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Viral Transport and Interaction with the Host Cytoskeleton

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Plant-Virus Interactions

Abstract

Viruses depend on host cell functions for replication and for spreading their genomes between cells and throughout the organism. The spread of viruses in plants relies on the ability of virus-encoded movement proteins (MPs) and interacting host components to facilitate the transport of the infectious viral genomes through plasmodesmata (PD), the gatable cytoplasmic cell wall channels through which adjacent cells are connected. Studies in the last 20 years have provided insights into the role of membranes and the dynamic cytoskeleton in the cell-to-cell movement of viruses. Using tobacco mosaic virus (TMV) as an example, this article highlights the specific roles of the actin and microtubule cytoskeletons in supporting the endoplasmic reticulum (ER)-associated assembly and trafficking of viral protein:RNA complexes and their targeting to PD.

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References

  • Agbeci M, Grangeon R, Nelson RS, Zheng H, Laliberte JF (2013) Contribution of host intracellular transport machineries to intercellular movement of turnip mosaic virus. PLoS Pathog 9(10):e1003683

    Google Scholar 

  • Akkerman M, Overdijk EJR, Schel JHN, Emons AMC, Ketelaar T (2011) Golgi body motility in the plant cell cortex correlates with actin cytoskeleton organization. Plant Cell Physiol 52(10):1844–1855

    Article  CAS  PubMed  Google Scholar 

  • Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL, Heinlein M, Mely Y, Maule AJ, Ritzenthaler C (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6(9):e1001119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amari K, Lerich A, Schmitt-Keichinger C, Dolja VV, Ritzenthaler C (2011) Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathog 7(10):e1002327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amari K, Di Donato M, Dolja VV, Heinlein M (2014) Myosins VIII and XI play distinct roles in reproduction and transport of tobacco mosaic virus. PLoS Pathog 10(10):e1004448

    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(17):8329–8344

    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 U S A 101(5):1415–1420

    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

    Article  CAS  PubMed  Google Scholar 

  • Avisar D, Prokhnevsky AI, Dolja VV (2008a) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82:2836–2843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008b) Myosin XI-K Is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146(3):1098–1108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avisar D, Abu-Abied M, Belausov E, Sadot E, Hawes C, Sparkes IA (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of golgi and other organelles. Plant Physiol 150:700–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avisar D, Abu-Abied M, Belausov E, Sadot E (2012) Myosin XIK is a major player in cytoplasm dynamics and is regulated by two amino acids in its tail. J Exp Bot 63:241–249

    Article  CAS  PubMed  Google Scholar 

  • Baek GH, Cheng H, Choe V, Bao X, Shao J, Luo S, Rao H (2013) Cdc48: a swiss army knife of cell biology. J Amino Acids 2013:183421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bak A, Gargani D, Macia JL, Malouvet E, Vernerey MS, Blanc S, Drucker M (2013) Virus factories of cauliflower mosaic virus are virion reservoirs that engage actively in vector transmission. J Virol 87(22):12207–12215

    Google Scholar 

  • Baron-Epel O, Hernandez D, Jiang LW, Meiners S, Schindler M (1988) Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Cell Biol 106:715–721

    Article  CAS  PubMed  Google Scholar 

  • Blackman LM, Overall RL (1998) Immunolocalization of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14:733–741

    Article  CAS  Google Scholar 

  • Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15(3):441–447

    Article  CAS  PubMed  Google Scholar 

  • Boutant E, Didier P, Niehl A, Mély Y, Ritzenthaler C, Heinlein M (2010) Fluorescent protein recruitment assay for demonstration and analysis of in vivo protein interactions in plant cells and its application to tobacco mosaic virus movement protein. Plant J 62(1):171–177

    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

    Article  CAS  PubMed  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(4):315–325

    Article  CAS  PubMed  Google Scholar 

  • Boyko V, van der Laak J, Ferralli J, Suslova E, Kwon MO, 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

    Article  CAS  PubMed  PubMed Central  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(8):3974–3980

    Google Scholar 

  • Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M (2007) Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51(4):589–603

