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Microtubules and Viral Movement

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Book cover Plant Microtubules

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 11))

Abstract

The spread of plant virus infection depends on specialized virus-encoded movement proteins (MP) that target plasmodesmata (PD) to facilitate viral movement from cell to cell. Cell biological studies have shown that the MP of tobacco mosaic virus (TMV) accumulates in PD and also associates with membranes and the cytoskeleton during infection. Whereas the targeting of the protein to PD involves the endoplasmic reticulum–actin network, additional contacts with elements of the microtubule (MT) cytoskeleton are implicated in the transport of viral RNA. This article provides an overview of recent and current findings that describe the interactions between MP and MT during early and late stages of TMV infection.

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References

  • Ackmann M, Wiech H, Mandelkow E (2000) Nonsaturable binding indicates clustering of tau on the microtubule surface in a paired helical filament-like conformation. J Biol Chem 275:30335–30343

    PubMed  CAS  Google Scholar 

  • Aguilar I, Sanchez F, Martin A, Martinez-Herrera D, Ponz F (1996) Nucleotide sequence of Chinese rape mosaic virus (oilseed rape mosaic virus), a crucifer tobamovirus infecting Arabidopsis thaliana. Plant Mol Biol 30:191–197

    PubMed  CAS  Google Scholar 

  • Ainger K, Avossa D, Morgan F, Hill SJ, Barry C, Barbarese E, Carson JH (1993) Transport and localization of exogeneous myelin basic protein mRNA microinjected into oligodendrocytes. J Cell Biol 123:431–441

    PubMed  CAS  Google Scholar 

  • Allan NS, Brown DT (1988) Dynamics of the endoplasmic reticulum in living onion epidermal cells in relation to microtubules, microfilaments and intracellular particle movement. Cell Motil Cytoskeleton 10:153–163

    Google Scholar 

  • Arce-Johnson P, Kahn TW, Reimann-Philipp U, Rivera-Bustamente 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 3:415–423

    Google Scholar 

  • Ashby J, Boutant E, Seemanpillai M, Groner A, Sambade A, Ritzenthaler C, Heinlein M (2006) Tobacco mosaic virus movement protein functions as a structural microtubule-associated protein. J Virol 80:8329–8344

    PubMed  CAS  Google Scholar 

  • Asurmendi S, Berg RH, Koo JC, Beachy RN (2004) Coat protein regulates formation of replication complexes during tobacco mosaic virus infection. Proc Natl Acad Sci USA 101:1415–1420

    PubMed  CAS  Google Scholar 

  • Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN (1991) The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol 72:209–211

    PubMed  CAS  Google Scholar 

  • Baulcombe DC, Chapman SN, Santa Cruz S (1995) Jellyfish green fluorescent protein as a reporter for virus infections. Plant J 7:1045–1053

    PubMed  CAS  Google Scholar 

  • Becht P, Konig J, Feldbrugge M (2006) The RNA-binding protein Rrm4 is essential for polarity in Ustilago maydis and shuttles along microtubules. J Cell Sci 119:4964–4973

    PubMed  CAS  Google Scholar 

  • Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445

    PubMed  CAS  Google Scholar 

  • Blanc S, Schmidt I, Vantard M, Scholthof HB, Kuhl G, Esperandieu P, Cerutti M, Louis C (1996) The aphid transmission factor of cauliflower mosaic virus forms a stable complex with microtubules in both insect and plant cells. Proc Natl Acad Sci USA 93:15158–15163

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 microtubules. Plant J 22:315–325

    PubMed  CAS  Google Scholar 

  • 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 GFP. J Virol 74:11339–11346

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M (2007) Validation of microtubule-associated TMV RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51:589–603

    PubMed  CAS  Google Scholar 

  • Brill LM, Nunn RS, Kahn TW, Yeager M, Beachy RN (2000) Recombinant tobacco mosaic virus movement protein is an RNA-binding, α-helical membrane protein. Proc Natl Acad Sci USA 97:7112–7117

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bullock SL, Nicol A, Gross SP, Zicha D (2006) Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr Biol 16:1447–1452

    PubMed  CAS  Google Scholar 

  • Carr T, Whitham SA (2007) An emerging model system: Arabidopsis as a viral host plant. In: Waigmann E, Heinlein M (eds) Viral transport in plants. Springer, Heidelberg, pp 159–183

