Viral Studies Point the Way: Mechanisms of Intercellular Transport

  • Eduardo Peña
  • Annette Niehl
  • Manfred HeinleinEmail author
Part of the Advances in Plant Biology book series (AIPB, volume 3)


Plant development depends on the intercellular transport of macromolecules through gatable channels in the cell wall known as plasmodesmata (PD). Plant viruses exploit this intercellular trafficking pathway to move cell-to-cell and to cause systemic infection. Dependent on viral species, movement through PD can occur in virion or non-virion form and by different mechanisms for targeting and modification of the pore. These mechanisms are supported by viral movement proteins and by other virus-encoded factors that interact among themselves and with plant cellular components to facilitate virus movement in a coordinated and regulated fashion. This chapter provides an overview about current knowledge in virus cell-to-cell movement with the aim to extract principal mechanisms playing a role in intercellular transport.


Tobacco Mosaic Virus Movement Protein Endoplasmic Reticulum Membrane Virus Movement Triple Gene Block 
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.



A.N. and E.P were supported through research grants provided by the HFSPO (RGP2006/22) and the ANR (ANR-08-BLAN-0244).


  1. Akamatsu N, Takeda A, Kishimoto M, Kaido M, Okuno T, Mise K (2007) Phosphorylation and interaction of the movement and coat proteins of Brome mosaic virus in infected barley protoplasts. Arch Virol 152:2087–2093PubMedGoogle Scholar
  2. Alzhanova DV, Napuli AJ, Creamer R, Dolja VV (2001) Cell-to-cell movement and assembly of a plant closterovirus: roles for the capsid proteins and Hsp70 homolog. EMBO J 20:6997–7007PubMedGoogle Scholar
  3. 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:e1001119PubMedGoogle Scholar
  4. Andreev IA, Hyon Kim S, Kalinina NO, Rakitina DV, Fitzgerald AG, Palukaitis P, Taliansky ME (2004) Molecular interactions between a plant virus movement protein and RNA: force spectroscopy investigation. J Mol Biol 339:1041–1047PubMedGoogle Scholar
  5. Aoki K, Kragler F, Xoconostle-Cazares B, Lucas WJ (2002) A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proc Natl Acad Sci USA 99:16342–16347PubMedGoogle Scholar
  6. 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 3:415–423Google Scholar
  7. 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 80:8329–8344PubMedGoogle Scholar
  8. 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 101:1415–1420PubMedGoogle Scholar
  9. 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 72:209–211PubMedGoogle Scholar
  10. Avisar D, Prokhnevsky AI, Dolja VV (2008a) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82:2836–2843PubMedGoogle Scholar
  11. 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 146:1098–1108PubMedGoogle Scholar
  12. Baluska F, Samaj J, Napier R, Volkmann D (1999) Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 19:481–488PubMedGoogle Scholar
  13. 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 106:715–721PubMedGoogle Scholar
  14. Barton DA, Cole L, Collings DA, Liu DY, Smith PM, Day DA, Overall RL (2011) Cell-to-cell transport via the lumen of the endoplasmic reticulum. Plant J 66:806–817PubMedGoogle Scholar
  15. Bayne EH, Rakitina DV, Morozov SY, Baulcombe DC (2005) Cell-to-cell movement of Potato potexvirus X is dependent on suppression of RNA silencing. Plant J 44:471–482PubMedGoogle Scholar
  16. Belin C, Schmitt C, Gaire F, Walter B, Demangeat G, Pinck L (1999) The nine C-terminal residues of the Grapevine fanleaf nepovirus movement protein are critical for systemic virus spread. J Gen Virol 80:1347–1356PubMedGoogle Scholar
  17. Bell K, Oparka K (2011) Imaging plasmodesmata. Protoplasma 248:9–25PubMedGoogle Scholar
  18. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445PubMedGoogle Scholar
  19. Bhat RA, Panstruga R (2005) Lipid rafts in plants. Planta 223:5–19PubMedGoogle Scholar
  20. Blackman LM, Overall RL (1998) Immunolocalization of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14:733–741Google Scholar
  21. Blackman LM, Harper JDI, Overall RL (1999) Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 78:297–304PubMedGoogle Scholar
  22. Blum H, Gross HJ, Beier H (1989) The expression of the TMV-specific 30-kDa protein in tobacco protoplasts is strongly and selectively enhanced by actinomycin. Virology 169:51–61PubMedGoogle Scholar
  23. 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 15:441–447PubMedGoogle Scholar
  24. Boutant E, Fitterer C, Ritzenthaler C, Heinlein M (2009) Interaction of the Tobacco mosaic virus movement protein with microtubules during the cell cycle in tobacco BY-2 cells. Protoplasma 237:3–12PubMedGoogle Scholar
  25. Boyko V, Ferralli J, Heinlein M (2000a) Cell-to-cell movement of TMV RNA is temperature-dependent and corresponds to the association of movement protein with microtubules. Plant J 22:315–325PubMedGoogle Scholar
  26. Boyko V, Ferralli J, Ashby J, Schellenbaum P, Heinlein M (2000b) Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2:826–832PubMedGoogle Scholar
  27. 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 74:11339–11346PubMedGoogle Scholar
  28. 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 76:3974–3980PubMedGoogle Scholar
  29. 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 51:589–603PubMedGoogle Scholar
  30. Brandner K, Sambade A, Boutant E, Didier P, Mely Y, Ritzenthaler C, Heinlein M (2008) TMV movement protein interacts with GFP-tagged microtubule Endbinding Protein 1 (EB1). Plant Physiol 147:611–623PubMedGoogle Scholar
  31. 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 97:7112–7117PubMedGoogle Scholar
  32. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533–544PubMedGoogle Scholar
  33. Bucher GL, Tarina C, Heinlein M, Di Serio F, Meins F Jr, Iglesias VA (2001) Local expression of enzymatically active class 1 beta-1,3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28:361–369PubMedGoogle Scholar
  34. Burch-Smith TM, Zambryski PC (2010) Loss of increased size exclusion limit (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Curr Biol 20:989–993PubMedGoogle Scholar
  35. Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC (2011) Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248:61–74PubMedGoogle Scholar
  36. Cantrill LC, Overall RL, Goodwin PB (1999) Cell-to-cell communication via plant endomembranes. Cell Biol Int 23:653–661PubMedGoogle Scholar