    Article  CAS  PubMed  Google Scholar 

  • Brandenburg B, Zhuang X (2007) Virus trafficking – learning from single-virus tracking. Nat Rev Microbiol 5:197–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandizzi F, Wasteneys GO (2013) Cytoskeleton-dependent endomembrane organization in plant cells: an emerging role for microtubules. Plant J 75:339–349

    Article  CAS  PubMed  Google Scholar 

  • Brandner K, Sambade A, Boutant E, Didier P, Mely Y, Ritzenthaler C, Heinlein M (2008) Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol 147:611–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burch-Smith TM, Zambryski PC (2012) Plasmodesmata paradigm shift: regulation from without versus within. Annu Rev Plant Biol 63:239–260

    Article  CAS  PubMed  Google Scholar 

  • Cai G, Cresti M (2012) Are kinesins required for organelle trafficking in plant cells? Front Plant Sci 3:170

    Article  PubMed  PubMed Central  Google Scholar 

  • Carette JE, Guhl K, Wellink J, Van Kammen A (2002) Coalescence of the sites of cowpea mosaic virus RNA replication into a cytopathic structure. J Virol 76:6235–6243

    Google Scholar 

  • Carluccio AV, Zicca S, Stavolone L (2014) Hitching a ride on vesicles: cauliflower mosaic virus movement protein trafficking in the endomembrane system. Plant Physiol 164:1261–1270

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen MH, Tian GW, Gafni Y, Citovsky V (2005) Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 138:1866–1876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin LS, Olzmann JA, Li L (2010) Parkin-mediated ubiquitin signalling in aggresome formation and autophagy. Biochem Soc Trans 38(Pt 1):144–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho SY, Cho WK, Choi HS, Kim KH (2012) Cis-acting element (SL1) of potato virus X controls viral movement by interacting with the NbMPB2Cb and viral proteins. Virology 427:166–176

    Google Scholar 

  • Christensen N, Tilsner J, Bell K, Hammann P, Parton R, Lacomme C, Oparka K (2009) The 5' cap of tobacco mosaic virus (TMV) is required for virion attachment to the actin/endoplasmic reticulum network during early infection. Traffic 10:536–551

    Google Scholar 

  • 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(4):637–647

    Google Scholar 

  • Citovsky V, Knorr D, Zambryski P (1991) Gene I, a potential cell-to-cell movement locus of cauliflower mosaic virus, encodes an RNA-binding protein. Proc Natl Acad Sci U S A 88:2476–2480

    Google Scholar 

  • Citovsky V, Wong ML, Shaw AL, Venkataram Prasad BV, Zambryski P (1992) Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397–411

    Google Scholar 

  • Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C, Wei T, Wang A, Laliberté JF (2009) Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J Virol 83:10460–10471

    Google Scholar 

  • Crosas B, Hanna J, Kirkpatrick DS, Zhang DP, Tone Y, Hathaway NA, Buecker C, Leggett DS, Schmidt M, King RW, Gygi SP, Finley D (2006) Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell 127:1401–1413

    Article  CAS  PubMed  Google Scholar 

  • Csorba T, Bovi A, Dalmay T, Burgyan J (2007) The p122 subunit of tobacco mosaic virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and microRNA-mediated pathways. J Virol 81:11768–11780

    Google Scholar 

  • Cui X, Wei T, Chowda-Reddy RV, Sun G, Wang A (2010) The tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. Virology 397:56–63

    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

    Google Scholar 

  • Dales S, Chardonnet Y (1973) Early events in the interaction of adenoviruses with HeLa cells. IV. Association with microtubules and the nuclear pore complex during vectorial movement of the inoculum. Virology 56:465–483

    Article  CAS  PubMed  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

    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 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

  • Ding B, Kwon M-O, Warnberg L (1996) Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 10:157–164

    Article  Google Scholar 

  • Dodding MP, Way M (2011) Coupling viruses to dynein and kinesin-1. EMBO J 30:3527–3539

    Article  CAS  PubMed  PubMed Central  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(7):320–327