    Google Scholar 

  • Carrington JC, Kasschau KD, Mahajan SK, Schaad MC (1996) Cell-to-cell and long distance transport of viruses in plants. Plant Cell 8:1669–1681

    PubMed  CAS  Google Scholar 

  • Chapman SN, Hills G, Watts J, Baulcombe DC (1992) Mutational analysis of the coat protein gene of potato virus X: effects on virion morphology and viral pathogenicity. Virology 191:223–230

    PubMed  CAS  Google Scholar 

  • Citovsky V, Knorr D, Schuster G, Zambryski P (1990) The P30 movement protein of tobacco mosaic virus is a single-stranded nucleic acid binding protein. Cell 60:637–647

    PubMed  CAS  Google Scholar 

  • Citovsky V, McLean BG, Zupan JR, 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Cowan GH, Lioliopoulou F, Ziegler A, Torrance L (2002) Subcellular localization, protein interactions, and RNA binding activity of potato mop-top virus triple gene block proteins. Virology 298:106–115

    PubMed  CAS  Google Scholar 

  • Curin M, Ojangu EL, Trutnyeva K, Ilau B, Truve E, Waigmann E (2007) MPB2C, a microtubule-associated plant factor, is required for microtubular accumulation of tobacco mosaic virus movement protein in plants. Plant Physiol 143:801–811

    PubMed  CAS  Google Scholar 

  • Czaplinski K, Singer RH (2006) Pathways for mRNA localization in the cytoplasm. Trends Biochem Sci 31:687–693

    PubMed  CAS  Google Scholar 

  • Dawson WO, Bubrick P, Grantham GL (1988) Modifications of the tobacco mosaic virus coat protein gene affecting replication, movement, and symptomatology. Phytopathology 78:783–789

    CAS  Google Scholar 

  • Deom CM, He XZ (1997) Second-site reversion of a dysfunctional mutation in a conserved region of the tobacco mosaic virus movement protein. Virology 232:13–18

    PubMed  CAS  Google Scholar 

  • Deom CM, Oliver MJ, Beachy RN (1987) The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237:384–389

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Derrick PM, Carter SA, Nelson RS (1997) Mutation of the tobacco mosaic tobamovirus 126- and 183-kDa proteins: effects on phloem-dependent virus accumulation and synthesis of viral proteins. Mol Plant Microbe Interact 10:589–596

    CAS  Google Scholar 

  • Derse D, Heidecker G (2003) Virology. Forced entry—or does HTLV-1 have the key? Science 299:1670–1671

    PubMed  CAS  Google Scholar 

  • Diaz-Griffero F, Espinoza Cancino C, Medina Arevalo C, Arce-Johnson P (2006) Expression of the crucifer-infecting TMV-Cg movement protein in tobacco plants complements in trans a TMV-U1 trafficking-deficient mutant. Biol Res 39:269–279

    Article  PubMed  CAS  Google Scholar 

  • Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ (1992a) Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4:915–928

    PubMed  CAS  Google Scholar 

  • Ding B, Turgeon R, Parthasarathy MV (1992b) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41

    Google Scholar 

  • Dohner K, Nagel CH, Sodeik B (2005) Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol 13:320–327

    PubMed  Google Scholar 

  • Dorokhov YL, Alexandrov NM, Miroshnichenko NA, Atabekov JG (1983) Isolation and analysis of virus-specific ribonucleoprotein of tobacco mosaic virus-infected tobacco. Virology 127:237–252

    CAS  PubMed  Google Scholar 

  • Dorokhov YL, Alexandrova NM, Miroshnichenko NA, Atabekov JG (1984) The informosome-like virus-specific ribonucleoprotein (vRNP) may be involved in the transport of tobacco mosaic virus infection. Virology 137:127–134

    CAS  PubMed  Google Scholar 

  • Dunoyer P, Voinnet O (2005) The complex interplay between plant viruses and host RNA-silencing pathways. Curr Opin Plant Biol 8:415–423

    PubMed  CAS  Google Scholar 

  • Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143:777–794

    PubMed  CAS  Google Scholar 

  • Epel B (1994) Plasmodesmata: composition, structure and trafficking. Plant Mol Biol 26:1343–1356

    PubMed  CAS  Google Scholar 

  • Epel BL, Padgett HS, Heinlein M, Beachy RN (1996) Plant virus movement protein dynamics probed with a GFP–protein fusion. Gene 173:75–79

