Skip to main content

Advertisement

SpringerLink
Log in

Cell-to-cell movement of viruses via plasmodesmata

  • JPR Symposium
  • Plasmodesmata: Function and Diversity in Plant Intercellular Communication
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Plant viruses utilize plasmodesmata (PD), unique membrane-lined cytoplasmic nanobridges in plants, to spread infection cell-to-cell and long-distance. Such invasion involves a range of regulatory mechanisms to target and modify PD. Exciting discoveries in this field suggest that these mechanisms are executed by the interaction between plant cellular components and viral movement proteins (MPs) or other virus-encoded factors. Striking working analogies exist among endogenous non-cell-autonomous proteins and viral MPs, in which not only do they all use PD to traffic, but also they exploit same regulatory components to exert their functions. Thus, this review discusses on the viral strategies to move via PD and the PD-regulatory mechanisms involved in viral pathogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aaziz R, Dinant S, Epel BL (2001) Plasmodesmata and plant cytoskeleton. Trends Plant Sci 6:326–330

    CAS  PubMed  Google Scholar 

  • Adams MJ, Antoniw JF, Bar-Joseph M, Brunt AA, Candresse T, Foster GD, Martelli GP, Milne RG, Zavriev SK, Fauquet CM (2004) The new plant virus family Flexiviridae and assessment of molecular criteria for species demarcation. Arch Virol 149:1045–1060

    CAS  PubMed  Google Scholar 

  • Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didies 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:e1001119

    PubMed Central  PubMed  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:e1002327

    CAS  PubMed Central  PubMed  Google Scholar 

  • Andret-Link P, Laporte C, Valat L, Ritzenthaler C, Demangea G, Vigne E, Laval V, Pfeiffer P, Stussi-Garaud C, Fuchs M (2004) Grapevine fanleaf virus: still a major threat to the grapevine industry. J Plant Pathol 86:183–195

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Atabekov JG, Rodionova NP, Karpova OV, Kozlovsky SV, Novikov VK, Arkhipenko MV (2001) Translational activation of encapsidated Potato virus X RNA by coat protein phosphorylation. Virology 286:466–474

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Baratova LA, Fedorova NV, Dobrov EN, Lukashina EV, Kharlanov AN, Nasonov VV, Serebryakova MV, Kozlovsky SV, Zayakina OV, Rodionova NP (2004) N-terminal segment of potato virus X coat protein subunits is glycosylated and mediates formation of a bound water shell on the virion surface. Eur J Biochem 271:3136–3145

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Beachy RN, Heinlein M (2000) Role of P30 in prelication and spread of TMV. Traffic 1:540–544

    CAS  PubMed  Google Scholar 

  • Beffa RS, Hofer RM, Thomas M, Meins F (1996) Decreased susceptibility to viral disease of [beta]-1,3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8(6):1001–1011

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 80:1347–1356

    CAS  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Faulkner C, Ritzenthaler C, Maule AJ (2010) Plasmodesmata: gateways to local and systemic virus infection. Mol Plant-Microbe Interact 23:1403–1412

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Boyko V, Ferralli J, Ashby J, Schellenbaum P, Heinlein M (2000) Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2:826–832

    CAS  PubMed  Google Scholar 

  • Brandner K, Sambade A, Boutant E, Didier P, Mély 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(2):611–623

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bucher GL, Tarina C, Heinlein M, Di Serio F, Meins F, Iglesias VA (2001) Local expression of enzymatically active class I beta-1,3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28:361–369

    CAS  PubMed  Google Scholar 

  • Carvalho CM, Wellink J, Ribeiro SG, Goldbach RW, van Lent JWM (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 84:2271–2277

    CAS  PubMed  Google Scholar 

  • Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signal Behav 4:489–492

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen MH, 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 19:913–920

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng CP, Tzafrir I, Lockhart BEL, Olszewski NE (1998) Tubules containing virions are present in plant tissues infected with Commelina yellow mottle badnavirus. J general Virol 79:925–929