  37. Canut H, Carrasco A, Galaud JP, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16:63–71PubMedGoogle Scholar
  38. Cao M, Ye X, Willie K, Lin J, Zhang X, Redinbaugh MG, Simon AE, Morris TJ, Qu F (2010) The capsid protein of Turnip crinkle virus overcomes two separate defense barriers to facilitate systemic movement of the virus in Arabidopsis. J Virol 84:7793–7802PubMedGoogle Scholar
  39. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321PubMedGoogle Scholar
  40. Carrington JC, Jensen PE, Schaad MC (1998) Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14:393–400PubMedGoogle Scholar
  41. Carvalho CM, Wellink J, Ribeiro SG, Goldbach RW, Van Lent JW (2003) The C-terminal region of the movement protein of Cowpea mosaic virus is involved in binding to the large but not to the small coat protein. J Gen Virol 84:2271–2277PubMedGoogle Scholar
  42. Carvalho MF, Turgeon R, Lazarowitz SG (2006) The geminivirus nuclear shuttle protein NSP inhibits the activity of AtNSI, a vascular-expressed Arabidopsis acetyltransferase regulated with the sink-to-source transition. Plant Physiol 140:1317–1330PubMedGoogle Scholar
  43. Carvalho CM, Fontenelle MR, Florentino LH, Santos AA, Zerbini FM, Fontes EP (2008) A novel nucleocytoplasmic traffic GTPase identified as a functional target of the bipartite geminivirus nuclear shuttle protein. Plant J 55:869–880PubMedGoogle Scholar
  44. 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: 223–230PubMedGoogle Scholar
  45. Chen M-H, Citovsky V (2003) Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant J 35:386–392PubMedGoogle Scholar
  46. Chen M-H, Sheng J, Hind G, Handa AK, 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 19:913–920PubMedGoogle Scholar
  47. Chen MH, Tian GW, Gafni Y, Citovsky V (2005) Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 138:1866–1876PubMedGoogle Scholar
  48. Cheng CP, Tzafrir I, Lockhart BE, Olszewski NE (1998) Tubules containing virions are present in plant tissues infected with Commelina yellow mottle badnavirus. J Gen Virol 79:925–929PubMedGoogle Scholar
  49. Chichili GR, Rodgers W (2009) Cytoskeleton-membrane interactions in membrane raft structure. Cell Mol Life Sci 66:2319–2328PubMedGoogle Scholar
  50. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554PubMedGoogle Scholar
  51. Chowdhury SR, Savithri HS (2011) Interaction of Sesbania mosaic virus movement protein with the coat protein – implications for viral spread. FEBS J 278:257–272PubMedGoogle Scholar
  52. 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/ER network during early infection. Traffic 10:536–551PubMedGoogle Scholar
  53. 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 60:637–647PubMedGoogle Scholar
  54. 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 4:397–411PubMedGoogle Scholar
  55. 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 7:904–910PubMedGoogle Scholar
  56. Cleland RE, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178:81–85PubMedGoogle Scholar
  57. Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C, Wei T, Wang A, Laliberte 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 83:10460–10471PubMedGoogle Scholar
  58. 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 298:106–115PubMedGoogle Scholar
  59. Crawford KM, Zambryski PC (2000) Subcellular localization determines the availability of ­non-targeted proteins to plasmodesmatal transport. Curr Biol 10:1032–1040PubMedGoogle Scholar
  60. Crawford KM, Zambryski PC (2001) Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol 125: 1802–1812PubMedGoogle Scholar
  61. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425PubMedGoogle Scholar
  62. 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 143:801–811PubMedGoogle Scholar
  63. Deom CM, Oliver MJ, Beachy RN (1987) The 30-kilodalton gene product of Tobacco mosaic virus potentiates virus movement. Science 237:384–389Google Scholar
  64. Desvoyes B, Faure-Rabasse S, Chen MH, Park JW, Scholthof HB (2002) A novel plant homeodomain protein interacts in a functionally relevant manner with a virus movement protein. Plant Physiol 129:1521–1532PubMedGoogle Scholar
  65. Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426PubMedGoogle Scholar
  66. Ding B, Turgeon R, Parthasarathy MV (1992a) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41Google Scholar
  67. Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ (1992b) Secondary plasmodesmata are specific sites of localization of the Tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4:915–928PubMedGoogle Scholar
  68. 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 10:157–164Google Scholar
  69. Dolja VV, Haldeman R, Robertson NL, Dougherty WG, Carrington JC (1994) Distinct functions of capsid protein in assembly and movement of Tobacco etch virus. EMBO J 13:1482–1491PubMedGoogle Scholar
  70. Dolja VV, Haldeman-Cahill R, Montgomery AE, Vandenbosch KA, Carrington JC (1995) Capsid protein determinants involved in cell-to-cell and long distance movement of Tobacco etch potyvirus. Virology 206:1007–1016PubMedGoogle Scholar
  71. Dolja VV, Kreuze JF, Valkonen JPT (2006) Comparative and functional genomics of closteroviruses. Virus Res 117:38–51PubMedGoogle Scholar
  72. Dorokhov YL, Alexandrov NM, Miroshnichenko NA, Atabekov JG (1983) Isolation and analysis of virus-specific ribonucleoprotein of Tobacco mosaic virus-infected tobacco. Virology 127: 237–252PubMedGoogle Scholar
  73. 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 137:127–134PubMedGoogle Scholar
  74. Dorokhov YL, Mäkinen K, Yu O, 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 461:223–228PubMedGoogle Scholar
  75. Dunoyer P, Thomas C, Harrison S, Revers F, Maule A (2004) A cysteine-rich plant protein potentiates potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78:2301–2309PubMedGoogle Scholar
  76. 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 37:1356–1360PubMedGoogle Scholar
  77. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010a) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912–916PubMedGoogle Scholar
  78. Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F, Alioua A, Himber C, Voinnet O (2010b) An endogenous, systemic RNAi pathway in plants. EMBO J 29:1699–1712PubMedGoogle Scholar
  79. Ehlers K, van Bel AJ (2010) Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231:371–385PubMedGoogle Scholar