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Ferrandon D, Elphick L, Nüsslein-Volhard C, St Johnston D (1994) Staufen protein associates with the 3′UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79:1221–1232

    PubMed  CAS  Google Scholar 

  • Forristal C, Pondel M, Chen L, Kung ML (1995) Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development 121:201–208

    Google Scholar 

  • Fricker M, Runions J, Moore I (2006) Quantitative fluorescence microscopy: from art to science. Annu Rev Plant Biol 57:79–107

    PubMed  CAS  Google Scholar 

  • Gillespie T, Boevink P, Haupt S, Roberts AG, Toth R, Vantine 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gorshkova EN, Erokhina TN, Stroganova TA, Yelina NE, Zamyatin AA, Kalinina NO, Schiemann J, Solovyev AG, Morozov SY (2003) Immunodetection and fluorescence microscopy of transgenically expressed hordeivirus TGBp3 movement protein reveals its association with endoplasmic reticulum elements in close proximity to plasmodesmata. J Gen Virol 84:985–994

    PubMed  CAS  Google Scholar 

  • Greber UF, Way M (2006) A superhighway to virus infection. Cell 124:741–754

    PubMed  CAS  Google Scholar 

  • Hagiwara H, Yorifuji H, Sato-Yoshitake R, Hirokawa N (1994) Competition between motor molecules (kinesin and cytoplasmic dynein) and fibrous microtubule-associated proteins in binding to microtubules. J Biol Chem 269:3581–3589

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hamada S, Ishiyama K, Choi SB, Wang C, Singh S, Kawai N, Franceschi VR, Okita TW (2003) The transport of prolamine RNAs to prolamine protein bodies in living rice endosperm cells. Plant Cell 15:2253–2264

    PubMed  CAS  Google Scholar 

  • Haseloff J, Amos B (1995) GFP in plants. Trends Genet 11:328–329

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell Supplement S303–S325

    Google Scholar 

  • Heinlein M (2002) The spread of tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport. Cell Mol Life Sci 59:58–82

    PubMed  CAS  Google Scholar 

  • Heinlein M (2005) Systemic RNA silencing. In: Oparka K (ed) Plasmodesmata. Blackwell, Oxford, pp 212–240

    Google Scholar 

  • Heinlein M (2006) TMV movement protein targets cell–cell channels in plants and prokaryotes: possible roles of tubulin- and FtsZ-based cytoskeletons. In: Baluska F, Volkmann D, Barlow PW (eds) Cell–cell channels. Landes Bioscience, Austin, pp 176–182

    Google Scholar 

  • Heinlein M, Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol 235:93–164

    PubMed  CAS  Google Scholar 

  • Heinlein M, Epel BL, Padgett HS, Beachy RN (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270:1983–1985

    PubMed  CAS  Google Scholar 

  • Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN (1998a) 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

    PubMed  CAS  Google Scholar 

  • Heinlein M, Wood MR, Thiel T, Beachy RN (1998b) Targeting and modification of prokaryotic cell–cell junctions by tobacco mosaic virus cell-to-cell movement protein. Plant J 14:345–351

    PubMed  CAS  Google Scholar 

  • Hilf ME, Dawson WO (1993) The tobamovirus capsid protein functions as a host-specific determinant of long-distance movement. Virology 193:106–114

    PubMed  CAS  Google Scholar 

  • Hirashima K, Watanabe Y (2001) Tobamovirus replicase coding region is involved in cell-to-cell movement. J Virol 75:8831–8836

    PubMed  CAS  Google Scholar 

  • Hirokawa N (2006) mRNA transport in dendrites: RNA granules, motors, and tracks. J Neurosci 26:7139–7142

    PubMed  CAS  Google Scholar 

  • Holt CA, Hodgson RA, Coker FA, Beachy RN, Nelson RS (1990) Characterization of the masked strain of tobacco mosaic virus: identification of the region responsible for symptom attenuation by analysis of an infectious cDNA clone. Mol Plant Microbe Interact 3:417–423

    PubMed  CAS  Google Scholar 

  • Huang Z, Han Y, Howell SH (2000) Formation of surface tubules and fluorescent foci in Arabidopsis thaliana protoplasts expressing a fusion between the green fluorescent protein and the cauliflower mosaic virus movement protein. Virology 271:58–64

