Plant Virus Movement


Plant virus movement is the process of the spread of virus genetic material from the initially infected cells to the rest of the plant. There are several distinct stages including intracellular movement from sites of virus replication to plasmodesmata (PD) (plant‐specific intercellular nanopores), cell‐to‐cell trafficking through PD and long‐distance movement between organs through the phloem (the specialized vascular system used by plants for the transport of assimilates and macromolecules). Transport is mediated by virus‐encoded ‘movement’ proteins. Several different types of movement proteins can be distinguished, which share properties such as nucleic acid binding, targeting and dilation of PD, and intercellular movement. These functions can be distributed amongst several movement proteins. Some movement proteins form a hollow tubule through PD which allows the passage of virus particles, but for the majority of viruses, the precise mechanism of transport through PD is still unknown.

Key Concepts:

  • Plant viruses need to overcome the barrier of the cell wall to spread from the initially infected cells to the rest of the plant.

  • Local cell‐to‐cell movement occurs through PD which are plant‐specific membrane‐lined nanopores that connect adjoining cells.

  • Long‐distance movement between plant organs occurs through the phloem, one of the two components of the plant's vasculature.

  • Viral cell‐to‐cell movement constitutes an extreme population bottleneck and needs to stay ahead of plant defence signals trafficking through the same channels.

  • Movement is mediated by one or several virus‐encoded movement proteins, which facilitate transport of virus genomes or virus particles between cells.

  • The transported form of the viral genome is usually either a virus particle that can be modified, or a nonvirion ribonucleoprotein complex containing RNA and movement proteins. Local and long‐distance movement forms can be different.

  • Two different movement mechanisms are observed: insertion of a MP‐comprised tubule into PD that forms a conduit for virus particles, or tubule‐less movement by an unknown mechanism.

  • Mechanisms contributing to PD dilation may include breakdown of the polysaccharide callose in the surrounding cell wall and severing of actin filaments.

  • Viruses use elements of the cell's cytoskeleton and/or endomembrane system to get from replication sites to PD, or replication and movement can be spatially linked at PD.

  • Nuclear host factors are required for long‐distance movement of some viruses.

Keywords: movement proteins; systemic infection; ribonucleoprotein particles; RNA binding; triple gene block; tubules

Figure 1.

(a) The two modes of plant virus movement: 1 – local cell‐to‐cell movement through plasmodesmata; 2 – systemic long‐distance movement through the phloem. (b,c) Electron micrographs showing longitudinal section of PD and cross‐section of the vascular system of Nicotiana benthamiana, routes of cell‐to‐cell and long‐distance virus movement, respectively. (b) Paired PD span cell wall (CW) linking the cytoplasm of two neighbouring cells. Bar, 0.4 μm (courtesy of Karl Oparka, Ian Roberts and Alison Roberts). (c) Typical section of class V vein showing bundle sheath (BS) cells, xylem parenchyma (XP) cell, xylem vessel and different types of phloem‐associated cells: phloem parenchyma (PP), companion cells (CC) and sieve elements (SE). Bar, 2 μm. M. Taliansky (unpublished).

Figure 2.

A Cowpea mosaic virusMP tubule containing virions traversing a plasmodesma and extending into the cytoplasm of the neighbouring cell. Courtesy of Jan van Lent and Joan Wellink, Wageningen University, The Netherlands.



Alzhanova DV, Prokhnevsky AI, Peremyslov VV and Dolja VV (2007) Virion tails of beet yellows virus: coordinated assembly by three structural proteins. Virology 359: 220–226.

Amari K, Boutant E, Hofmann C et al. (2010) A family of plasmodesmal proteins with receptor‐like properties for plant viral movement proteins. PLoS Pathogens 6: e1001119.

Atabekov JG, Rodionova NP, Karpova OV, Kozlovsky SV and Poljakov VY (2000) The movement protein‐triggered in situ conversion of potato virus X virion RNA from a nontranslatable into a translatable form. Virology 271: 259–263.

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

Bamunusinghe D, Hemenway CL, Nelson RS et al. (2009) Analysis of potato virus X replicase and TGBp3 subcellular locations. Virology 393: 272–285.