    Article  PubMed  CAS  Google Scholar 

  • Ernst R, Claessen JH, Mueller B, Sanyal S, Spooner E, van der Veen AG, Kirak O, Schlieker CD, Weihofen WA, Ploegh HL (2011) Enzymatic blockade of the ubiquitin-proteasome pathway. PLoS Biol 8:e1000605

    Article  PubMed  CAS  Google Scholar 

  • Esau K, Cronshaw J (1967) Tubular components in cells of healthy and tobacco mosaic virus-infected nicotiana. Virology 33:26–35

    Google Scholar 

  • Faulkner C (2013) Receptor-mediated signaling at plasmodesmata. Front Plant Sci 4:521

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng Z, Chen X, Bao Y, Dong J, Zhang Z, Tao X (2013) Nucleocapsid of tomato spotted wilt tospovirus forms mobile particles that traffic on an actin/endoplasmic reticulum network driven by myosin XI-K. New Phytol 200:1212–1224

    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

    Google Scholar 

  • Foissner I, Menzel D, Wasteneys GO (2009) Microtubule-dependent motility and orientation of the cortical endoplasmic reticulum in elongating characean internodal cells. Cell Motil Cytoskeleton 66:142–155

    Article  CAS  PubMed  Google Scholar 

  • Genoves A, Navarro JA, Pallas V (2009) A self-interacting carmovirus movement protein plays a role in binding of viral RNA during the cell-to-cell movement and shows an actin cytoskeleton dependent location in cell periphery. Virology 395:133–142

    Article  CAS  PubMed  Google Scholar 

  • Genoves A, Navarro JA, Pallas V (2010) The Intra- and intercellular movement of melon necrotic spot virus (MNSV) depends on an active secretory pathway. Mol Plant Microbe Interact 23:263–272

    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

    Google Scholar 

  • Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3

    Article  PubMed  PubMed Central  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

    Google Scholar 

  • Grabski S, de Feijter AW, Schindler M (1993) Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell 5:25–38

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Griffing LR (2010) Networking in the endoplasmic reticulum. Biochem Soc Trans 38:747–753

    Article  CAS  PubMed  Google Scholar 

  • Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL (2008) Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant Microbe Interact 21:335–345

    Article  CAS  PubMed  Google Scholar 

  • Haikonen T, Rajamaki ML, Valkonen JP (2013) Interaction of the microtubule-associated host protein HIP2 with viral helper component proteinase is important in infection with potato virus A. Mol Plant Microbe Interact 26:734–744

    Google Scholar 

  • Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A, Watanabe Y, Hashimoto T, Baskin TI (2012) RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol 53:699–708

    Article  CAS  PubMed  Google Scholar 

  • Hao R, Nanduri P, Rao Y, Panichelli RS, Ito A, Yoshida M, Yao TP (2013) Proteasomes activate aggresome disassembly and clearance by producing unanchored ubiquitin chains. Mol Cell 51:819–828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harries PA, Palanichelvam K, Yu W, Schoelz JE, Nelson RS (2009a) The cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149:1005–1016

    Google Scholar 

  • Harries PA, Park JW, Sasaki N, Ballard KD, Maule AJ, Nelson RS (2009b) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc Natl Acad Sci U S A 106:17594–17599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harries PA, Schoelz JE, Nelson RS (2009c) Covering common ground: F-actin-dependent transport of plant viral protein inclusions reveals a novel mechanism for movement utilized by unrelated viral proteins. Plant Signal Behav 4:454–456

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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

    Google Scholar 

  • Heinlein M (2008) Microtubules and viral movement. In: Nick P (ed) Plant microtubules, vol 11, Plant cell monographs. Springer, Berlin, pp 141–173

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper 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

    Google Scholar 

  • Herranz MC, Pallas V (2004) RNA-binding properties and mapping of the RNA-binding domain from the movement protein of prunus necrotic ringspot virus. J Gen Virol 85(Pt 3):761–768