    PubMed  CAS  Google Scholar 

  • Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA (2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis–virus interactions. Plant Physiol 137:1147–1159

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Januschke J, Gervais L, Dass S, Kaltschmidt JA, Lopez-Schier H, St Johnston D, Brand AH, Roth S, Guichet A (2002) Polar transport in the Drosophila oocyte requires dynein and kinesin I cooperation. Curr Biol 12:1971–1981

    PubMed  CAS  Google Scholar 

  • Jockusch H (1968) Two mutants of tobacco mosaic virus temperature sensitive in two different functions. Virology 35:94–101

    PubMed  CAS  Google Scholar 

  • Ju HJ, Samuels TD, Wang YS, Blancaflor E, Payton M, Mitra R, Krishnamurthy K, Nelson RS, 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Karasev AV, Kashina AS, Gelfand VI, Dolja VV (1992) HSP70-related 65 kDa protein of beet yellows closterovirus is a microtubule-binding protein. FEBS Lett 304:12–14

    PubMed  CAS  Google Scholar 

  • Karchar B, Reese TS (1988) The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J Cell Biol 106:1545–1552

    Google Scholar 

  • Karger EM, Frolova OY, Fedorova NV, Baratova LA, Ovchinnikova TV, Susi P, Makinen K, Ronnstrand L, Dorokhov YL, Atabekov JG (2003b) Dysfunctionality of tobacco mosaic virus movement protein mutant mimicking threonine 104 phosphorylation. J Gen Virol 84:727–732

    PubMed  CAS  Google Scholar 

  • Karpova OV, Rodionova NP, Ivanov KI, Kozlovsky SV, Dorokhov YL, Atabekov JG (1999) Phosphorylation of tobacco mosaic virus movement protein abolishes its translation repressing ability. Virology 261:20–24

    PubMed  CAS  Google Scholar 

  • Kassanis B (1952) Some effects of high temperature on the susceptibility of plants to infection with viruses. Ann Appl Biol 39:358–369

    Google Scholar 

  • Kasteel D, van der Wel N, Jansen K, Goldbach R, van Lent J (1997) Tubule-forming capacity of the movement proteins of alfalfa mosaic virus and brome mosaic virus. J Gen Virol 78:2089–2093

    PubMed  CAS  Google Scholar 

  • Kasteel DTJ, Perbal M-C, Boyer J-C, Wellink J, Goldbach RW, Maule AJ, van Lent JWM (1996) The movement proteins of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J Gen Virol 77:2857–2864

    PubMed  CAS  Google Scholar 

  • Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 101:6291–6296

    PubMed  CAS  Google Scholar 

  • Kirst ME, Meyer DJ, Gibbon BC, Jung R, Boston RS (2005) Identification and characterization of endoplasmic reticulum-associated degradation proteins differentially affected by endoplasmic reticulum stress. Plant Physiol 138:218–231

    PubMed  CAS  Google Scholar 

  • Kloc M, Etkin LD (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121:287–297

    PubMed  CAS  Google Scholar 

  • Knapp E, Dawson WO, Lewandowski DJ (2001) Conundrum of the lack of defective RNAs (dRNAs) associated with tobamovirus infections: dRNAs that can move are not replicated by the wild-type virus; dRNAs that are replicated by the wild-type virus do not move. J Virol 75:5518–5525

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Knowles RB, Sabry JH, Martone ME, Deerinck TF, Ellisman MH, Bassel GJ, Kosik KS (1996) Translocation of RNA granules in living neurons. J Neurosci 16:7812–7820

    PubMed  CAS  Google Scholar 

  • Kohrmann M, Luo M, Kaether C, DesGroseillers L, Dotti CG, Kiebler MA (1999) Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol Biol Cell 10:2945–2953

    PubMed  CAS  Google Scholar 

  • 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 7:895–904

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Krishnamurthy K, Heppler M, Mitra R, Blancaflor E, Payton M, Nelson RS, Verchot-Lubicz J (2003) The potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virology 309:135–151

    PubMed  CAS  Google Scholar 

  • 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 spread in transgenic plants. Plant J 4:959–970

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lartey R, Ghoshroy S, Ho J, Citovsky V (1997) Movement and subcellular localization of a tobamovirus in Arabidopsis. Plant J 12:537–545

    PubMed  CAS  Google Scholar 

  • Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jürgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 139:1485–1493