Canetta E, Kim SH, Kalinina NO et al. (2008) A plant virus movement protein forms ringlike complexes with the major nucleolar protein, fibrilarin, in vitro . Journal of Molecular Biology 376: 932–937.

Chung BY‐W, Miller WA, Atkins JA and Firth AE (2008) An overlapping essential gene in the potyviridae . Proceedings of the National Academy of Sciences of the USA 105: 5897–5902.

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

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

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

Gabrenaite‐Verkhovskaya R, Andreev IA, Kalinina NO et al. (2008) Cylindrical inclusion protein of potato virus A is associated with a subpopulation of particles isolated from infected plants. Journal of General Virology 89: 829–838.

Genovés A, Navarro JA and Pallás V (2010) The intra‐ and intercellular movement of melon necrotic spot virus (MNSV) depends on an active secretory pathway. Molecular Plant‐Microbe Interactions 23: 263–272.

Gutiérrez S, Michalakis Y and Blanc S (2012) Virus population bottlenecks during within‐host progression and host‐to‐host transmission. Current Opinion in Virology 2: 546–555.

Harries PA, Park J‐W, Sasaki N et al. (2009) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proceedings of the National Academy of Sciences of the USA 106: 17594–17599.

Heinlein M, Padgett HS, Gens JS et al. (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.

Karpova OV, Rodionova NP, Ivanov KI et al. (1999) Phosphorylation of tobacco mosaic virus movement protein abolishes its translation repressing ability. Virology 261: 20–24.

Karpova OV, Zayakina OV, Arkhipenko MV et al. (2006) Potato virus X RNA‐mediated assembly of single‐tailed ternary ‘coat protein‐RNA‐movement protein’ complexes. Journal of General Virology 87: 2731–2740.

Kawakami S, Watanabe Y and Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proceedings of the National Academy of Sciences of the USA 101: 6291–6296.

Kim SH, Kalinina NO, Andreev I et al. (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. Journal of General Virology 85: 221–230.

Kim SH, Macfarlane S, Kalinina NO et al. (2007b) Interaction of a plant virus‐encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proceedings of the National Academy of Sciences of the USA 104: 11115–11120.

Kim SH, Ryabov EV, Kalinina NO et al. (2007a) Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO Journal 26: 2169–2179.

Kiselyova OI, Yaminsky IV, Karger EM et al. (2001) Visualization by atomic force microscopy of tobacco mosaic virus movement protein‐RNA complexes formed in vitro . Journal of General Virology 82: 1503–1508.

Latham JR and Wilson AK (2008) Transcomplementation and synergism in plants: implications for viral transgenes? Molecular Plant Pathology 9: 85–103.

van Lent J, Wellink J and Goldbach R (1990) Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus . Journal of General Virology 71: 219–223.

Lim HS, Bragg JN, Ganesan U et al. (2008) Triple gene block protein interactions involved in movement of barley stripe mosaic virus . Journal of Virology 82: 4991–5006.

Lim HS, Bragg JN, Ganesan U et al. (2009) Subcellular localization of the barley stripe mosaic virus triple gene block proteins. Journal of Virology 83: 9432–9448.

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

Makarov V, Rybakova E, Efimov A et al. (2009) Domain organization of the N‐terminal portion of hordeivirus movement protein TGBp1. Journal of General Virology 90: 3022–3032.

Melcher U (2000) The ‘30k’ superfamily of viral movement proteins. Journal of General Virology 81: 257–266.

Meshi T, Watanabe Y, Saito T et al. (1987) Function of the 30 kd protein of tobacco mosaic virus: involvement in cell‐to‐cell movement and dispensability for replication. EMBO Journal 6: 2557–2563.

Nagano H, Mise K, Furusawa I and Okuno T (2001) Conversion in the requirement of coat protein in cell‐to‐cell movement mediated by the cucumber mosaic virus movement protein. Journal of Virology 75: 8045–8053.

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

Oparka KJ, Roberts AG, Prior DAM et al. (1995) Imaging the green fluorescent protein in plants – viruses carry the torch. Protoplasma 189: 133–141.

Peremyslov VV, Andreev IA, Prokhnevsky AI et al. (2004) Complex molecular architecture of beet yellows virus particles. Proceedings of the National Academy of Sciences of the USA 189: 133–141.