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Citovsky V, McLean BG, Zupan J, Zambryski PC (1993) Phosphorylation of Tobacco mosaic virus cell-to-cell movement protein by a developmentally-regulated plant cell wall-associated protein kinase. Genes Dev 7:904–910

    CAS  PubMed  Google Scholar 

  • Deom CM, Oliver MJ, Beachy RN (1987) The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237:389–394

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Ding B, Li Q, Nguyen L, Palukaitis P, Lucas WJ (1995) Cucumber mosaic virus 3a protein potentiates cell-to-cell trafficking of CMV RNA in tobacco plants. Virology 207(2):345–353

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328

    CAS  PubMed  Google Scholar 

  • Dong X, Hong Z, Chatterjee J, Kim S, Verma DP (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229:87–98

    CAS  PubMed  Google Scholar 

  • Dorokhov YL, Frolova OY, Skurat EV, Ivanov PA, Gasanova TV, Sheveleva AA, Ravin NV, Makinen KM, Klimyuk VI, Skryabin KG, Gleba YY, Atabekov JG (2006) A novel function for a ubiquitous plant enzyme pectin methylesterase: the enhancer of RNA silencing. FEBS Lett 580:3872–3878

    CAS  PubMed  Google Scholar 

  • Doxey AC, Yaish MW, Moffatt BA, Griffith M, McConkey BJ (2007) Functional divergence in the Arabidopsis beta-1,3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 24:1045–1055

    CAS  PubMed  Google Scholar 

  • Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37:1356–1360

    CAS  PubMed  Google Scholar 

  • Fedorkin ON, Merits A, Lucchesi J, Solovyev AG, Saarma M, Morozov SY, Makinen K (2000) Complementation of the movement-deficient mutations in Potato virus X: Potyvirus coat protein mediates cell-to-cell trafficking of C-terminal truncation but not deletion mutant of potexvirus coat protein. Virology 270:31–42

    CAS  PubMed  Google Scholar 

  • Fedorkin ON, Solovyev AG, Yelina NE, Zamyatnin Jr AA, Zinovkin RA, Makinen K, Schiemann J, Morozov SY (2001) Cell-to-cell movement of Potato virus X involves distinct functions of the coat protein. J Gen Virol 82:449–458

    CAS  PubMed  Google Scholar 

  • Forster 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 191:480–484

    CAS  PubMed  Google Scholar 

  • Fujiwara T, Giesman-Cookmeyer D, Ding B, Lommel SA, Lucas WJ (1993) Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red clover necrotic mosaic virus movement protein. Plant Cell 5:1783–1794

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gaire F, Schmitt C, Stussi-Garaud C, Pinck L, Ritzenthaler C (1999) Protein 2A of grapevine fanleaf nepovirus is implicated in RNA2 replication and colocalizes to the replication site. Virology 264:25–36

    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

    CAS  PubMed  Google Scholar 

  • Gillespie T, Boevink P, Haupt S, Roberts AG, Toth R, Valentine T, Chapman S, Oparka KJ (2002) Functional analysis of a DNA shuffled movement protein reveals that microtubules are dispensable for the cell-to-cell movement of Tobacco mosaic virus. Plant Cell 14:1207–1222

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harries PA, Schoelz JE, Nelson RS (2010) Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol Plant-Microbe Interact 23:1381–1393

    CAS  PubMed  Google Scholar 

  • Haupt S, Cowan GH, Ziegler A, Roberts AG, Oparka KJ, Torrance L (2005) Two plant-viral movement proteins traffic in endocytic recycling pathway. Plant Cell 17:164–181

    CAS  PubMed Central  PubMed  Google Scholar 

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

    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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hsu HT, Hsu YH, Bi IP, Lin NS, Chang BY (2004) Biological functions of the cytoplasmic TGBp1 inclusions of bamboo mosaic potexvirus. Arch Virol 149:1027–1035

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Huisman MJ, Linthorst HJ, Bol JF, Cornelissen JC (1988) The complete nucleotide sequence of potato virus X and its homologies at the amino acid level with various plus-stranded RNA viruses. J Gen Virol 69:1789–1798