    PubMed  CAS  Google Scholar 

  • Lebeurier G, Hirth L (1966) Effect of elevated temperatures on the development of two strains of tobacco mosaic virus. Virology 29:385–395

    PubMed  CAS  Google Scholar 

  • Leopold PL, Pfister KK (2006) Viral strategies for intracellular trafficking: motors and microtubules. Traffic 7:516–523

    PubMed  CAS  Google Scholar 

  • Lewandowski DJ, Dawson WO (2000) Functions of the 126- and 183-kDa proteins of tobacco mosaic virus. Virology 271:90–98

    PubMed  CAS  Google Scholar 

  • Li H, Roossinck MJ (2004) Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 78:10582–10587

    PubMed  CAS  Google Scholar 

  • Lichtscheidl IK, Baluska F (2000) Motility of endoplasmic reticulum in plant cells. In: Staiger CJ, Baluska F, Volkmann D, Barlow PW (eds) Actin, a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 191–201

    Google Scholar 

  • 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 138:1877–1895

    Google Scholar 

  • Lopez LA, Sheetz MP (1993) Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil Cytoskeleton 24:1–16

    PubMed  CAS  Google Scholar 

  • Lucas WJ, Yoo B-C, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2:849–857

    PubMed  CAS  Google Scholar 

  • MacDougall N, Clark A, MacDougall E, Davis I (2003) Drosophila gurken (TGFalpha) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps. Dev Cell 4:307–319

    PubMed  CAS  Google Scholar 

  • Más P, Beachy RN (1999) Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement in intracellular distribution of viral RNA. J Cell Biol 147:945–958

    PubMed  Google Scholar 

  • Más 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

    PubMed  Google Scholar 

  • Matthews REF (1991) Plant virology, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • McLean BG, Zupan J, Zambryski PC (1995) Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco plants. Plant Cell 7:2101–2114

    PubMed  CAS  Google Scholar 

  • Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, Okada Y (1987) Function of the 30k protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6:2557–2563

    PubMed  CAS  Google Scholar 

  • Meshi T, Hosokawa D, Kawagishi M, Watanabe Y, Okada Y (1992) Reinvestigation of intra-cellular localization of the 30 kD protein in tobacco protoplasts infected with tobacco mosaic virus RNA. Virology 187:809–813

    PubMed  CAS  Google Scholar 

  • Mitra R, Krishnamurthy K, Blancaflor E, Payton M, Nelson RS, Verchot-Lubicz J (2003) The potato virus X TGBp2 protein association with the endoplasmic reticulum plays a role in but is not sufficient for viral cell-to-cell movement. Virology 312:35–48

    PubMed  CAS  Google Scholar 

  • Moore P, Fenczik CA, Deom CM, Beachy RN (1992) Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of tobacco mosaic virus. Protoplasma 170:115–127

    Google Scholar 

  • Morozov SY, Solovyev AG (2003) Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366

    PubMed  CAS  Google Scholar 

  • Moser O, Gagey M-J, Godefroy-Colburn T, Stussi-Garaud C, Ellwart-Tschurtz M, Nitschko H, Mundry K-W (1988) The fate of the transport protein of tobacco mosaic virus in systemic and hypersensitive hosts. J Gen Virol 69:1367–1373

    Article  CAS  Google Scholar 

  • Muller J, Piffanelli P, Devoto A, Miklis M, Elliott C, Ortmann B, Schulze-Lefert P, Panstruga R (2005) Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell 17:149–163

    PubMed  Google Scholar 

  • Muslinov IA, Titmus M, Koenig E, Tiedge H (2002) Transport of neuronal BC1 RNA in mauthner axons. J Neurosci 22:4293–4301

    Google Scholar 

  • Niedz RP, Sussman MR, Satterlee JS (1995) Green fluorescent protein: an in vivo reporter of plant gene expression. Plant Cell Rep 14:403–406

    CAS  Google Scholar 

  • Nishiguchi M, Motoyoshi F, Oshima N (1978) Behaviour of a temperature-sensitive strain of tobacco mosaic virus in tomato leaves and protoplasts. J Gen Virol 39:53–61

    Google Scholar 

  • Nogales E, Whittaker M, Milligan RA, Downing KH (1999) High-resolution model of the microtubule. Cell 96:70–88

    Google Scholar 

  • Ohno T, Takamatsu N, Meshi T, Okada Y, Nishigushi M, Kiho Y (1983) Single amino acid substitution in 30k protein of TMV defective in virus transport function. Virology 131:255–258