Peremyslov VV, Hagiwara Y and Dolja VV (1999) Hsp70 homolog functions in cell‐to‐cell movement of a plant virus. Proceedings of the National Academy of Sciences of the USA 96: 14771–14776.

Roberts IM, Wang D, Findlay K and 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: 173–181.

Saito T, Hosokawa D, Meshi T and Okada Y (1987) Immunocytochemical localisation of the 130k and 180k proteins (putative replicase components) of tobacco mosaic virus . Virology 160: 477–481.

Schoelz JE, Harries PA and Nelson RS (2011) Intercellular transport of plant viruses: finding the door out of the cell. Molecular Plant 4: 813–831.

Semashko MA, González I, Shaw J et al. (2012) The extreme N‐terminal domain of a hordeivirus TGB1 movement protein mediates its localization to the nucleolus and interaction with fibrillarin. Biochimie 94: 1180–1188.

Su S, Liu Z, Chen C et al. (2010) Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22: 1373–1387.

Tilsner J, Linnik O, Louveaux M et al. (2013) Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. Journal of Cell Biology 201: 981–995.

Tilsner J and Oparka KJ (2012) Missing links? – the connection between replication and movement of plant RNA viruses. Current Opinion in Virology 2: 699–705.

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

Torrance L, Andreev IA, Gabrenaite‐Verhovskaya R et al. (2006) An unusual structure at one end of potato potyvirus particles. Journal of Molecular Biology 357: 1–8.

Torrance L, Wright KM, Crutzen F et al. (2011) Unusual features of pomoviral RNA movement. Frontiers in Microbiology 2: 259.

Verchot‐Lubicz J, Torrance L, Solovyev AG et al. (2010) Varied movement strategies employed by triple gene block‐encoding viruses. Molecular Plant‐Microbe Interactions 23: 1231–1247.

Waigmann E, Chen MH, Bachmaier R, Ghoshroy S and Citovsky V (2000) Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell‐to‐cell movement protein. EMBO Journal 19: 4875–4884.

Wei T, Zhang C, Hong J et al. (2010) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N‐PIPO. PLoS Pathogens 6: e1000962.

Wright KM, Cowan GH, Lukhovitskaya NI et al. (2010) The N‐terminal domain of PMTV TGB1 movement protein is required for nucleolar localization, microtubule association, and long‐distance movement. Molecular Plant–Microbe Interactions 23: 1486–1497.

Wright KM, Wood NT, Roberts AG et al. (2007) Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8: 21–31.

Zavaliev R, Levy A, Gera A and Epel BL (2013) Subcellular dynamics and role of Arabidopsis β‐1,3‐glucanases in cell‐to‐cell movement of tobamoviruses. Molecular Plant–Microbe Interactions 26: 1016–1030.

Further Reading

Adams MJ and Antoniw JF (2006) DPVweb: a comprehensive database of plant and fungal virus genes and genomes. Nucleic Acids Research 34: Database issue, D382–D385.

Brunt AA, Crabtree K, Dallwitz MJ et al. (eds) (1996) Plant Viruses Online: Descriptions and Lists from the VIDE Database. Version: 20 August 1996.‐

Mushegian AR and Koonin EV (1993) Cell‐to‐cell‐movement of plant viruses. Insights from amino acid sequence comparisons of movement proteins and from analogies with cellular transport system. Archives of Virology 133: 239–257.

Nelson RS and van Bel AJE (1998) The mystery of virus trafficking into, through and out of the vascular tissue. Progress in Botany 59: 476–533.

Nelson RS and Citovsky V (2005) Plant viruses. Invaders of cells and pirates of cellular pathways. Plant Physiology 138: 1809–1814.

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

Oparka KJ and Turgeon R (1999) Sieve elements and companion cells – traffic control centers of the phloem. Plant Cell 11: 739–750.

Taliansky M, Brown JWS, Rajamaki ML, Valkonen JPT and Kalinina NO (2010) Involvement of the plant nucleolus in virus and viroid infections: parallels with animal pathosystems. Advances in Virus Research 77: 119–158.

Tilsner J, Amari K and Torrance L (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248: 39–60.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Tilsner, Jens, Taliansky, Michael E, and Torrance, Lesley(Jun 2014) Plant Virus Movement. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0020711.pub2]