    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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofmann C, Niehl A, Sambade A, Steinmetz A, Heinlein M (2009) Inhibition of tobacco mosaic virus movement by expression of an actin-binding protein. Plant Physiol 149:1810–1823

    Google Scholar 

  • Holt CA, Beachy RN (1991) In vivo complementation of infectious transcripts from mutant tobacco mosaic virus cDNAs in transgenic plants. Virology 181:109–117

    Google Scholar 

  • Hu Q, Hollunder J, Niehl A, Korner CJ, Gereige D, Windels D, Arnold A, Kuiper M, Vazquez F, Pooggin M, Heinlein M (2011) Specific impact of tobamovirus infection on the Arabidopsis small RNA profile. PLoS One 6:e19549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280:40282–40292

    Article  CAS  PubMed  Google Scholar 

  • Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3:e156

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jansen KA, Wolfs CJ, Lohuis H, Goldbach RW, Verduin BJ (1998) Characterization of the brome mosaic virus movement protein expressed in E. coli. Virology 242:387–394

    Google Scholar 

  • Jarsch IK, Konrad SS, Stratil TF, Urbanus SL, Szymanski W, Braun P, Braun KH, Ott T (2014) Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698–1711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ju JS, Weihl CC (2010) Inclusion body myopathy, Paget’s disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum Mol Genet 19:R38–R45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karpova OV, Ivanov KI, Rodionova P, Dorokhov YL, Atabekov JG (1997) Nontranslatability and dissimilar behavior in plants and protoplasts of viral RNA and movement protein complexes formed in vitro. Virology 230:11–21

    Article  CAS  PubMed  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

    Google Scholar 

  • Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115:727–738

    Article  CAS  PubMed  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 U S A 101:6291–6296

    Google Scholar 

  • Kawamura-Nagaya K, Ishibashi K, Huang YP, Miyashita S, Ishikawa M (2014) Replication protein of tobacco mosaic virus cotranslationally binds the 5' untranslated region of genomic RNA to enable viral replication. Proc Natl Acad Sci U S A 111:E1620–E1628

    Google Scholar 

  • Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51:685–690

    Article  CAS  PubMed  Google Scholar 

  • Kim KS, Fulton JP (1971) Tubules with viruslike particles in leaf cells infected with bean pod mottle virus. Virology 43:329–337

    Google Scholar 

  • Kim KS, Fulton JP (1975) An association of plant cell microtubules and virus particles. Virology 64:560–565

    Article  CAS  PubMed  Google Scholar 

  • Knebel W, Quader H, Schnepf E (1990) Mobile and immobile endoplasmic reticulum in onion bulb epidermis cells: short- and long-term observations with a confocal laser scanning microscope. Eur J Cell Biol 52:328–340

    CAS  PubMed  Google Scholar 

  • Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL (2011) An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol 21:1559–1564

    Article  CAS  PubMed  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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laliberté JF, Sanfacon H (2010) Cellular remodeling during plant virus infection. Annu Rev Phytopathol 48:69–91

    Article  PubMed  CAS  Google Scholar 

  • Langford GM (1995) Actin- and microtubule-dependent organelle motors: interrelationships between the two motility systems. Curr Opin Cell Biol 7:82–88

    Article  CAS  PubMed  Google Scholar 

  • Langhans M, Niemes S, Pimpl P, Robinson DG (2009) Oryzalin bodies: in addition to its anti-microtubule properties, the dinitroaniline herbicide oryzalin causes nodulation of the endoplasmic reticulum. Protoplasma 236:73–84

    Article  CAS  PubMed  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

    Google Scholar 

  • Lee YR, Giang HM, Liu B (2001) A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13:2427–2439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E, Gao YS, Pandey UB, Kaushik S, Tresse E, Lu J, Taylor JP, Cuervo AM, Yao TP (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 29:969–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A 107:2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Ye Y (2012) Roles of p97-associated deubiquitinases in protein quality control at the endoplasmic reticulum. Curr Protein Pept Sci 13:436–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu GQ, Cai G, Del Casino C, Tiezzi A, Cresti M (1994) Kinesin-related polypeptide is associated with vesicles from Corylus avellana pollen. Cell Motil Cytoskeleton 29:155–166