    PubMed  CAS  Google Scholar 

  • Okita TW, Choi S-B (2002) mRNA localization in plants: targeting to the cell's cortical region and beyond. Curr Opin Plant Biol 5:553–559

    PubMed  CAS  Google Scholar 

  • Oparka K (2005) Plasmodesmata. Blackwell, Oxford

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 9:307–311

    Google Scholar 

  • Padgett HS, Beachy RN (1993) Analysis of a tobacco mosaic virus strain capable of overcoming N gene-mediated resistance. Plant Cell 5:577–586

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Palacios IM, St Johnston D (2001) Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu Rev Cell Dev Biol 17:569–614

    PubMed  CAS  Google Scholar 

  • Pouwels J, Van Der Krogt GN, Van Lent J, Bisseling T, Wellink J (2002) The cytoskeleton and the secretory pathway are not involved in targeting the cowpea mosaic virus movement protein to the cell periphery. Virology 297:48–56

    PubMed  CAS  Google Scholar 

  • Prokhnevsky AI, Peremyslov VV, Dolja VV (2005) Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79:14421–14428

    PubMed  CAS  Google Scholar 

  • Quader H, Hoffman A, Schnepf E (1989) Reorganization of the endoplasmic reticulum in epidermal cells of onion bulb scales after cold stress: involvement of cytoskeletal elements. Planta 177:273–280

    Google Scholar 

  • Radtke K, Dohner K, Sodeik B (2006) Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol 8:387–400

    PubMed  CAS  Google Scholar 

  • Reichel C, Beachy RN (1998) Tobacco mosaic virus infection induces severe morphological changes of the endoplasmatic reticulum. Proc Natl Acad Sci USA 95:11169–11174

    PubMed  CAS  Google Scholar 

  • Reichel C, Beachy RN (2000) Degradation of the tobacco mosaic virus movement protein by the 26S proteasome. J Virol 74:3330–3337

    PubMed  CAS  Google Scholar 

  • Ritzenthaler C, Hofmann C (2007) Tubule-guided movement of plant viruses. In: Waigmann E, Heinlein M (eds) Viral transport in plants. Springer, Heidelberg, pp 63–83

    Google Scholar 

  • Ritzenthaler C, Schmidt A-C, Michler P, Stussi-Garaud C, Pinck L (1995) Grapevine fanleaf nepovirus putative movement protein is involved in tubule formation in vivo. Mol Plant Microbe Interact 8:379–387

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Saito T, Yamanaka K, Okada Y (1990) Long-distance movement and viral assembly of tobacco mosaic virus mutants. Virology 176:329–336

    PubMed  CAS  Google Scholar 

  • Satoh H, Matsuda H, Kawamura T, Isogai M, Yoshikawa N, Takahashi T (2000) Intracellular distribution, cell-to-cell trafficking and tubule-inducing activity of the 50 kDa movement protein of apple chlorotic leaf spot virus fused to green fluorescent protein. J Gen Virol 81:2085–2093

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E (2002) Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 21:4896–4905

    PubMed  CAS  Google Scholar 

  • Serazev TV, Nadezhdina ES, Shanina NA, Leshchiner AD, Kalinina NO, Morozov S (2003) Virions and membrane proteins of the potato X virus interact with microtubules and enables tubulin polymerization in vitro. Mol Biol 37:919–925

    CAS  Google Scholar 

  • Siegel A, Hari V, Kolacz K (1978) The effect of tobacco mosaic virus infection on host and virus-specific protein synthesis in protoplasts. Virology 85:494–503

    PubMed  CAS  Google Scholar 

  • Smith R (2004) Moving molecules: mRNA trafficking in mammalian oligodendrocytes and neurons. Neuroscientist 10:495–500

    PubMed  CAS  Google Scholar 

  • Solovyev AG, Stroganova TA, Zamyatin AAJ, Fedorkin ON, Schiemann J, Morozov SY (2000) Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269:113–127

    PubMed  CAS  Google Scholar 

  • Sossin WS, DesGroseillers L (2006) Intracellular trafficking of RNA in neurons. Traffic 7:1581–1589

    PubMed  CAS  Google Scholar 

  • St Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6:363–375

    PubMed  CAS  Google Scholar 

  • Staehelin LA (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11:1151–1165