  80. Epel BL (2009) Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host beta-1,3-glucanases. Semin Cell Dev Biol 20:1074–1081PubMedGoogle Scholar
  81. Erhardt M, Stussi-Garaud C, Guilley H, Richards KE, Jonard G, Bouzoubaa S (1999) The first triple gene block protein of Peanut clump virus localizes to the plasmodesmata during virus infection. Virology 264:220–229PubMedGoogle Scholar
  82. Erhardt M, Morant M, Ritzenthaler C, Stussi-Garaud C, Guilley H, Richards K, Jonard G, Bouzoubaa S, Gilmer D (2000) P42 movement protein of Beet necrotic yellow vein virus is targeted by the movement proteins P13 and P15 to punctate bodies associated with plasmodesmata. Mol Plant Microbe Interact 13:520–528PubMedGoogle Scholar
  83. Faik A, Laboure AM, Gulino D, Mandaron P, Falconet D (1998) A plant surface protein sharing structural properties with animal integrins. Eur J Biochem 253:552–559PubMedGoogle Scholar
  84. Faulkner C, Maule A (2010) Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248:27–38PubMedGoogle Scholar
  85. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A (2011) Arabidopsis plasmodesmal proteome. PLoS One 6:e18880PubMedGoogle Scholar
  86. 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 80:5807–5821PubMedGoogle Scholar
  87. Fitzgibbon J, Bell K, King E, Oparka K (2010) Super-resolution imaging of plasmodesmata using three-dimensional structured illumination microscopy. Plant Physiol 153:1453–1463PubMedGoogle Scholar
  88. Florentino LH, Santos AA, Fontenelle MR, Pinheiro GL, Zerbini FM, Baracat-Pereira MC, Fontes EP (2006) A PERK-like receptor kinase interacts with the geminivirus nuclear shuttle protein and potentiates viral infection. J Virol 80:6648–6656PubMedGoogle Scholar
  89. Foster RLS, Beck DL, Guilford PJ, Voot DM, Van Dolleweerd CJ, Andersen MT (1992) The coat protein of White clover mosaic potexvirus has a role in facilitating cell-to-cell transport in plants. Virology 191:480–484Google Scholar
  90. Fridborg I, Grainger J, Page A, Coleman M, Findlay K, Angell S (2003) TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X. Mol Plant Microbe Interact 16:132–140PubMedGoogle Scholar
  91. Fujiki M, Kawakami S, Kim RW, Beachy RN (2006) Domains of Tobacco mosaic virus movement protein essential for its membrane association. J Gen Virol 87:2699–2707PubMedGoogle Scholar
  92. Gardiner WE, Sunter G, Brand L, Elmer JS, Rogers SG, Bisaro DM (1988) Genetic analysis of Tomato golden mosaic virus: the coat protein is not required for systemic spread or symptom development. EMBO J 7:899–904PubMedGoogle Scholar
  93. 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: 263–272PubMedGoogle Scholar
  94. Giddings TH, Staehelin LA (1978) Plasma membrane architecture of Anabaena cylindrica: occurrence of microplasmodesmata and changes associated with heterocyst development and the cell cycle. Eur J Cell Biol 16:235–249Google Scholar
  95. 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 14:1207–1222PubMedGoogle Scholar
  96. Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3PubMedGoogle Scholar
  97. 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 84:985–994PubMedGoogle Scholar
  98. Grabski S, de Feijter AW, Schindler M (1993) Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell 5:25–38PubMedGoogle Scholar
  99. Grieco F, Castellano MA, Di Sansebastiano GP, Maggipinto G, Neuhaus JM, Martelli GP (1999) Subcellular localization and in vivo identification of the putative movement protein of Olive latent virus 2. J Gen Virol 80(Pt 5):1103–1109PubMedGoogle Scholar
  100. Griffing LR (2010) Networking in the endoplasmic reticulum. Biochem Soc Trans 38:747–753PubMedGoogle Scholar
  101. 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 21:335–345PubMedGoogle Scholar
  102. Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, Kanaoka MM, Hong Z, Torii KU (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8). Development 137:1731–1741PubMedGoogle Scholar
  103. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11:797–806PubMedGoogle Scholar
  104. 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: 715–724PubMedGoogle Scholar
  105. Ham B-K, Lee T-H, You JS, Nam Y-W, Kim J-K, Paek K-H (1999) Isolation of a putative tobacco host factor interacting with Cucumber mosaic virus 2b protein by yeast two-hybrid screening. Mol Cells 9:548–555PubMedGoogle Scholar
  106. Harries PA, Schoelz JE, Nelson RS (2009a) 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 4:454–456PubMedGoogle Scholar
  107. Harries PA, Palanichelvam K, Yu W, Schoelz JE, Nelson RS (2009b) The Cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149:1005–1016PubMedGoogle Scholar
  108. Harries PA, Park JW, Sasaki N, Ballard KD, Maule AJ, Nelson RS (2009c) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc Natl Acad Sci USA 106:17594–17599PubMedGoogle Scholar
  109. 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 17:164–181PubMedGoogle Scholar
  110. Havelda Z, Maule AJ (2000) Complex spatial responses to Cucumber mosaic virus infection in susceptible Cucurbita pepo cotyledons. Plant Cell 12:1975–1985PubMedGoogle Scholar
  111. Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14(Supplement):S303–S325PubMedGoogle Scholar
  112. Heinlein M (2002) Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signalling. Curr Opin Plant Biol 5:543–552PubMedGoogle Scholar
  113. Heinlein M (2005) Systemic RNA silencing. In: Oparka K (ed) Plasmodesmata. Oxford, Blackwell, pp 212–240Google Scholar
  114. 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 176–182Google Scholar
  115. Heinlein M, Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol 235:93–164PubMedGoogle Scholar
  116. Heinlein M, Epel BL, Padgett HS, Beachy RN (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270:1983–1985PubMedGoogle Scholar
  117. Heinlein M, Wood MR, Thiel T, Beachy RN (1998a) Targeting and modification of prokaryotic cell-cell junctions by Tobacco mosaic virus cell-to-cell movement protein. Plant J 14:345–351PubMedGoogle Scholar
  118. Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN (1998b) Changing patterns of localization of the Tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107–1120PubMedGoogle Scholar
  119. Hirashima K, Watanabe Y (2001) Tobamovirus replicase coding region is involved in cell-to-cell movement. J Virol 75:8831–8836PubMedGoogle Scholar
  120. 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: 12357–12362PubMedGoogle Scholar