    CAS  PubMed  Google Scholar 

  • Hyun TK, Uddin MN, Rim Y, Kim JY (2011) Cell-to-cell trafficking of RNA and RNA silencing through plasmodesmata. Protoplasma 248:101–116

    CAS  PubMed  Google Scholar 

  • Iglesias VA, Meins FJr (2000) Movement of plant viruses is delayed in a beta-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21:157–166

    CAS  PubMed  Google Scholar 

  • 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 205:12–22

    CAS  PubMed  Google Scholar 

  • Jackson AO, Kim HS, Bragg J, Ganesan U, Lee MY (2009) Hordeivirus replication, movement, and pathogenesis. Annu Rev Phytopathol 47:385–422

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kawakami S, Hori K, Hosokawa D, Okada Y, Watanabe Y (2003) Defective tobamovirus movement protein lacking wild-type phosphorylation sites can be complemented by substitutions found in revertants. J Virol 77:1452–1461

    CAS  PubMed Central  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 USA 101:6291–6296

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim JY, Rim Y, Wang J, Jackson D (2005) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev 19:788–793

    CAS  PubMed Central  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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 132:5387–5398

    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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee JY, Lu H (2011) Plasmodesmata: the battleground against intruders. Trends Plant Sci 16:201–210

    CAS  PubMed  Google Scholar 

  • Lee JY, Yoo B, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–396

    CAS  PubMed  Google Scholar 

  • Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17:2817–2831

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee JY, Wang X, Cui W, Sager R, Modla S, Czymmek K, Zybaliov B, van Wijk K, Zhang C, Lu H, Laskshmanan V (2011) A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:3353–3373

    CAS  PubMed Central  PubMed  Google Scholar 

  • Levy A, Guenoune-Gelbart D, Epel BL (2007a) Beta-1,3-glucanases: plasmodesmal gate keepers for intercellular communication. Plant Signal Behav 2:404–407

    PubMed Central  PubMed  Google Scholar 

  • Levy A, Erlanger M, Rosenthal M, Epel BL (2007b) A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. Plant J 49:669–682

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lico C, Capuano F, Renzone G, Donini M, Marusic C, Scaloni A, Benvenuto E, Baschieri S (2006) Peptide display on Potato virus X: molecular features of the coat protein-fused peptide affecting cell-to-cell and phloem movement of chimeric virus particles. J Gen Virol 87:3103–3112

    CAS  PubMed  Google Scholar 

  • Lionetti V, Raiola A, Cervone F, Bellincampi D (2014) Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis. Mol Plant Pathol 15:265–274. doi:10.1111/mpp.12090

    CAS  PubMed  Google Scholar 

  • Lough TJ, Shash K, Xoconostle-Cázares B, Hofstra KR, Beck DL, Balmori E, Forster RLS, 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 11:801–814

    CAS  Google Scholar 

  • Lough TJ, Netzler NE, Emerson SJ, Sutherland P, Carr F, Beck DL, Lucas WJ, Forster RLS (2000) Cell-to-cell movement of potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Mol Plant-Microbe Interact 13:962–974

    CAS  PubMed  Google Scholar 

  • Lough TJ, Lee RH, Emerson SJ, Forster RL, Lucas WJ (2006) Functional analysis of the 5′ untranslated region of potexvirus RNA reveals a role in viral replication and cell-to-cell movement. Virology 351:455–465

    CAS  PubMed  Google Scholar 

  • Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184

    CAS  PubMed  Google Scholar 

  • Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasodesmata. Science 270:1980–1983

    CAS  PubMed  Google Scholar 

  • Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata-bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mekuria TA, Gutha LR, Martin RR, Naidu RA (2009) Genome diversity and intra- and interspecies recombination events in Grapevine fanleaf virus. Phytopathology 12:1394–1402

    Google Scholar 

  • 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 6:2557–2563

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Morvan O, Quentin M, Jauneau A, Mareck A, Morvan C (1998) Immunogold localization of pectin methylesterases in the cortical tissues of flax hypocotyl. Protoplasma 202:175–184