    Article  CAS  PubMed  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

    Article  CAS  Google Scholar 

  • Lu L, Lee YR, Pan R, Maloof JN, Liu B (2005) An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol Biol Cell 16:811–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martens HJ, Roberts AG, Oparka KJ, Schulz A (2006) Quantification of plasmodesmatal endoplasmic reticulum coupling between sieve elements and companion cells using fluorescence redistribution after photobleaching. Plant Physiol 142:471–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinière A, Gargani D, Uzest M, Lautredou N, Blanc S, Drucker M (2009) A role for plant microtubules in the formation of transmission-specific inclusion bodies of cauliflower mosaic virus. Plant J 58:135–146

    Google Scholar 

  • Martinière A, Bak A, Macia JL, Lautredou N, Gargani D, Doumayrou J, Garzo E, Moreno A, Fereres A, Blanc S, Drucker M (2013) A virus responds instantly to the presence of the vector on the host and forms transmission morphs. eLife 2:00183

    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

    Google Scholar 

  • Mayhew DE, Carrol TW (1974) Barley stripe mosaic virions associated with spindle microtubules. Science 185:957–958

    Article  CAS  PubMed  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

    Google Scholar 

  • Morozov SY, Fedorkin ON, Juttner G, Schiemann J, Baulcombe DC, Atabekov JG (1997) Complementation of potato virus X mutant mediated by bombardment of plant tissues with cloned viral movement protein genes. J Gen Virol 78:2077–2081

    Google Scholar 

  • Nakamura M, Ehrhardt DW, Hashimoto T (2010) Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat Cell Biol 12:1064–1070

    Article  CAS  PubMed  Google Scholar 

  • Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–1142

    Article  PubMed  PubMed Central  Google Scholar 

  • Ni CZ, Wang HQ, Xu T, Qu Z, Liu GQ (2005) AtKP1, a kinesin-like protein, mainly localizes to mitochondria in Arabidopsis thaliana. Cell Res 15:725–733

    Article  CAS  PubMed  Google Scholar 

  • Niehl A, Amari K, Gereige D, Brandner K, Mély Y, Heinlein M (2012) Control of tobacco mosaic virus movement protein fate by CELL-DIVISION-CYCLE protein 48. Plant Physiol 160:2093–2108

    Google Scholar 

  • Niehl A, Amari K, Heinlein M (2013a) CDC48 function during TMV infection: regulation of virus movement and replication by degradation? Plant Signal Behav 8:e22865

    Article  PubMed  Google Scholar 

  • Niehl A, Peña EJ, Amari K, Heinlein M (2013b) Microtubules in viral replication and transport. Plant J 75:290–308

    Article  CAS  PubMed  Google Scholar 

  • Niehl A, Pasquier A, Ferriol I, Mély Y, Heinlein M (2014) Comparison of the oilseed rape mosaic virus and tobacco mosaic virus movement proteins (MP) reveals common and dissimilar MP functions for tobamovirus spread. Virology 456–457:43–54

    Google Scholar 

  • Oda Y, Fukuda H (2013) Rho of plant GTPase signaling regulates the behavior of Arabidopsis kinesin-13A to establish secondary cell wall patterns. Plant Cell 25:4439–4450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ojangu EL, Tanner K, Pata P, Jarve K, Holweg CL, Truve E, Paves H (2012) Myosins XI-K, XI-1, and XI-2 are required for development of pavement cells, trichomes, and stigmatic papillae in Arabidopsis. BMC Plant Biol 12:81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osman TAM, Hayes RJ, Buck KW (1992) Cooperative binding of the red clover necrotic mosaic virus movement protein to single stranded nucleic acids. J Gen Virol 73:223–227

    Google Scholar 

  • Ouko MO, Sambade A, Brandner K, Niehl A, Peña E, Ahad A, Heinlein M, Nick P (2010) Tobacco mutants with reduced microtubule dynamics are less susceptible to TMV. Plant J 62:829–839