    PubMed  CAS  Google Scholar 

  • Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051–1063

    PubMed  CAS  Google Scholar 

  • Sundell CL, Singer RH (1990) Actin mRNA localizes in the absence of protein synthesis. J Cell Biol 111:2397–2403

    PubMed  CAS  Google Scholar 

  • Szécsi J, Ding XS, Lim CO, Bendahmane M, Cho MJ, Nelson RS, Beachy RN (1999) Development of tobacco mosaic virus infection sites in Nicotiana benthamiana. Mol Plant Microbe Interact 2:143–152

    Google Scholar 

  • Tagami Y, Watanabe Y (2007) Effects of brefeldin A on the localization of tobamovirus movement protein and cell-to-cell movement of the virus. Virology 361:133–140

    PubMed  CAS  Google Scholar 

  • Takamatsu K, Ishikawa M, Meshi T, Okada Y (1987) Expression of bacterial chloramphenicol acetyltransferase gene in tobacco plants mediated by TMV-RNA. EMBO J 6:307–311

    PubMed  CAS  Google Scholar 

  • Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Basell GJ (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23:3251–3261

    PubMed  CAS  Google Scholar 

  • Tomenius K, Clapham D, Meshi T (1987) Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363–371

    CAS  PubMed  Google Scholar 

  • Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci 112:2355–2367

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • van Lent JWM, Schmitt-Keichinger C (2006) Viral movement proteins induce tubule formation in plant and insect cells. In: Baluska F, Volkmann D, Barlow PW (eds) Cell–cell channels. Landes Bioscience, Austin

    Google Scholar 

  • von Massow A, Mandelkow EM, Mandelkow E (1989) Interaction between kinesin, microtubules, and microtubule-associated protein 2. Cell Motil Cytoskeleton 14:562–571

    Google Scholar 

  • Waigmann E, Heinlein M (eds) (2007) Viral transport in plants. Springer, Heidelberg

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Waigmann E, Chen M-H, Bachmeier R, Ghoshroy S, Citovsky V (2000) Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J 19:4875–4884

    PubMed  CAS  Google Scholar 

  • Waigmann E, Curin M, Heinlein M (2007) Tobacco mosaic virus—a model for macromolecular cell-to-cell spread. In: Waigmann E, Heinlein M (eds) Viral transport in plants. Springer, Heidelberg, pp 29–62

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Watanabe Y, Emori Y, Ooshika I, Meshi T, Ohno T, Okada Y (1984) Synthesis of TMV-specific RNAs and proteins at the early stage of infection in tobacco protoplasts: transient expression of 30k protein and its mRNA. Virology 133:18–24

    CAS  PubMed  Google Scholar 

  • Watanabe Y, Meshi T, Okada Y (1992) In vivo phosphorylation of the 30-kDa protein of tobacco mosaic virus. FEBS Lett 313:181–184

    PubMed  CAS  Google Scholar 

  • Weil TT, Forrest KM, Gavis ER (2006) Localization of bicoid mRNA in late oocytes is maintained by continual active transport. Dev Cell 11:251–262

    PubMed  CAS  Google Scholar 

  • Whitham SA, Quan S, Chang HS, Cooper B, Estes B, Zhu T, Wang X, Hou YM (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis plants. Plant J 33:271–283

    PubMed  CAS  Google Scholar 

  • Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379

    PubMed  CAS  Google Scholar 

  • Wright KM, Wood NT, Roberts AG, Chapman S, Boevink P, Mackenzie KM, Oparka KJ (2007) Targeting of TMV movement protein to plasmodesmata requires the actin/ER network; evidence from FRAP. Traffic 8:21–31

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Zambryski P (1995) Plasmodesmata: plant channels for molecules on the move. Science 270:1943–1944

    PubMed  CAS  Google Scholar 

  • Zamyatnin AAJ, Solovyev AG, Sablina AA, Agranovsky AA, Katul L, Vetten HJ, Schiemann J, Hinkkanen AE, Lehto K, Morozov SY (2002) Dual-colour imaging of membrane protein targeting directed by poa semilatent virus movement protein TGBp3 in plant and mammalian cells. J Gen Virol 83:651–662

    PubMed  Google Scholar 

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Heinlein, M. (2008). Microtubules and Viral Movement. In: Nick, P. (eds) Plant Microtubules. Plant Cell Monographs, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2007_147

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