    CAS  Google Scholar 

  • 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 75:8045–8053

    CAS  PubMed Central  PubMed  Google Scholar 

  • Niehl A, Heinlein M (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75–99

    CAS  PubMed  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid dependent disease resistance. Science 301:969–972

    CAS  PubMed  Google Scholar 

  • Oparka KJ, Prior DAM, Santa Cruz S, Padgett HS, Beachy RN (1997) Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus. Plant J 12:781–789

    CAS  PubMed  Google Scholar 

  • Otulak K, Garbaczewska G (2011) Cell-to-cell movement of three genera (+) ssRNA plant viruses. Acta Physiol. Plant 33:249–260

    CAS  Google Scholar 

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

    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

    CAS  PubMed  Google Scholar 

  • Perbal MC, Thomas CL, Maule AJ (1993) Cauliflower mosaic virus gene I product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195:281–285

    CAS  PubMed  Google Scholar 

  • Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z (1996) Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–3441

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ritzenthaler C, Pinck M, Pinck L (1995a) Grapevine fanleaf nepovirus P38 putative movement protein is not transiently expressed and is a stable final maturation product in vivo. J Gen Virol 76:907–915

    CAS  PubMed  Google Scholar 

  • Ritzenthaler C, Schmit AC, Michler P, Stussi-Garaud C, Pinck L (1995b) Grapevine fanleaf nepovirus P38 putative movement protein is located on tubules in vivo. Mol Plant-Microb Interact 8:379–387

    CAS  Google Scholar 

  • Roberts IM, Boevink P, Roberts AG, Sauer N, Reichel C, Oparka KJ (2001) Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218:31–44

    CAS  PubMed  Google Scholar 

  • Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component proteinase function as potyvirus cellto-cell movement proteins. Virology 237:283–295

    CAS  PubMed  Google Scholar 

  • Sagi G, Katz A, Guenoune-Gelbart D, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. Plant Cell 17:1788–1800

    CAS  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • 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 367:375–389

    CAS  PubMed  Google Scholar 

  • Santa Cruz S, Roberts AG, Prior DA, Chapman S, Oparka KJ (1998) Cell-to-cell and phloem-mediated transport of potato virus X. The role of virions. Plant Cell 10:495–510

    Google Scholar 

  • Schmitz I, Rao ALN (1996) Molecular studies on bromovirus capsid protein: I. Characterization of cell-to-cell movement-defective RNA3 variants of brome mosaic virus. Virology 226:281–293

    CAS  PubMed  Google Scholar 

  • Scholthof HB (2005) Plant virus transport: motions of functional equivalence. Trends Plant Sci 10:376–382

    CAS  PubMed  Google Scholar 

  • Schwach F, Vaistij FE, Jones L, Baulcombe DC (2005) An RNA dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 154:959–967

    CAS  PubMed  Google Scholar 

  • Shukla DD, Ward CW (1989) Identification and classification of potyviruses on the basis of coat protein sequence data and serology. Arch Virol 06:171–200

    Google Scholar 

  • 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 21:581–594

  • 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 214:485–493

    CAS  PubMed  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 22:1373–1387

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamai A, Meshi T (2001) Cell-to-cell movement of Potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Mol Plant-Microbe Interact 14:1158–1167

    CAS  PubMed  Google Scholar 

  • Tozzini AC, Ek B, Palva ET, Hopp HE (1994) Potato virus X coat protein: a glycoprotein. Virology 202:651–658

    CAS  PubMed  Google Scholar 

  • Tzfira T, Rhee Y, Chen MH, Kunik T, Citovsky V (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54:187–219

    CAS  PubMed  Google Scholar 

  • Ueki S, Citovsky V (2002) Cadmium ion-induced glycine-rich protein inhibits systemic movement of a tobamovirus. Nat Cell Biol 4:478–485