    Article  CAS  PubMed  Google Scholar 

  • Ouyang H, Ali YO, Ravichandran M, Dong A, Qiu W, MacKenzie F, Dhe-Paganon S, Arrowsmith CH, Zhai RG (2012) Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J Biol Chem 287:2317–2327

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Peiro A, Martinez-Gil L, Tamborero S, Pallas V, Sanchez-Navarro JA, Mingarro I (2013) The tobacco mosaic virus movement protein associates with but does not integrate into biological membranes. J Virol 88:3016–3026

    Google Scholar 

  • Peña EJ, Heinlein M (2013) Cortical microtubule-associated ER sites: organization centers of cell polarity and communication. Curr Opin Plant Biol 16:764–773

    Article  PubMed  CAS  Google Scholar 

  • Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146:1109–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peremyslov VV, Prokhnevsky AI, Dolja VV (2010) Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell 22:1883–1897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peremyslov VV, Mockler TC, Filichkin SA, Fox SE, Jaiswal P, Makarova KS, Koonin EV, Dolja VV (2011) Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol 155:1191–1204

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prokhnevsky AI, Peremyslov VV, Dolja VV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A 105:19744–19749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14:743–750

    Article  CAS  PubMed  Google Scholar 

  • Radford JE, White RG (2011) Inhibitors of myosin, but not actin, alter transport through tradescantia plasmodesmata. Protoplasma 248:205–216

    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

    Article  CAS  PubMed  Google Scholar 

  • Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J, Noirot E, Satiat-Jeunemaitre B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, Reymond P, Simon-Plas F, Farmer EE, Bessoule JJ, Mongrand S (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21:1541–1555

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Reichelt S, Knight AE, Hodge TP, 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

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro D, Jung M, Moling S, Borst JW, Goldbach R, Kormelink R (2013) The cytosolic nucleoprotein of the plant-infecting bunyavirus tomato spotted wilt recruits endoplasmic reticulum-resident proteins to endoplasmic reticulum export sites. Plant Cell 25:3602–3614

    Google Scholar 

  • Robles Luna G, Peña EJ, Borniego MB, Heinlein M, Garcia ML (2013) Ophioviruses CPsV and MiLBVV movement protein is encoded in RNA 2 and interacts with the coat protein. Virology 441:152–161

    Article  CAS  PubMed  Google Scholar 

  • Ruiz MT, Voinnet O, Baulcombe DC (1998) Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:937–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rumpf S, Jentsch S (2006) Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol Cell 21:261–269

    Article  CAS  PubMed  Google Scholar 

  • Runions J, Brach T, Kuhner S, Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57:43–50

    Article  CAS  PubMed  Google Scholar 

  • Sambade A, Brandner K, Hofmann C, Seemanpillai M, Mutterer J, Heinlein M (2008) Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9:2073–2088

    Article  CAS  PubMed  Google Scholar 

  • Sampathkumar A, Lindeboom JJ, Debolt S, Gutierrez R, Ehrhardt DW, Ketelaar T, Persson S (2011) Live cell imaging reveals structural associations between the actin and microtubule cytoskeleton in Arabidopsis. Plant Cell 23:2302–2313

    Article  CAS  PubMed  PubMed Central  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

    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

    Article  CAS  Google Scholar 

  • Serra-Soriano M, Pallas V, Navarro JA (2014) A model for transport of a viral membrane protein through the early secretory pathway: minimal sequence and endoplasmic reticulum lateral mobility requirements. Plant J 77:863–879

    Article  CAS  PubMed  Google Scholar 

  • Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136:3968–3978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shemyakina EA, Solovyev AG, Leonova OG, Popenko VI, Schiemann J, Morozov SY (2011) The role of microtubule association in plasmodesmal targeting of potato mop-top virus movement protein TGBp1. Open Virol J 5:1–11

    Google Scholar 

  • Shoumacher F, Erny C, Berna A, Godefroy-Colburn T, Stussi-Garaud C (1992) Nucleic acid-binding properties of the alfalfa mosaic virus movement protein produced in yeast. Virology 188:896–899