  121. Hofius D, Maier AT, Dietrich C, Jungkunz I, Bornke F, Maiss E, Sonnewald U (2007) Capsid protein-mediated recruitment of host DnaJ-like proteins is required for Potato virus Y infection in tobacco plants. J Virol 81:11870–11880PubMedGoogle Scholar
  122. Hofmann C, Sambade A, Heinlein M (2007) Plasmodesmata and intercellular transport of viral RNA. Biochem Soc Trans 35:142–145PubMedGoogle Scholar
  123. 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 149:1810–1823PubMedGoogle Scholar
  124. Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL (2000) Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329–335PubMedGoogle Scholar
  125. Holt CA, Beachy RN (1991) In vivo complementation of infectious transcripts from mutant Tobacco mosaic virus cDNAs in transgenic plants. Virology 181:109–117PubMedGoogle Scholar
  126. Howard AR, Heppler ML, Ju HJ, Krishnamurthy K, Payton ME, Verchot-Lubicz J (2004) Potato virus X TGBp1 induces plasmodesmata gating and moves between cells in several host species whereas CP moves only in N. benthamiana leaves. Virology 328:185–197PubMedGoogle Scholar
  127. Huang Z, Andianov VM, Han Y, Howell SH (2001) Identification of Arabidopsis proteins that interact with the Cauliflower mosaic virus (CaMV) movement protein. Plant Mol Biol 47: 663–675PubMedGoogle Scholar
  128. 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 309:1694–1696PubMedGoogle Scholar
  129. Iglesias VA, Meins F Jr (2000) Movement of plant viruses is delayed in a β-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21:157–166PubMedGoogle Scholar
  130. Ishiwatari Y, Fujiwara T, McFarland KC, Nemoto K, Hayashi H, Chino M, Lucas WJ (1998) Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta 205:12–22PubMedGoogle Scholar
  131. Jackson AO, Lim HS, Bragg J, Ganesan U, Lee MY (2009) Hordeivirus replication, movement, and pathogenesis. Annu Rev Phytopathol 47:385–422PubMedGoogle Scholar
  132. Jimenez I, Lopez L, Alamillo JM, Valli A, Garcia JA (2006) Identification of a Plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol Plant Microbe Interact 19:350–358PubMedGoogle Scholar
  133. 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 138:1877–1895PubMedGoogle Scholar
  134. 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 15:15–25PubMedGoogle Scholar
  135. Kaido M, Inoue Y, Takeda Y, Sugiyama K, Takeda A, Mori M, Tamai A, Meshi T, Okuno T, Mise K (2007) Downregulation of the NbNACa1 gene encoding a movement-protein-interacting protein reduces cell-to-cell movement of Brome mosaic virus in Nicotiana benthamiana. Mol Plant Microbe Interact 20:671–681PubMedGoogle Scholar
  136. Kalinina NO, Rakitina DA, Solovyev AG, Schiemann J, Morozov SY (2002) RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296:321–329PubMedGoogle Scholar
  137. 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 230:11–21PubMedGoogle Scholar
  138. 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 261:20–24PubMedGoogle Scholar
  139. 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 77:2857–2864PubMedGoogle Scholar
  140. Kawakami S, Padgett HS, Hosokawa D, Okada Y, Beachy RN, Watanabe Y (1999) Phosphorylation and/or presence of serine 37 in the movement protein of Tomato mosaic tobamovirus is essential for intracellular localization and stability in vivo. J Virol 73:6831–6840PubMedGoogle Scholar
  141. Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 101:6291–6296PubMedGoogle Scholar
  142. Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92PubMedGoogle Scholar
  143. Kim JY (2005) Regulation of short-distance transport of RNA and protein. Curr Opin Plant Biol 8:45–52PubMedGoogle Scholar
  144. Kim JY, Yan Z, Cilia M, Khalfan-Jagani Z, Jackson D (2002) Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc Natl Acad Sci USA 99:4103–4108PubMedGoogle Scholar
  145. Kim SH, Kalinina NO, Andreev I, Ryabov EV, Fitzgerald AG, Taliansky ME, Palukaitis P (2004) The C-terminal 33 amino acids of the Cucumber mosaic virus 3a protein affect virus movement, RNA binding and inhibition of infection and translation. J Gen Virol 85:221–230PubMedGoogle Scholar
  146. Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC (2005a) Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci USA 102:2227–2231PubMedGoogle Scholar
  147. Kim JY, Rim Y, Wang J, Jackson D (2005b) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev 19:788–793PubMedGoogle Scholar
  148. Kim SH, Macfarlane S, Kalinina NO, Rakitina DV, Ryabov EV, Gillespie T, Haupt S, Brown JW, Taliansky M (2007) Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc Natl Acad Sci USA 104: 11115–11120PubMedGoogle Scholar
  149. Kitajima EW, Lauritis JA, Swift H (1969) Fine structure of zinnial leaf tissues infected with Dahlia mosaic virus. Virology 39:240–249PubMedGoogle Scholar
  150. Kleinow T, Nischang M, Beck A, Kratzer U, Tanwir F, Preiss W, Kepp G, Jeske H (2009) Three C-terminal phosphorylation sites in the Abutilon mosaic virus movement protein affect symptom development and viral DNA accumulation. Virology 390:89–101PubMedGoogle Scholar
  151. 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 7:895–904Google Scholar
  152. Kragler F, Monzer J, Shash K, Xoconoctle-Cazares B, Lucas WJ (1998) Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J 15:367–381Google Scholar
  153. Kragler F, Monzer J, Xoconostle-Cazares B, Lucas WJ (2000) Peptide antagonists of the plasmodesmal macromolecular trafficking pathway. EMBO J 19:2856–2868PubMedGoogle Scholar
  154. 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 132:1870–1883PubMedGoogle Scholar
  155. Krenz B, Windeisen V, Wege C, Jeske H, Kleinow T (2010) A plastid-targeted heat shock cognate 70 kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 401:6–17PubMedGoogle Scholar
  156. 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 309:135–151PubMedGoogle Scholar
  157. Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T, Sato S, Tabata S, Okada K, Wada T (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132:5387–5398PubMedGoogle Scholar
  158. 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 15:2058–2075PubMedGoogle Scholar
  159. Laval V, Chabannes M, Carriere M, Canut H, Barre A, Rouge P, Pont-Lezica R, Galaud J (1999) A family of Arabidopsis plasma membrane receptors presenting animal beta-integrin domains. Biochim Biophys Acta 1435:61–70PubMedGoogle Scholar
