Summary
Cell-to-cell movement is a crucial step in plant virus infection. In many viruses, the movement function is secured by specific virus-encoded proteins. Amino acid sequence comparisons of these proteins revealed a vast superfamily containing a conserved sequence motif that may comprise a hydrophobic interaction domain. This superfamily combines proteins of viruses belonging to all principal groups of positive-strand RNA viruses, as well as single-stranded DNA containing geminiviruses, double-stranded DNA-containing pararetroviruses (caulimoviruses and badnaviruses), and tospoviruses that have negative-strand RNA genomes with two ambisense segments. In several groups of positive-strand RNA viruses, the movement function is provided by the proteins encoded by the so-called triple gene block including two putative small membrane-associated proteins and a putative RNA helicase. A distinct type of movement proteins with very high content of proline is found in tymoviruses. It is concluded that classification of movement proteins based on comparison of their amino acid sequences does not correlate with the type of genome nucleic acid or with grouping of viruses based on phylogenetic analysis of replicative proteins or with the virus host range. Recombination between unrelated or distantly related viruses could have played a major role in the evolution of the movement function. Limited sequence similarities were observed between i) movement proteins of dianthoviruses and the MIP family of cellular integral membrane proteins, and ii) between movement proteins of bromoviruses and cucumoviruses and M1 protein of influenza viruses which is involved in nuclear export of viral ribonucleoproteins. It is hypothesized that all movement proteins of plant viruses may mediate hydrophobic interactions between viral and cellular macromolecules.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Agutter PS (ed) (1991) Between nucleus and cytoplasm. Chapman and Hall, New York
Albrecht H, Geldreich A, Menissier de Murcia J, Kirchnerr D, Mesnard J-M, Lebeurier G (1988) Cauliflower mosaic virus gene I product detected in cell wall-enriched fraction. Virology 163: 503–508
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J. Mol Biol 215: 403–410
Atabekov JG, Taliansky ME (1990) Expression of a plant virus-coded transport function by different viral genomes. Adv Virus Res 38: 201–248
Baron-Epel O, Hernandez D, Jiang L-W, Meiners S, Schindler M (1988) Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Cell Biol 106: 715–721
Beck DL, Guilford PJ, Voot DM, Andersen MT, Forster RL (1991) Triple gene block proteins of white clover mosaic potexviurs are required for transport. Virology 183: 695–702
Berna A, Gafny R, Wolf S, Lucas WJ, Holt CA, Beachy RN (1991) The TMV movement protein: role of the C-terminal 73 amino acids in subcellular localization and function. Virology 182: 682–689
Boccard F, Baulcombe D (1993) Mutational analysis of cis-acting sequences and gene function in RNA 3 of cucumber mosaic virus. Virology 193: 563–578
Bouhida M, Lockhart BEL, Olszewski N (1993) An analysis of the complete nucleotide sequence of a sugarcane bacilliform virus genome infectious to banana and rice. J Gen Virol 74: 15–22
Boulton MI, Pallaghy CK, Chatani M, MacFarlane S, Davies JW (1993) Replication of maize streak virus mutants in maize protoplasts: evidence for a movement protein. Virology 192: 85–93
Bozart CS, Weiland JJ, Dreher TW (1992) Expression of ORF-69 of turnip yellow mosaic virus is necessary for virus spread in plants. Virology 187: 124–130
Calder VL, Palukaitis P (1992) Nucleotide sequence analysis of the movement genes of resistance breaking strains of tomato mosaic virus. J Gen Virol 73: 165–168
Carter KC, Bowman D, Carrington W, Fogarty K, McNeil JA, Fay FS, Lawrence JB (1993) A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science 259: 1330–1335
Chapman S, Kavanagh T, Baulcombe D (1992) Potato virus X as a vector for gene expression in plants. Plant J 2: 549–557
