Cell wall localization of Red clover necrotic mosaic virus movement protein is required for cell-to-cell movement

Virology

Volumn 333, Issue 1, 2005, Pages 10-21

  Tremblay, Douglas ^a,b   Vaewhongs, Andrew A ^a,c   Turner, Katherine A ^a,d   Sit, Tim L ^a   Lommel, Steven A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b BASF CORPORATION   (United States)

^c Large Scale Biology Corporation   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Confocal microscopy; GFP; Intracellular localization; Plasmodesmata; RCNMV movement protein; Viral movement

Indexed keywords

GREEN FLUORESCENT PROTEIN; MOVEMENT PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BIOACCUMULATION; CELL WALL; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; GENETIC COMPLEMENTATION; MOSAIC VIRUS; NONHUMAN; PLANT VIRUS; PLASMODESMA; PRIORITY JOURNAL; PROTEIN DOMAIN; RED CLOVER; RNA ANALYSIS; VIRUS ACTIVATION; VIRUS CHARACTERIZATION; VIRUS TRANSCRIPTION;

RED CLOVER NECROTIC MOSAIC VIRUS; TRIFOLIUM PRATENSE;

EID: 13644249879     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.12.019     Document Type: Article

References (56)

1. D. Atkins, R. Hull, B. Wells, K. Roberts, P. Moore, and R.N. Beachy The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata J. Gen. Virol. 72 1991 209 211
2. L.M. Blackman, P. Boevink, S. Santa Cruz, P. Palukaitis, and K.J. Oparka The movement protein of cucumber mosaic virus traffics into sieve elements in minor veins of Nicotiana clevelandii Plant Cell 10 1998 525 538
3. L.M. Brill, R.S. Nunn, T.W. Kahn, M. Yeager, and R.N. Beachy Recombinant tobacco mosaic virus movement protein is an RNA-binding, alpha-helical membrane protein Proc. Natl. Acad. Sci. U.S.A. 97 2000 7112 7117
4. A. Callaway, D. Giesman-Cookmeyer, E.T. Gillock, T.L. Sit, and S.A. Lommel The multifunctional capsid proteins of plant RNA viruses Annu. Rev. Phytopathol. 39 2001 419 460
5. J.C. Carrington, K.D. Kasschau, S.K. Mahajan, and M.C. Schaad Cell-to-cell and long-distance transport of viruses in plants Plant Cell 8 1996 1669 1681
6. V. Citovsky, B.G. McLean, J.R. Zupan, and P. Zambryski Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase Genes Dev. 7 1993 904 910
7. R. Dasgupta, B.H. Garcia, and R.M. Goodman Systemic spread of an RNA insect virus in plants expressing plant viral movement protein genes Proc. Natl. Acad. Sci. U.S.A. 98 2001 4910 4915
8. B. Ding, J.S. Haudenshield, R.J. Hull, S. Wolf, R.N. Beachy, and W.J. Lucas Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic plants Plant Cell 4 1992 915 928
9. B.L. Epel, H.S. Padgett, M. Heinlein, and R.N. Beachy Plant virus movement protein dynamics probed with a GFP-protein fusion Gene 173 1996 75 79
10. Y. Fujita, K. Mise, and I. Furusawa Genotypic and phenotypic analysis of bromovirus adaptive mutants derived from a single plant Microbiol. Immunol. 43 1999 181 185
11. T. Fujiwara, D. Giesman-Cookmeyer, B. Ding, S.A. Lommel, and W.J. Lucas Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red clover necrotic mosaic virus movement protein Plant Cell 5 1993 1783 1794
12. Z. Ge, C. Hiruki, and K.L. Roy A comparative study of the RNA-2 nucleotide sequences of two sweet clover necrotic mosaic virus strains J. Gen. Virol. 73 1992 2483 2486
13. D. Giesman-Cookmeyer, and S.A. Lommel Alanine scanning mutagenesis of a plant virus movement protein identifies three functional domains Plant Cell 5 1993 973 982
14. D. Giesman-Cookmeyer, S. Silver, A.A. Vaewhongs, S.A. Lommel, and C.M. Deom Tobamovirus and dianthovirus movement proteins are functionally homologous Virology 213 1995 38 45
15. K. Gopinath, P. Bertens, J. Pouwels, H. Marks, J. Van Lent, J. Wellink, and A. Van Kammen Intracellular distribution of cowpea mosaic virus movement protein as visualized by green fluorescent protein fusions Arch. Virol. 148 2003 2099 2114