    Google Scholar 

  • Siegel A, Zaitlin M, Sehgal OP (1962) The isolation of defective tobacco mosaic virus strains. Proc Natl Acad Sci U S A 48:1845–1851

    Google Scholar 

  • Simon-Buelo L, García-Arenal F (1999) Virus particles of cucumber green mottle mosaic tobamovirus move systemically in the phloem of infected cucumber plants. Mol Plant Microbe Interact 12:112–118

    Google Scholar 

  • Sparkes I, Runions J, Hawes C, Griffing L (2009a) Movement and remodeling of the endoplasmic reticulum in nondividing cells of tobacco leaves. Plant Cell 21:3937–3949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sparkes IA, Frigerio L, Tolley N, Hawes C (2009b) The plant endoplasmic reticulum: a cell-wide web. Biochem J 423:145–155

    Article  CAS  PubMed  Google Scholar 

  • Sparkes IA, Ketelaar T, de Ruijter NC, Hawes C (2009c) Grab a Golgi: laser trapping of Golgi bodies reveals in vivo interactions with the endoplasmic reticulum. Traffic 10:567–571

    Article  CAS  PubMed  Google Scholar 

  • Spitsin S, Steplewski K, Fleysh N, Belanger H, Mikheeva T, Shivprasad S, Dawson W, Koprowski H, Yusibov V (1999) Expression of alfalfa mosaic virus coat protein in tobacco mosaic virus (TMV) deficient in the production of its native coat protein supports long-distance movement of a chimeric TMV. Proc Natl Acad Sci U S A 96:2549–2553

    Google Scholar 

  • St Johnston D (1995) The intracellular localization of messenger RNAs. Cell 81:161–170

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Su S, Liu Z, Chen C, Zhang Y, Wang X, Zhu L, Miao L, Wang XC, Yuan M (2010) cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22(4):1373–1387

    Google Scholar 

  • Sun Z, Zhang S, Xie L, Zhu Q, Tan Z, Bian J, Sun L, Chen J (2013) The secretory pathway and the actomyosin motility system are required for plasmodesmatal localization of the P7-1 of rice black-streaked dwarf virus. Arch Virol 158:1055–1064

    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 Nicothiana benthamiana. Mol Plant Microbe Interact 2:143–152

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taliansky M, Roberts IM, Kalinina N, Ryabov EV, Raj SK, Robinson DJ, Oparka KJ (2003) An umbraviral protein, involved in long-distance RNA movement, binds viral RNA and forms unique, protective ribonucleoprotein complexes. J Virol 77:3031–3040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:e7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tilsner J, Linnik O, Wright KM, Bell K, Roberts AG, Lacomme C, Santa Cruz S, Oparka KJ (2012) The TGB1 movement protein of potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol 158:1359–1370

    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

    Google Scholar 

  • Torvund-Jensen J, Steengaard J, Reimer L, Fihl LB, Laursen LS (2014) Transport and translation of MBP mRNA is regulated differently by distinct hnRNP proteins. J Cell Sci 127(Pt 7):1550–1564

    Article  CAS  PubMed  Google Scholar 

  • Tromas N, Zwart MP, Lafforgue G, Elena SF (2014) Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLoS Genet 10:e1004186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsai YC, Weissman AM (2011) Ubiquitylation in ERAD: reversing to go forward? PLoS Biol 9:e1001038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda K, Matsuyama T, Hashimoto T (1999) Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206:201–206

    Article  Google Scholar 

  • Ueda H, Yokota E, Kutsuna N, Shimada T, Tamura K, Shimmen T, Hasezawa S, Dolja VV, Hara-Nishimura I (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci U S A 107:6894–6899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vale RD (1987) Intracellular transport using microtubule-based motors. Annu Rev Cell Biol 3:347–378

    Article  CAS  PubMed  Google Scholar 

  • Verchot-Lubicz J, Torrance L, Solovyev AG, Morozov SY, Jackson AO, Gilmer D (2010) Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23:1231–1247