Citovsky V, Knorr D, Schuster G, Zambryski P (1990) The P 30 movement protein of tobacco mosaic virus is a single-stranded nucleic acid binding protein. Cell 60: 637–647
Citovsky V, Knorr D, Zambryski P (1991) Gene I, a potential cell-to-cell movement locus of cauliflower mosaic virus, encodes an RNA-binding protein. Proc Natl Acad Sci USA 88: 2476–2480
Citovsky V, Zambryski P (1991) How do plant virus nucleic acids move through intercellular connections? BioEssays 13: 373–379
Citovsky V, Wong ML, Shaw AL, Venkataram Prasad BV, Zambryski P (1992) Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4: 397–411
Dawson WO (1990) Relationship of tobacco mosaic virus gene expression to movement within plant. In: Pirone TP, Shaw JG (eds) Viral genes and plant pathogenesis. Springer, Wien New York, pp 39–52
Deom CM, Lapidot M, Beachy RN (1992) Plant virus movement proteins. Cell 69: 221–224
Derrick PM, Barker H, Oparka KJ (1992) Increase in plasmodesmatal permeability during cell-to-cell spread of tobacco rattle virus from individually inoculated cells. Plant Cell 4: 1405–1412
Doolittle RF (1986) Of URFs and ORFs. A primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley
Dorokhov Yul, Alexandrova NM, Miroshnichenko NA, Atabekov JG (1984) The informosome-like virus-specific ribonucleoprotein (vRNP) may be involved in the transport of tobacco mosaic virus infection. Virology 137: 127–134
Enami K, Qiao Y, Fukuda R, Enami M (1993) An influenza virus temperature-sensitive mutant defective in the nuclear-cytoplasmic transport of the negative-sense viral RNAs. Virology 194: 822–827
Erny C, Schoumacher F, Jung C, Gagey M-J, Godefroy-Colburn T, Stussi-Garaud C, Berna A (1992) An N-proximal sequence of alfalfa mosaic virus movement protein is necessary for association with cell walls in transgenic plants. J Gen Virol 73: 2115–2119
Francki RIB, Fauquet CM, Knudson DL, Brown F (eds) (1991) Classification and nomenclature of viruses. Fifth Report of the International Committee on Taxonomy of Viruses. Springer, Wien New York (Arch Virol [Suppl] 2)
Gilmer D, Bouzoubaa S, Guilley H, Richards K, Jonard G (1992) Efficient cell-to-cell movement of beet necrotic yellow vein virus requires 3′ proximal genes located on RNA 2. Virology 189: 40–47
Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1988) A novel superfamily of nucleoside triphosphate-binding motif-containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett 239: 16–24
Gorbalenya AE, Blinov VM, Donchenko AP, Koonin EV (1989) An ATP-binding motif is the most conserved sequence in a highly diverged group of proteins involved in positive strand RNA viral replication. J Mol Evol 28: 256–268
Hacker DL, Petty ITD, Wei N, Morris TJ (1992) Turnip crinkle virus genes required for RNA replication and virus movement. Virology 186: 1–8
Hamilton WDO, Boccara M, Robinson DJ, Baulcombe DC (1987) The complete nucleotide sequence of tobacco rattle virus RNA-1. J Gen Virol 70: 963–968
Hull R, Saedler J, Longstaff M (1986) The sequence of carnation etched ring virus DNA: comparison with cauliflower mosaic virus and retroviruses. EMBO J 5: 3083–3090
Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72: 2179–2207
Koonin EV (1992) Virus evolution: time for Sturm und Drang. Semin Virol 3: 311–313
Koonin EV, Mushegian AR, Ryabov EV, Dolja VV (1991) Diverse groups of plant DNA and RNA viruses share related movement proteins that may possess chaperone-like activity. J Gen Virol 72: 2895–2903
Koonin EV, Dolja VV (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol (in press)
Lamb RA (1989) Genes and proteins of the influenza viruses. In: King RM (ed) The influenza viruses. Plenum Press, New York, pp 1–87
Linstead PJ, Hills GJ, Plaskitt KA, Wilson IG, Harker CL, Maule AJ (1988) The subcellular localization of gene I product of cauliflower mosaic virus is consistent with a function associated with virus spread. J Gen Virol 69: 1809–1818