16. R. Guenther, T.L. Sit, H. Gracz, G. Liu, W.H. Newman, M. Dolan, P. Agris, and S.A. Lommel Structural characterization of an intermolecular RNA/RNA interaction involved in the transcription regulation element of a bipartite plant virus Nucleic Acids Res. 32 2004 2819 2828
17. M. Huang, L. Jongejan, H. Zheng, L. Zhang, and J.F. Bol Intracellular localization and movement phenotypes of alfalfa mosaic virus movement protein mutants Mol. Plant-Microb. Interact. 14 2001 1063 1074
18. D.T. Kasteel, N.N. van der Wel, K.A. Jansen, R.W. Goldbach, and J.W. van Lent Tubule-forming capacity of the movement proteins of alfalfa mosaic virus and brome mosaic virus J. Gen. Virol. 78 1997 2089 2093
19. T.K. Kendall, and S.A. Lommel Nucleotide sequence of carnation ringspot dianthovirus RNA-2 J. Gen. Virol. 73 1992 2479 2482
20. K.H. Kim, and S.A. Lommel Identification and analysis of the site of -1 ribosomal frameshifting in Red clover necrotic mosaic virus Virology 200 1994 574 582
21. K.-H. Kim, and S.A. Lommel Sequence element required for efficient -1 ribosomal frameshifting in Red clover necrotic mosaic dianthovirus Virology 250 1998 50 59
22. G. Kotlizky, A. Katz, J. van der Laak, V. Boyko, M. Lapidot, R.N. Beachy, M. Heinlein, and B.L. Epel A dysfunctional movement protein of Tobacco mosaic virus interferes with targeting of wild-type movement protein to microtubules Mol. Plant-Microb. Interact. 14 2001 895 904
23. S.G. Lazarowitz Probing plant cell structure and function with viral movement proteins Curr. Opin. Plant Biol. 2 1999 332 338
24. S.A. Lommel, M. Weston-Fina, Z. Xiong, and G.P. Lomonossoff The nucleotide sequence and gene organization of red clover necrotic mosaic virus RNA-2 Nucleic Acids Res. 16 1988 8587 8602
25. W.J. Lucas Plasmodesmata: intercellular channels for macromolecular transport in plants Curr. Opin. Cell Biol. 7 1995 673 680
26. W.J. Lucas, S. Bouche-Pillon, D.P. Jackson, L. Nguyen, L. Baker, B. Ding, and S. Hake Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata Science 270 1995 1980 1983
27. B.G. McLean, E. Waigmann, V. Citovsky, and P. Zambryski Cell-to-cell movement of plant viruses Trends Microbiol. 1 1993 105 109
28. S.Y.u. Morozov, O.N. Fedorkin, G. Juttner, J. Schiemann, D.C. Baulcombe, and J.G. Atabekov Complementation of a potato virus X mutant mediated by bombardment of plant tissues with cloned viral movement protein genes J. Gen. Virol. 78 1997 2077 2083
29. T. Okuno, C. Hiruki, D.V. Rao, and G.C. Figueiredo Genetic determinants distributed in two genomic RNAs of sweet clover necrotic mosaic, red clover necrotic mosaic and clover primary leaf necrosis viruses J. Gen. Virol. 64 1983 1907 1914
30. T.A. Osman, and K.W. Buck Detection of the movement protein of Red clover necrotic mosaic virus in a cell wall fraction from infected Nicotiana clevelandii plants J. Gen. Virol. 72 1991 2853 2856
31. T.A. Osman, R.J. Hayes, and K.W. Buck Cooperative binding of the Red clover necrotic mosaic virus movement protein to single stranded nucleic acids J. Gen. Virol. 73 1992 223 227
32. T.A. Osman, P.J. Ingles, S.J. Miller, and K.W. Buck A spontaneous Red clover necrotic mosaic virus mutant with a truncated movement protein J. Gen. Virol. 72 1991 1793 1800
33. H.S. Padgett, B.L. Epel, T.W. Kahn, M. Heinlein, Y. Watanabe, and R.N. Beachy Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection Plant J. 10 1996 1079 1088
34. J. Pouwels, N. Kornet, N. van Bers, T. Guighelaar, J. van Lent, T. Bisseling, and J. Wellink Identification of distinct steps during tubule formation by the movement protein of Cowpea mosaic virus J. Gen. Virol. 84 2003 3485 3494
35. A.L.N. Rao, B. Cooper, and C.M. Deom Defective movement of viruses in the family Bromoviridae is differentially complemented in Nicotiana benthamiana expressing tobamovirus or dianthovirus movement proteins Phytopathology 88 1998 666 672