  160. Lawrence DM, Jackson AO (2001) Interactions of the TGB1 protein during cell-to-cell movement of Barley stripe mosaic virus. J Virol 75:8712–8723PubMedGoogle Scholar
  161. Lee JY, Lu H (2011) Plasmodesmata: the battleground against intruders. Trends Plant Sci 16: 201–210PubMedGoogle Scholar
  162. Lee J-Y, Yoo B-C, Lucas WJ (2000) Parallels between nuclear-pore and plasmodesmal trafficking of informational molecules. Planta 210:177–187PubMedGoogle Scholar
  163. Lee J-Y, Yoo B-C, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–396PubMedGoogle Scholar
  164. 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 17:2817–2831PubMedGoogle Scholar
  165. Lee SC, Wu CH, Wang CW (2010) Traffic of a viral movement protein complex to the highly curved tubules of the cortical endoplasmic reticulum. Traffic 11:912–930PubMedGoogle Scholar
  166. Lekkerkerker A, Wellink J, Yuan P, van Lent J, Goldbach R, van Kammen AB (1996) Distinct functional domains in the Cowpea mosaic virus movement protein. J Virol 70:5658–5661PubMedGoogle Scholar
  167. Leonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, Laliberte JF (2000) Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol 74:7730–7737PubMedGoogle Scholar
  168. Leonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberte JF (2004) Interaction of VPg-Pro of Turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J Gen Virol 85:1055–1063PubMedGoogle Scholar
  169. Levy A, Erlanger M, Rosenthal M, Epel BL (2007) A plasmodesmata-associated beta-1,3-­glucanase in Arabidopsis. Plant J 49:669–682PubMedGoogle Scholar
  170. Lew RR (1994) Regulation of electrical coupling between Arabidopsis root hairs. Planta 193: 67–73Google Scholar
  171. Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci USA 107:2491–2496PubMedGoogle Scholar
  172. Li Q, Palukaitis P (1996) Comparison of the nucleic acid- and NTP-binding properties of the movement protein of Cucumber mosaic cucumovirus and Tobacco mosaic tobamovirus. Virology 216:71–79PubMedGoogle Scholar
  173. Li Y, Wu MY, Song HH, Hu X, Qiu BS (2005) Identification of a tobacco protein interacting with Tomato mosaic virus coat protein and facilitating long-distance movement of virus. Arch Virol 150:1993–2008PubMedGoogle Scholar
  174. Lim HS, Bragg JN, Ganesan U, Lawrence DM, Yu J, Isogai M, Hammond J, Jackson AO (2008) Triple gene block protein interactions involved in movement of Barley stripe mosaic virus. J Virol 82:4991–5006PubMedGoogle Scholar
  175. Lin B, Heaton LA (2001) An Arabidopsis thaliana protein interacts with a movement protein of Turnip crinkle virus in yeast cells and in vitro. J Gen Virol 82:1245–1251PubMedGoogle Scholar
  176. Liu H, Boulton MI, Oparka KJ, Davies JW (2001) Interaction of the movement and coat proteins of Maize streak virus: implications for the transport of viral DNA. J Gen Virol 82:35–44PubMedGoogle Scholar
  177. 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 138:1877–1895Google Scholar
  178. Lough TJ, Shash K, Xoconostle-Cazares B, Hofstra KR, Beck DL, Balmori E, Forster RL, Lucas WJ (1998) Molecular dissection of the mechanism by which potexvirus triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol Plant Microbe Interact 11:801–814Google Scholar
  179. Lough TJ, Netzler NE, Emerson SJ, Sutherland P, Carr F, Beck DL, Lucas WJ, Forster RL (2000) Cell-to-cell movement of potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Mol Plant Microbe Interact 13:962–974PubMedGoogle Scholar
  180. Luby-Phelps K (2000) Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int Rev Cytol 192:189–221PubMedGoogle Scholar
  181. Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184PubMedGoogle Scholar
  182. Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its RNA through plasmodesmata. Science 270:1980–1983PubMedGoogle Scholar
  183. Lucas WJ, Yoo B-C, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2:849–857PubMedGoogle Scholar
  184. Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata – bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503PubMedGoogle Scholar
  185. Makarov VV, Rybakova EN, Efimov AV, Dobrov EN, Serebryakova MV, Solovyev AG, Yaminsky IV, Taliansky ME, Morozov SY, Kalinina NO (2009) Domain organization of the N-terminal portion of hordeivirus movement protein TGBp1. J Gen Virol 90:3022–3032PubMedGoogle Scholar
  186. Mariano AC, Andrade MO, Santos AA, Carolino SM, Oliveira ML, Baracat-Pereira MC, Brommonshenkel SH, Fontes EP (2004) Identification of a novel receptor-like protein kinase that interacts with a geminivirus nuclear shuttle protein. Virology 318:24–31PubMedGoogle Scholar
  187. 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 142:471–480PubMedGoogle Scholar
  188. 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 147:945–958PubMedGoogle Scholar
  189. Matsushita Y, Hanazawa K, Yoshioka K, Oguchi T, Kawakami S, Watanabe Y, Nishiguchi M, Nyunoya H (2000) In vitro phosphorylation of the movement protein of Tomato mosaic tobamovirus by a cellular kinase. J Gen Virol 81:2095–2102PubMedGoogle Scholar
  190. Matsushita Y, Deguchi M, Youda M, Nishiguchi M, Nyunoya H (2001) The Tomato mosaic tobamovirus movement protein interacts with a putative transcriptional coactivator KELP. Mol Cells 12:57–66PubMedGoogle Scholar
  191. Matsushita M, Miyakawa O, Deguchi M, Nishiguchi M, Nyunoya H (2002) Cloning of a tobacco cDNA coding for a putative transcriptional coactivator MBF1 that interacts with the Tomato mosaic virus movement protein. J Exp Bot 53:1531–1532PubMedGoogle Scholar
  192. Matsushita Y, Ohshima M, Yoshioka K, Nishiguchi M, Nyunoya H (2003) The catalytic subunit of protein kinase CK2 phosphorylates in vitro the movement protein of Tomato mosaic virus. J Gen Virol 84:497–505PubMedGoogle Scholar
  193. Maule AJ (2008) Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol 11: 680–686PubMedGoogle Scholar
  194. McGarry RC, Barron YD, Carvalho MF, Hill JE, Gold D, Cheung E, kraus WL, Lazarowitz SG (2003) A novel Arabidopsis acetyltransferase interacts with the geminivirus movement protein NSP. Plant Cell 15:1605–1618PubMedGoogle Scholar
  195. McLean BG, Zupan J, Zambryski PC (1995) Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco plants. Plant Cell 7:2101–2114PubMedGoogle Scholar
  196. Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, Okada Y (1987) Function of the 30 kd ­protein of Tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6:2557–2563PubMedGoogle Scholar