MacKenzie DJ, Tremaine JH (1988) Ultrastructural location of non-structural protein 3A of cucumber mosaic virus in infected tissue using monoclonal antibodies to a cloned chimeric fusion protein. J Gen Virol 60: 2387–2394
Maquat LE (1991) Nuclear mRNA export. Curr Opin Cell Biol 3: 1004–1012
Martin K, Helenius A (1991) Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67: 117–130
Maule AJ (1991) Virus movement in infected plants. Crit Rev Plant Sci 9: 457–473
Mehlin H, Daneholt B, Skoglund U (1992) Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell 69: 605–613
Meiners S, Xu A, Schindler M (1991) Gap junction protein homologue inArabidopsis thaliana: evidence for connexins in plants. Proc Natl Acad Sci USA 88: 4119–4122
Melcher U (1990) Similarities between putative transport proteins of plant viruses. J Gen Virol 71: 1009–1018
Morozov SYu, Dolja VV, Atabekov JG (1989) Probable reassortment of genomic elements among elongated RNA-containing plant viruses. J Mol Evol 29: 52–62
Nigg EA, Bauerle PA, Luhrmann R (1991) Nuclear import-export: in search of signals and mechanisms. Cell 66: 15–22
Osman TAM, Buck KW (1991) Detection of the movement protein of red clover necrotic mosaic virus in a cell wall fraction from infectedNicotiana clevelandii plants. J Gen Virol 72: 2853–2856
Osman TAM, Hayes RJ, Buck KW (1992) Cooperative binding of the red clover necrotic mosaic movement protein to single stranded nucleic acids. J Gen Virol 73: 223–227
Pao GM, Wu L-F, Johnson KD, Hofte H, Chrispeels MJ, Sweet G, Sandal NN, Saler Jr MH (1991) Evolution of the MIP family of integral membrane transport proteins. Mol Microbiol 5: 33–37
Perbal MC, Thomas CL, Maule AJ (1993) Cauliflower mosaic virus gene I product (P 1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195: 281–285
Petty ITD, French R, Jones RW, Jackson AO (1990) Identification of barley stripe mosaic virus genes involved in viral RNA replication and systemic spread. EMBO J 9: 3452–3457
Rao MJK, Argos P (1985) A conformation preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta 869: 197–214
Robards AW, Lucas WJ, Pitts JD, Jongsma JD, Spray DC (eds) (1990) Parallels in cell-to-cell junctions in plants and animals. Springer, Berlin Heidelberg New York Tokyo
Sacher R, Ahlquist P (1989) Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. J Virol 63: 4545–4552
Schroder HC, Ugarkovic D, Langen P, Bachmann M, Dorn A, Kuchino Y, Muller WEG (1990) Evidence for involvement of a nuclear envelope-associated RNA helicase activity in nucleocytoplasmic RNA transport. J Cell Physiol 145: 136–146
Schuler GD, Altschul SF, Lipman DJ (1991) A workbench for multiple alignments construction and analysis. Proteins Struct Funct Genet 9: 180–190
Thomas GL, Perbal C, Maule AJ (1993) A mutation in cauliflower mosaic virus gene I interferes with virus movement but not virus replication. Virology 192: 415–421
Traynor P, Young BM, Ahlquist P (1991) Deletion analysis of brome mosaic virus 2 a protein: effects on RNA replication and virus spread. J Virol 65: 2807–2815
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
Wolf S, Deom CM, Beachy RN, Lucas WJ (1991) Plasmodesmatal function is probed using transgenic tobacco plants that express a virus movement protein. Plant Cell 3: 593–604
Wellink J, van Kammen A (1989) Cell-to-cell transport of cowpea mosaic virus requires both the 58/48 K proteins and the capsid proteins. J Gen Virol 51: 317–325
Xiong Z, Kim KH, Giesman-Cookmeyer D, Lommel S (1993) The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology 192: 27–32
Ziegler-Graff V, Guilford PJ, Baulcombe DC (1991) Tobacco rattle virus RNA-1 29 K gene product potentiates viral movement and also affects symptom production in tobacco. Virology 182: 144–155
Zimmern D (1988) Evolution of RNA viruses. In: Holland JJ, Domingo E, Ahlquist P (eds) RNA genetics. CRC Press, Boca Raton
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mushegian, A.R., Koonin, E.V. Cell-to-cell movement of plant viruses. Archives of Virology 133, 239–257 (1993). https://doi.org/10.1007/BF01313766
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01313766