence from FRAP. Traffic 8(1):21–31 PubMedCrossRefGoogle Scholar
  152. Wu X, Weigel D, Wigge PA (2002) Signaling in plants by intercellular RNA and protein movement. Genes Dev 16:151–158 PubMedCrossRefGoogle Scholar
  153. Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ (2004) A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000 PubMedCrossRefGoogle Scholar
  154. Young ND, Zaitlin M (1986) An analysis of tobacco mosaic virus replicative structures synthesized in vitro. Plant Mol Biol 6:455–465 CrossRefGoogle Scholar
  155. Young ND, Forney J, Zaitlin M (1987) Tobacco mosaic virus replicase and replicative structures synthesized in vitro. J Cell Sci 7(Suppl):277–285 Google Scholar
  156. Zamyatnin AA Jr, Solovyev AG, Savenkov EI, Germundsson A, Sandgren M, Valkonen JP, Morozov SY (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 PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  1. 1.Max F. Perutz Laboratories, Department of Medical BiochemistryMedical University of ViennaViennaAustria
  2. 2.Institut Biologie Moléculaire des Plantes (IBMP)Strasbourg cedexFrance

Personalised recommendations