Inhibition of tobacco mosaic virus movement by expression of an actin-binding protein1[W][OA]

Plant Physiology

Volumn 149, Issue 4, 2009, Pages 1810-1823

  Hofmann, Christina ^a   Niehl, Annette ^a   Sambade, Adrian ^a,c   Steinmetz, André ^b   Heinlein, Manfred ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA BENTHAMIANA; TOBACCO MOSAIC VIRUS;

EID: 65249163294     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.133827     Document Type: Article

References (84)

1. Ashby J, Boutant E, Seemanpillai M, Groner A, Sambade A, Ritzenthaler C, Heinlein M (2006) Tobaccomosaic virus movement protein functions as a structural microtubule-associated protein. J Virol 80: 8329-8344
2. Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN (1991) The Tobaccomosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol 72: 209-211
3. Avisar D, Prokhnevsky AI, Dolja VV (2008a) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82: 2836-2843
4. 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: 1098-1108
5. 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: 441-447
6. Boyko V, Ferralli J, Ashby J, Schellenbaum P, Heinlein M (2000a) Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2: 826-832
7. Boyko V, Ferralli J, Heinlein M (2000b) Cell-to-cell movement of TMV RNA is temperature-dependent and corresponds to the association of movement protein with microtubules. Plant J 22: 315-325
8. Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M (2007) Validation of microtubule-associated Tobaccomosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51: 589-603
9. Brandizzi F, Snapp EL, Roberts AG, Lippincott-Schwartz J, Hawes C (2002) Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 14: 1293-1309
10. Brandner K, Sambade A, Boutant E, Didier P, Mely Y, Ritzenthaler C, Heinlein M (2008) TMV movement protein interacts with GFP-tagged microtubule end-binding protein 1 (EB1). Plant Physiol 147: 611-623
11. Brill LM, Nunn RS, Kahn TW, Yeager M, Beachy RN (2000) Recombinant Tobaccomosaic virus movement protein is an RNA-binding, α-helical membrane protein. Proc Natl Acad Sci USA 97: 7112-7117
12. Carrington JC, Kasschau KD, Mahajan SK, Schaad MC (1996) Cell-to-cell and long distance transport of viruses in plants. Plant Cell 8: 1669-1681
13. Chan J, Calder GM, Doonan JH, Lloyd CW (2003) EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5: 967-971
14. Citovsky V (1999) Tobaccomosaic virus : a pioneer of cell-to-cell movement. Philos Trans R Soc Lond B Biol Sci 354: 637-643
15. Citovsky V, Knorr D, Schuster G, Zambryski P (1990) The P30 movement protein of Tobaccomosaic virus is a single-stranded nucleic acid binding protein. Cell 60: 637-647
16. Dawson WO, Bubrick P, Grantham GL (1988) Modifications of the Tobacco mosaic virus coat protein gene affecting replication, movement, and symptomatology. Phytopathology 78: 783-789
17. Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ (1992a) Secondary plasmodesmata are specific sites of localization of the Tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4: 915-928
18. Ding B, Turgeon R, Parthasarathy MV (1992b) Substructure of freeze-substituted plasmodesmata. Protoplasma 169: 28-41
19. Dixit R, Chang E, Cyr R (2006) Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell 17: 1298-1305
20. Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319: 1086-1089
21. Dorokhov YL, Alexandrova NM, Miroshnichenko NA, Atabekov JG (1983) Isolation and analysis of virus-specific ribonucleoprotein of Tobacco mosaic virus-infected tobacco. Virology 127: 237-252
22. Dorokhov YL, Alexandrova NM, Miroshnichenko NA, Atabekov JG(1984) The informosome-like virus-specific ribonucleoprotein (vRNP) may be involved in the transport of Tobaccomosaic virus infection. Virology 137: 127-134
23. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143: 777-794
24. 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: 5807-5821
25. Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152: 1019-1032
26. Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8: 3
27. Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL (2008) Tobacco mosaic virus (TMV) replicase and movement protein function synergis-tically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant Microbe Interact 21: 335-345
28. Heinlein M (2002) Plasmodesmata: dynamic regulation and role in mac-romolecular cell-to-cell signalling. Curr Opin Plant Biol 5: 543-552
29. Heinlein M, Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol 235: 93-164
30. Heinlein M, Epel BL, Padgett HS, Beachy RN (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270: 1983-1985
31. 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
32. Hilf ME, Dawson WO (1993) The tobamovirus capsid protein functions as a host-specific determinant of long-distance movement. Virology 193: 106-114
33. Holweg C, Susslin C, Nick P (2004) Capturing in vivo dynamics of the actin cytoskeleton stimulated by auxin or light. Plant Cell Physiol 45: 855-863
34. Holweg CL (2007) Living markers for actin block myosin-dependent motility of plant organelles and auxin. Cell Motil Cytoskeleton 64: 69-81
35. Horsch RB, Rogers SG, Fraley RT (1985) Transgenic plants. Cold Spring Harb Symp Quant Biol 50: 433-437
36. Ilgenfritz H, Bouyer D, Schnittger A, Mathur J, Kirik V, Schwab B, Chua NH, Jürgens G, Hülskamp M (2003) The Arabidopsis STICHEL gene is a regulator of trichome branch number and encodes a novel protein. Plant Physiol 131: 643-655