36. R. Reade, K. Delroux, K. Macdonald, T.L. Sit, S.A. Lommel, and D. Rochon Spontaneous deletion enhances movement of a cucumber necrosis virus based chimera expressing the red clover necrotic mosaic virus movement protein gene Mol. Plant Pathol. 2 2001 13 25
37. R. Reade, J. Miller, M. Robbins, Y. Xiang, and D. Rochon Molecular analysis of the Cucumber leaf spot virus genome Virus Res. 91 2003 171 179
38. A.G. Roberts, and K.J. Oparka Plasmodesmata and the control of symplastic transport Plant Cell Environ. 26 2003 103 124
39. I.M. Roberts, D. Wang, K. Findlay, and A.J. Maule Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (Cls) show that the Cl protein acts transiently in aiding virus movement Virology 245 1998 173 181
40. T.L. Sit, A.A. Vaewhongs, and S.A. Lommel RNA-mediated trans-activation of transcription from a viral RNA Science 281 1998 829 832
41. A.G. Solovyev, D.A. Zelenina, E.I. Savenkov, V.Z. Grdzelishvili, S.Yu. Morozov, E. Maiss, R. Casper, and J.G. Atabekov Host-controlled cell-to-cell movement of a hybrid barley stripe mosaic virus expressing a dianthovirus movement protein Intervirology 40 1997 1 6
42. A. Tamai, K. Kubota, H. Nagano, M. Yoshii, M. Ishikawa, K. Mise, and T. Meshi Cucumovirus- and bromovirus-encoded movement functions potentiate cell-to-cell movement of tobamo- and potexviruses Virology 315 2003 56 67
43. M. Tatsuta, H. Mizumoto, M. Kaido, K. Mise, and T. Okuno The Red clover necrotic mosaic virus RNA-2 trans-activator is also a cis-acting RNA-2 replication element J. Virol. 79 2005 978 986
44. K.A. Turner, T.L. Sit, A.S. Callaway, N.S. Allen, and S.A. Lommel Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum Virology 320 2004 276 290
45. A.A. Vaewhongs, and S.A. Lommel Virion formation is required for the long-distance movement of red clover necrotic mosaic virus in movement protein transgenic plants Virology 212 1995 607 613
46. N.N. van der Wel, R.W. Goldbach, and J.W. van Lent The movement protein and coat protein of alfalfa mosaic virus accumulate in structurally modified plasmodesmata Virology 244 1998 322 329
47. M. Vilar, A. Sauri, M. Monne, J.F. Marcos, G. von Heijne, E. Perez-Paya, and I. Mingarro Insertion and topology of a plant viral movement protein in the endoplasmic reticulum membrane J. Biol. Chem. 277 2002 23447 23452
48. E. Waigmann, W.J. Lucas, V. Citovsky, and P. Zambryski 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. U.S.A. 91 1994 1433 1437
49. E. Waigmann, M.H. Chen, R. Bachmaier, S. Ghoshroy, and V. Citovsky Regulation of plasmodesmal transport by phosphorylation of Tobacco mosaic virus cell-to-cell movement protein EMBO J. 19 2000 4875 4884
50. H.L. Wang, Y. Wang, D. Giesman-Cookmeyer, S.A. Lommel, and W.J. Lucas Mutations in viral movement protein alter systemic infection and identify an intercellular barrier to entry into the phloem long-distance transport system Virology 245 1998 75 89
51. S. Wolf, C.M. Deom, R.N. Beachy, and W.J. Lucas Movement protein of Tobacco mosaic virus modifies plasmodesmatal size exclusion limit Science 246 1989 377 379
52. Z. Xiong, and S.A. Lommel The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA-1 Virology 171 1989 543 554
53. Z. Xiong, and S.A. Lommel Red clover necrotic mosaic virus infectious transcripts synthesized in vitro Virology 182 1991 388 392
54. Z. Xiong, K.H. Kim, T.L. Kendall, and S.A. Lommel Synthesis of the putative red clover necrotic mosaic virus RNA polymerase by ribosomal frameshifting in vitro Virology 193 1993 213 221
55. Z. Xiong, K.H. Kim, D. Giesman-Cookmeyer, and S.A. Lommel The roles of the Red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection Virology 192 1993 27 32
56. S.K. Zavriev, C.M. Hickey, and S.A. Lommel Mapping of the Red clover necrotic mosaic virus subgenomic RNA Virology 216 1996 407 410