  197. Meusser B, Hirsch C, Jarosch E, Sommer T (2005) ERAD: the long road to destruction. Nat Cell Biol 7:766–772PubMedGoogle Scholar
  198. Min BE, Martin K, Wang RY, Tafelmeyer P, Bridges M, Goodin M (2010) A host-factor interaction and localization map for a plant-adapted rhabdovirus implicates cytoplasm-tethered transcription activators in cell-to-cell movement. Mol Plant Microbe Interact 23:1420–1432PubMedGoogle Scholar
  199. Modena NA, Zelada AM, Conte F, Mentaberry A (2008) Phosphorylation of the TGBp1 movement protein of Potato virus X by a Nicotiana tabacum CK2-like activity. Virus Res 137:16–23PubMedGoogle Scholar
  200. 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 170:115–127Google Scholar
  201. Morozov SY, Solovyev AG (2003) Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366PubMedGoogle Scholar
  202. Morvan O, Quentin M, Jauneau A, Mareck A, Morvan C (1998) Immunogold localization of pectin methylesterases in the cortical tissues of flax hypocotyl. Protoplasma 202:175–184Google Scholar
  203. Nagano H, Mise K, Furusawa I, Okuno T (2001) Conversion in the requirement of coat protein in cell-to-cell movement mediated by the Cucumber mosaic virus movement protein. J Virol 75:8045–8053PubMedGoogle Scholar
  204. Nagpal P, Quatrano RS (1999) Isolation and characterization of a cDNA clone from Arabidopsis thaliana with partial sequence similarity to integrins. Gene 230:33–40PubMedGoogle Scholar
  205. Noris E, Vaira AM, Caciagli P, Masenga V, Gronenborn B, Accotto GP (1998) Amino acids in the capsid protein of Tomato yellow leaf curl virus that are crucial for systemic infection, particle formation, and insect transmission. J Virol 72:10050–10057PubMedGoogle Scholar
  206. Northcote DH, Davey R, Lay J (1989) Use of antisera to localize callose, xylan and arabinogalactan in the cell-plate, primary and secondary walls of plant-cells. Planta 178:353–366Google Scholar
  207. Nziengui H, Bouhidel K, Pillon D, Der C, Marty F, Schoefs B (2007) Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Lett 581:3356–3362PubMedGoogle Scholar
  208. 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 12:781–789PubMedGoogle Scholar
  209. 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 97:743–754PubMedGoogle Scholar
  210. 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 62:829–839PubMedGoogle Scholar
  211. Overall RL (1999) Structure of plasmodesmata. In: van Bel AJE, van Kesteren WJP (eds) Plasmodesmata, structure, function, role in cell communication. Springer, Berlin/Heidelberg/New York, pp 129–148Google Scholar
  212. Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 9:307–311Google Scholar
  213. Paape M, Solovyev AG, Erokhina TN, Minina EA, Schepetilnikov MV, Lesemann DE, Schiemann J, Morozov SY, Kellmann JW (2006) At-4/1, an interactor of the Tomato spotted wilt virus movement protein, belongs to a new family of plant proteins capable of directed intra- and intercellular trafficking. Mol Plant Microbe Interact 19:874–883PubMedGoogle Scholar
  214. 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 10:1079–1088PubMedGoogle Scholar
  215. Padidam M, Beachy RN, Fauquet CM (1995) Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol 76:25–35PubMedGoogle Scholar
  216. Perbal M-C, Thomas CL, Maule AJ (1993) Cauliflower mosaic virus gene I product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195: 281–285PubMedGoogle Scholar
  217. Perbal M-C, Haughn G, Saedler H, Schwarz-Sommer Z (1996) Non-autonomous function of Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–3441PubMedGoogle Scholar
  218. Peremyslov VV, Hagiwara Y, Dolya VV (1999) HSP70 homolog functions in cell-to-cell movement of a plant virus. Proc Natl Acad Sci USA 96:14771–14776PubMedGoogle Scholar
  219. 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 297:48–56PubMedGoogle Scholar
  220. Pouwels J, van der Velden T, Willemse J, Borst JW, van Lent J, Bisseling T, Wellink J (2004) Studies on the origin and structure of tubules made by the movement protein of Cowpea mosaic virus. J Gen Virol 85:3787–3796PubMedGoogle Scholar
  221. Prokhnevsky AI, Peremyslov VV, Dolja VV (2005) Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79:14421–14428PubMedGoogle Scholar
  222. 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 USA 105:19744–19749PubMedGoogle Scholar
  223. Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14:743–750PubMedGoogle Scholar
  224. Radford JE, White RG (2011) Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata. Protoplasma 248:205–216PubMedGoogle Scholar
  225. 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 21:1541–1555PubMedGoogle Scholar
  226. Rao W, Isaac RE, Keen JN (2011) An analysis of the Caenorhabditis elegans lipid raft proteome using geLC-MS/MS. J Proteomics 74:242–253PubMedGoogle Scholar
  227. Reichel C, Beachy RN (1998) Tobacco mosaic virus infection induces severe morphological changes of the endoplasmatic reticulum. Proc Natl Acad Sci USA 95:11169–11174PubMedGoogle Scholar
  228. Reichel C, Beachy RN (2000) Degradation of the Tobacco mosaic virus movement protein by the 26S proteasome. J Virol 74:3330–3337PubMedGoogle Scholar
  229. 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 19:555–569PubMedGoogle Scholar
  230. Rhee Y, Tzfira T, Chen MH, Waigmann E, Citovsky V (2000) Cell-to-cell movement of Tobacco mosaic virus: enigmas and explanations. Mol Plant Pathol 1:33–39PubMedGoogle Scholar
  231. Ribeiro D, Goldbach R, Kormelink R (2009) Requirements for ER-arrest and sequential exit to the golgi of Tomato spotted wilt virus glycoproteins. Traffic 10:664–672PubMedGoogle Scholar
  232. Rigden JE, Krake LR, Rezaian MA, Dry IB (1994) ORF C4 of Tomato leaf curl geminivirus is a determinant of symptom severity. Virology 204:847–850PubMedGoogle Scholar
  233. 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 8:379–387Google Scholar
  234. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45PubMedGoogle Scholar
  235. Roberts IM, Wang D, Findlay K, Maule AJ (1998) Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (CIs) show that the CI protein acts transiently in aiding virus movement. Virology 245:173–181PubMedGoogle Scholar
  236. Rojas MR, Zerbini M, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237: 283–295PubMedGoogle Scholar
  237. Rojas MR, Jiang H, Salati R, Xoconostle-Cazares B, Sudarshana MR, Lucas WJ, Gilbertson RL (2001) Functional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus. Virology 291:110–125PubMedGoogle Scholar