    Article  CAS  PubMed  Google Scholar 

  • Vidali L, Burkart GM, Augustine RC, Kerdavid E, Tuzel E, Bezanilla M (2010) Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell 22:1868–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vijayapalani P, Maeshima M, Nagasaki-Takekuchi N, Miller WA (2012) Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. PLoS Pathog 8:e1002639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogel F, Hofius D, Sonnewald U (2007) Intracellular trafficking of potato leafroll virus movement protein in transgenic Arabidopsis. Traffic 8:1205–1214

    Google Scholar 

  • Vogler H, Akbergenov R, Shivaprasad PV, Dang V, Fasler M, Kwon MO, Zhanybekova S, Hohn T, Heinlein M (2007) Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J Virol 81:10379–10388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward BM (2011) The taking of the cytoskeleton one two three: how viruses utilize the cytoskeleton during egress. Virology 411:244–250

    Article  CAS  PubMed  PubMed Central  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 the 30K protein and its mRNA. Virology 133:18–24

    Article  CAS  PubMed  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

    Google Scholar 

  • Wei L, Zhang W, Liu Z, Li Y (2009) AtKinesin-13A is located on Golgi-associated vesicle and involved in vesicle formation/budding in Arabidopsis root-cap peripheral cells. BMC Plant Biol 9:138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180:169–184

    Article  CAS  Google Scholar 

  • Wightman R, Chomicki G, Kumar M, Carr P, Turner SR (2013) SPIRAL2 determines plant microtubule organization by modulating microtubule severing. Curr Biol 23:1902–1907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wileman T (2006) Aggresomes and autophagy generate sites for virus replication. Science 312:875–878

    Article  CAS  PubMed  Google Scholar 

  • Wolf DH, Stolz A (2012) The Cdc48 machine in endoplasmic reticulum associated protein degradation. Biochim Biophys Acta 1823:117–124

    Article  CAS  PubMed  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

    Google Scholar 

  • Wolf S, Deom CM, Beachy RN, Lucas WJ (1991) Plasmodesmatal function is probed using transgenic plants that express a virus movement protein. Plant Cell 3:593–604

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Wright KM, Cowan GH, Lukhovitskaya NI, Tilsner J, Roberts AG, Savenkov EI, Torrance L (2010) The N-terminal domain of PMTV TGB1 movement protein is required for nucleolar localization, microtubule association, and long-distance movement. Mol Plant Microbe Interact 23:1486–1497

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Gallagher KL (2013) Intact microtubules are required for the intercellular movement of SHORT-ROOT transcription factor. Plant J 74:148–159

    Article  CAS  PubMed  Google Scholar 

  • Yao M, Wakamatsu Y, Itoh TJ, Shoji T, Hashimoto T (2008) Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics. J Cell Sci 121(Pt 14):2372–2381

    Article  CAS  PubMed  Google Scholar 

  • Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414:652–656

    Article  CAS  PubMed  Google Scholar 

  • Yuan Z, Chen H, Chen Q, Omura T, Xie L, Wu Z, Wei T (2011) The early secretory pathway and an actin-myosin VIII motility system are required for plasmodesmatal localization of the NSvc4 protein of rice stripe virus. Virus Res 159:62–68

    Google Scholar 

  • Zhu C, Dixit R (2011) Single molecule analysis of the Arabidopsis FRA1 kinesin shows that it is a functional motor protein with unusually high processivity. Mol Plant 4:879–885

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Dixit R (2012) Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma 249:887–899

    Article  CAS  PubMed  Google Scholar 

  • Zwart MP, Tromas N, Elena SF (2013) Model-selection-based approach for calculating cellular multiplicity of infection during virus colonization of multi-cellular hosts. PLoS One 8:e64657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Heinlein, M. (2016). Viral Transport and Interaction with the Host Cytoskeleton. In: Kleinow, T. (eds) Plant-Virus Interactions. Springer, Cham. https://doi.org/10.1007/978-3-319-25489-0_2

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