    CAS  PubMed  Google Scholar 

  • van Lent J, Storms M, van der Meer F, Wellink J, Goldbach R (1991) Tubular structures involved in movement of cowpea mosaic virus are also formed in infected cowpea protoplasts. J Gen Virol 72:2615–2623

    PubMed  Google Scholar 

  • Verchot-Lubicz J (2005) A new cell-to-cell transport model for potexviruses. Mol Plant-Microbe Interact 18:283–290

    CAS  PubMed  Google Scholar 

  • Verchot-Lubicz J, Ye CM, Bamunusinghe D (2007) Molecular biology of potexviruses: recent advances. J Gen Virol 88:1643–1655

    CAS  PubMed  Google Scholar 

  • Waigmann E, Lucas W, Citovsky V, Zambryski P (1994) Direct functional assay for Tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc Natl Acad Sci USA 91:1433–1437

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waigmann E, Ueki S, Trutnyeva K, Vitaly C (2004) The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Crit Rev Plant Sci 23:195–250

    CAS  Google Scholar 

  • Wawrzynska A, Rodibaugh NL, Innes RW (2010) Synergistic activation of defense responses in Arabidopsis by simultaneous loss of the GSL5 callose synthase and the EDR1 protein kinase. Mol Plant-Microbe Interact 23:578–584

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wellink J, van Lent JW, Verver J, Sijen T, Goldbach RW, van Kammen A (1993) The Cowpea mosaic virus M RNA-encoded 48-kilodalton protein is responsible for induction of tubular structures in protoplasts. J Virol 67:3660–3664

    CAS  PubMed Central  PubMed  Google Scholar 

  • Winter N, Kollwig G, Zhang S, Kragler F (2007) MPB2C, a microtubule-associated protein, regulates non-cell-autonomy of the homeodomain protein KNOTTED1. Plant Cell 19:3001–3018

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Wu X, Weigel D, Wigge PA (2002) Signaling in plants by intercellular RNA and protein movement. Genes Dev 16:151–158

    CAS  PubMed  Google Scholar 

  • Xie Q, Guo HS (2006) Systemic antiviral silencing in plants. Virus Res 118:1–6

    CAS  PubMed  Google Scholar 

  • Zavaliev R, Ueki S, Epel BL, Citovsky V (2011) Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma 248:117–130

    CAS  PubMed  Google Scholar 

  • Zavaliev R, Levy A, Gera A, Epel B (2013) Subcellular dynamics and role of Arabidopsis β-1,3-glucanases in cell-to-cell movement of tobamoviruses. Mol Plant-Microbe Interact 26:1016–1030

    CAS  PubMed  Google Scholar 

  • Zayakina O, Arkhipenko M, Kozlovsky S, Nikitin N, Smirnov A, Susi P, Rodionova N, Karpova O, Atabekov J (2008) Mutagenic analysis of Potato Virus X movement protein (TGBp1) and the coat protein (CP): in vitro TGBp1-CP binding and viral RNA translation activation. Mol Plant Pathol 9:37–44

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The support for this work was provided by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2013R1A1A2007230) and by a grant from the Next-Generation BioGreen 21 Program (SSAC, Grant PJ009495), Rural Development Administration, Republic of Korea. D. K and R. K were supported by a scholarship from the BK21Plus Program, the Ministry of Education Korea.

Author information

Authors and Affiliations

  1. Division of Applied Life Science (BK21plus), Department of Biochemistry, Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, 27-306, 501 Jinju-Daero, Jinju, 660-701, Korea

    Dhinesh Kumar, Ritesh Kumar, Tae Kyung Hyun & Jae-Yean Kim

Authors
  1. Dhinesh Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ritesh Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tae Kyung Hyun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jae-Yean Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jae-Yean Kim.

Additional information

D. Kumar, R. Kumar, T. K. Hyun equally contributed to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, D., Kumar, R., Hyun, T.K. et al. Cell-to-cell movement of viruses via plasmodesmata. J Plant Res 128, 37–47 (2015). https://doi.org/10.1007/s10265-014-0683-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-014-0683-6

Keywords

Search

Navigation