  238. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394PubMedGoogle Scholar
  239. Ruggenthaler P, Fichtenbauer D, Krasensky J, Jonak C, Waigmann E (2009) Microtubule-associated protein AtMPB2C plays a role in organization of cortical microtubules, stomata patterning, and tobamovirus infectivity. Plant Physiol 149:1354–1365PubMedGoogle Scholar
  240. Ruiz-Medrano R, Xoconostle-Cazares B, Kragler F (2004) The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses. Curr Opin Plant Biol 7:641–650PubMedGoogle Scholar
  241. Runions J, Brach T, Kuhner S, Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57:43–50PubMedGoogle Scholar
  242. 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 17:1788–1800PubMedGoogle Scholar
  243. Sambade A, Heinlein M (2009) Approaching the cellular mechanism that supports the intercellular spread of Tobacco mosaic virus. Plant Signal Behav 4:35–38PubMedGoogle Scholar
  244. 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 9:2073–2088PubMedGoogle Scholar
  245. Samuels TD, Ju HJ, Ye CM, Motes CM, Blancaflor EB, Verchot-Lubicz J (2007) Subcellular targeting and interactions among the Potato virus X TGB proteins. Virology 367(2):375–389PubMedGoogle Scholar
  246. Sanderfoot AA, Ingham DJ, Lazarowitz SG (1996) A viral movement protein as a nuclear shuttle. The geminivirus BR1 movement protein contains domains essential for interaction with BL1 and nuclear localization. Plant Physiol 110:23–33PubMedGoogle Scholar
  247. Sanfacon H (2005) Replication of positive-strand RNA viruses in plants: contact points between plant and virus components. Can J Bot 83:1529–1549Google Scholar
  248. Santa Cruz S, Roberts AG, Prior DAM, Chapman S, Oparka KJ (1998) Cell-to-cell and phloem-mediated transport of Potato virus X: the role of virions. Plant Cell 10:495–510Google Scholar
  249. Santos AA, Lopes KV, Apfata JA, Fontes EP (2010) NSP-interacting kinase, NIK: a transducer of plant defence signalling. J Exp Bot 61(14):3839–3845PubMedGoogle Scholar
  250. Schaad MC, Anderberg RJ, Carrington JC (2000) Strain-specific interaction of the Tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two-hybrid system. Virology 273:300–306PubMedGoogle Scholar
  251. Schepetilnikov MV, Manske U, Solovyev AG, Zamyatnin AA Jr, Schiemann J, Morozov SY (2005) The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J Gen Virol 86:2379–2391PubMedGoogle Scholar
  252. 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: 6712–6715PubMedGoogle Scholar
  253. Seksek O, Biwersi J, Verkman AS (1997) Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J Cell Biol 138:131–142PubMedGoogle Scholar
  254. Selth LA, Dogra SC, Rasheed MS, Randles JW, Rezaian MA (2006) Identification and characterization of a host reversibly glycosylated peptide that interacts with the Tomato leaf curl virus V1 protein. Plant Mol Biol 61:297–310PubMedGoogle Scholar
  255. Senchou V, Weide R, Carrasco A, Bouyssou H, Pont-Lezica R, Govers F, Canut H (2004) High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif. Cell Mol Life Sci 61:502–509PubMedGoogle Scholar
  256. Shimizu T, Yoshii A, Sakurai K, Hamada K, Yamaji Y, Suzuki M, Namba S, Hibi T (2009) Identification of a novel tobacco DnaJ-like protein that interacts with the movement protein of Tobacco mosaic virus. Arch Virol 154:959–967PubMedGoogle Scholar
  257. Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16:68–72PubMedGoogle Scholar
  258. Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ (2009) An Arabidopsis GPI-anchor ­plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21:581–594PubMedGoogle Scholar
  259. Sit TL, AbouHaidir MG (1993) Infectious RNA transcripts derived from cloned cDNA of Papaya mosaic virus: effect of mutations to the capsid and polymerase proteins. J Gen Virol 74: 1133–1140PubMedGoogle Scholar
  260. Soellick TR, Uhrig JF, Bucher GL, Kellmann JW, Schreier PH (2000) The movement protein NSm of Tomato spotted wilt tospovirus: RNA binding, interaction with TSWV N protein, and identification of interacting plant proteins. Proc Natl Acad Sci USA 97:2373–2378PubMedGoogle Scholar
  261. Sokolova M, Prufer D, Tacke E, Rohde W (1997) The Potato leafroll virus 17 k movement protein is phosphorylated by a membrane-associated protein kinase from potato with biochemical features of protein kinase C. FEBS Lett 400:201–205PubMedGoogle Scholar
  262. Solovyev AG, Stroganova TA, Jr Zamyatin AA, Fedorkin ON, Schiemann J, Morozov SY (2000) Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269:113–127PubMedGoogle Scholar
  263. Sparkes I, Runions J, Hawes C, Griffing L (2009) Movement and remodeling of the endoplasmic reticulum in nondividing cells of tobacco leaves. Plant Cell 21:3937–3949PubMedGoogle Scholar
  264. Storms MMH, Kormelink R, Peters D, van Lent JWM, Goldbach RW (1995) The nonstructural NSm protein of Tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214:485–493PubMedGoogle Scholar
  265. 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 22:1373–1387PubMedGoogle Scholar
  266. Sun Y, Qian H, Xu XD, Han Y, Yen LF, Sun DY (2000) Integrin-like proteins in the pollen tube: detection, localization and function. Plant Cell Physiol 41:1136–1142PubMedGoogle Scholar
  267. 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 2:143–152Google Scholar
  268. 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 361:133–140PubMedGoogle Scholar
  269. Taoka K, Ham BK, Xoconostle-Cazares B, Rojas MR, Lucas WJ (2007) Reciprocal phosphorylation and glycosylation recognition motifs control NCAPP1 interaction with pumpkin phloem proteins and their cell-to-cell movement. Plant Cell 19:1866–1884PubMedGoogle Scholar
  270. Thomas CL, Maule AJ (1995) Identification of structural domains within the Cauliflower mosaic virus movement protein by scanning deletion mutagenesis and epitope tagging. Plant Cell 7:561–572PubMedGoogle Scholar
  271. 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:e7PubMedGoogle Scholar
  272. Tilsner J, Cowan GH, Roberts AG, Chapman SN, Ziegler A, Savenkov E, Torrance L (2010) Plasmodesmal targeting and intercellular movement of Potato mop-top pomovirus is mediated by a membrane anchored tyrosine-based motif on the lumenal side of the endoplasmic reticulum and the C-terminal transmembrane domain in the TGB3 movement protein. Virology 402:41–51PubMedGoogle Scholar
  273. 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 160:363–371PubMedGoogle Scholar
  274. 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 332:563–577PubMedGoogle Scholar
  275. Tucker EB (1990) Calcium-loaded 1,2-bis(2-aminophenoxy)ethane-N, N, N′, N′- tetraacetic acid blocks cell-to-cell diffusion of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 182:34–38Google Scholar
  276. Tucker EB (1993) Azide treatment enhances cell-to-cell diffusion in staminal hairs of Setcreasea purpurea. Protoplasma 174:45–49Google Scholar
  277. Tucker EB, Boss WF (1996) Mastoparan induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111:459–467PubMedGoogle Scholar
  278. Tyulkina LG, Karger EM, Sheveleva AA, Atabekov JG (2010) Binding of monoclonal antibodies to the movement protein (MP) of Tobacco mosaic virus: influence of subcellular MP localization and phosphorylation. J Gen Virol 91:1621–1628PubMedGoogle Scholar
  279. Tzfira T, Rhee Y, Chen M-H, Kunik T, Citovsky V (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54:187–219PubMedGoogle Scholar
  280. 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 USA 107:6894–6899PubMedGoogle Scholar
  281. Ueki S, Spektor R, Natale DM, Citovsky V (2010) ANK, a host cytoplasmic receptor for the Tobacco mosaic virus cell-to-cell movement protein, facilitates intercellular transport through plasmodesmata. PLoS Pathog 6:e1001201PubMedGoogle Scholar
  282. van Bargen S, Salchert K, Paape M, Piechulla B, Kellmann J-W (2001) Interactions between Tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin, and DNAJ-like chaperones. Plant Physiol Biochem 39:1083–1093Google Scholar
  283. van der Wel NN, Goldbach R, van Lent J (1998) The movement protein and coat protein of Alfalfa mosaic virus accumulate in structurally modified plasmodesmata. Virology 244:322–329PubMedGoogle Scholar
  284. 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 72:2615–2623PubMedGoogle Scholar
  285. Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23:855–864PubMedGoogle Scholar
  286. Verchot-Lubicz J (2005) A new cell-to-cell transport model for potexviruses. Mol Plant Microbe Interact 18:283–290PubMedGoogle Scholar
  287. Verchot-Lubicz J, Ye CM, Bamunusinghe D (2007) Molecular biology of potexviruses: recent advances. J Gen Virol 88:1643–1655PubMedGoogle Scholar
  288. 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 23:1231–1247PubMedGoogle Scholar
  289. Vogel F, Hofius D, Sonnewald U (2007) Intracellular trafficking of Potato leafroll virus movement protein in transgenic Arabidopsis. Traffic 8:1205–1214PubMedGoogle Scholar
  290. Vogler H, Kwon MO, Dang V, Sambade A, Fasler M, Ashby J, Heinlein M (2008) Tobacco mosaic virus movement protein enhances the spread of RNA silencing. PLoS Pathog 4:e1000038PubMedGoogle Scholar
  291. Waigmann E, Zambryski P (1995) Tobacco mosaic virus movement protein-mediated protein transport between trichome cells. Plant Cell 7:2069–2079PubMedGoogle Scholar
  292. Waigmann E, Zambryski P (2000) Trichome plasmodesmata: a model system for cell-to-cell movement. Adv Bot Res 31:261–283Google Scholar
  293. 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 91:1433–1437PubMedGoogle Scholar
  294. 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 19:4875–4884PubMedGoogle Scholar
  295. 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 30 k protein and its mRNA. Virology 133:18–24PubMedGoogle Scholar
  296. Watanabe Y, Meshi T, Okada Y (1992) In vivo phosphorylation of the 30-kDa protein of Tobacco mosaic virus. FEBS Lett 313:181–184PubMedGoogle Scholar
  297. Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou X, Carrington JC, Wang A (2010) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 6:e1000962PubMedGoogle Scholar
  298. 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 67:3660–3664PubMedGoogle Scholar
  299. White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180:169–184Google Scholar
  300. 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 33:271–283PubMedGoogle Scholar
  301. Wieczorek A, Sanfacon H (1993) Characterization and subcellular location of Tomato ringspot nepovirus putative movement protein. Virology 194:734–742PubMedGoogle Scholar
  302. Wille A, Lucas WJ (1984) Ultrastructural and histochemical changes on guard cells. Planta 160: 129–142Google Scholar
  303. Wittmann S, Chatel H, Fortin MG, Laliberte JF (1997) Interaction of the viral protein genome linked of Turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234:84–92PubMedGoogle Scholar
  304. Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of Tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379PubMedGoogle Scholar
  305. 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 8:21–31PubMedGoogle Scholar
  306. 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 23:1486–1497PubMedGoogle Scholar
  307. Wu X, Weigel D, Wigge PA (2002) Signaling in plants by intercellular RNA and protein movement. Genes Dev 16:151–158PubMedGoogle Scholar
  308. Wu X, Dinneny JR, Crawford KM, Rhee Y, Citovsky V, Zambryski PC, Weigel D (2003) Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130: 3735–3745PubMedGoogle Scholar
  309. Wu Q, Wang X, Ding SW (2010) Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8:12–15PubMedGoogle Scholar
  310. Wu CH, Lee SC, Wang CW (2011) Viral protein targeting to the cortical endoplasmic reticulum is required for cell-cell spreading in plants. J Cell Biol 193:521–535PubMedGoogle Scholar
  311. Yaholom A, Lando R, Katz A, Epel BL (1998) A calcium-dependent protein kinase is associated with maize mesocotyl plasmodesmata. J Plant Physiol 153:354–362Google Scholar
  312. 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 16:1979–2000PubMedGoogle Scholar
  313. Yoshioka K, Matsushita Y, Kasahara M, Konagaya K, Nyunoya H (2004) Interaction of Tomato mosaic virus movement protein with tobacco RIO kinase. Mol Cells 17:223–229PubMedGoogle Scholar
  314. Zavaliev R, Ueki S, Epel BL, Citovsky V (2011) Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma 248:117–130PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Eduardo Peña
    • 1
  • Annette Niehl
    • 1
  • Manfred Heinlein
    • 1
    • 2
    Email author
  1. 1.Institut de Biologie Moléculaire des Plantes du CNRSUniversité de StrasbourgStrasbourgFrance
  2. 2.Department of Plant Physiology, Botanical InstituteUniversity of BaselBaselSwitzerland

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