37. Karimi M, Inze D, Depicker A (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195
38. Kashiyama T, Kimura N, Mimura T, Yamamoto K (2000) Cloning and characterization of a myosin from characean alga, the fastest motor protein in the world. J Biochem 127: 1065-1070
39. Kawakami S, Watanabe Y, Beachy RN (2004) Tobaccomosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 01 6291-6296
40. Ketelaar T, Anthony RG, Hussey PJ (2004) Green fluorescent protein-mTalin causes defects in actin organization and cell expansion in Arabidopsis and inhibits actin depolymerizing factor's actin depoly-merizing activity in vitro. Plant Physiol 136: 3990-3998
41. Kimura Y, Toyoshima N, Hirakawa N, Okamoto K, Ishijima A (2003) A kinetic mechanism for the fast movement of Chara myosin. J Mol Biol 328: 939-950
42. Kost B, Spielhofer P, Chua NH (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16: 393-401
43. Lazarowitz SG, Beachy RN (1999) Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11: 535-548
44. Li H, Roossinck MJ (2004) Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 78: 10582-10587
45. Lichtscheidl IK, Baluska F (2000) Actin-based motility of endoplasmic reticulum in plant cells. In CJ Staiger, F Baluska, D Volkmann, PW Barlow, eds, Actin, a Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 191-201
46. Liu JZ, 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: 1877-1895
47. Lopez LA, Sheetz MP (1993) Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil Cytoskeleton 24: 1-16
48. Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344: 169-184
49. Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5: 712-726
50. Mathur J, Mathur N, Kernebeck B, Srinivas BP, Hülskamp M (2003) A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization. Curr Biol 13: 1991-1997
51. Mathur J, Spielhofer P, Kost B, Chua N (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559-5568
52. McLean BG, Zupan J, Zambryski PC (1995) Tobaccomosaic virus movement protein associates with the cytoskeleton in tobacco plants. Plant Cell 7: 2101-2114
53. Moore P, Fenczik CA, Deom CM, Beachy RN (1992) Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of Tobaccomosaic virus. Protoplasma 170: 115-127
54. Morimatsu M, Nakamura A, Sumiyoshi H, Sakaba N, Taniguchi H, Kohama K, Higashi-Fujime S (2000) The molecular structure of the fastest myosin from green algae, Chara. Biochem Biophys Res Commun 270: 147-152
55. Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121: 1127-1142
56. 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 Tobaccomosaic virus. Plant J 12: 781-789
57. Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146: 1109-1116
58. 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: 14421-14428
59. 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: 19744-19749
60. 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: 555-567
61. Ruiz MT, Voinnet O, Baulcombe DC (1998) Initiation and maintenance of virus-induced gene silencing. Plant Cell 10: 937-946
62. Runions J, Brach T, Kuhner S, Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57: 43-50
63. Sacristan S, Malpica JM, Fraile A, Garcia-Arenal F (2003) Estimation of population bottlenecks during systemic movement of Tobaccomosaic virus in tobacco plants. J Virol 77: 9906-9911
64. Saito T, Yamanaka K, Okada Y (1990) Long-distance movement and viral assembly of Tobaccomosaic virus mutants. Virology 176: 329-336
65. 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
66. Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136: 3968-3978
67. Siegel A, Hari V, Kolacz K (1978) The effect of Tobacco mosaic virus infection on host and virus-specific protein synthesis in protoplasts. Virology 85: 494-503
68. Sparkes IA, Teanby NA, Hawes C (2008) Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J Exp Bot 59: 2499-2512
69. Staiger CJ, Blanchoin L (2006) Actin dynamics: old friends with new stories. Curr Opin Plant Biol 9: 554-562
70. Tomenius K, Clapham D, Meshi T (1987) Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with Tobacco mosaic virus. Virology 160: 363-371
71. Tominaga M, Kojima H, Yokota E, Orii H, Nakamori R, Katayama E, Anson M, Shimmen T, Oiwa K (2003) Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. EMBO J 22: 1263-1272
72. 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: 187-219
73. Van Damme D, Van Poucke K, Boutant E, Ritzenthaler C, Inze D, Geelen D (2004) In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136: 3956-3967
74. Verchot-Lubicz J, Ye CM, Bamunusinghe D (2007) Molecular biology of potexviruses: recent advances. J Gen Virol 88: 1643-1655
75. Vershinin M, Xu J, Razafsky DS, King SJ, Gross SP (2008) Tuning microtubule-based transport through filamentous MAPs: the problem of dynein. Traffic 9: 882-892
76. Vetter G, Hily JM, Klein E, Schmidlin L, Haas M, Merkle T, Gilmer D (2004) Nucleo-cytoplasmic shuttling of the Beet necrotic yellow vein virus RNA-3-encoded p25 protein. J Gen Virol 85: 2459-2469
77. Volkmann D, Mori T, Tirlapur UK, Konig K, Fujiwara T, Kendrick-Jones J, Baluska F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 27: 289-291
78. Waigmann E, Ueki S, Trutnyeva K, Citovsky V (2004) The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Crit Rev Plant Sci 23: 195-250
79. Wang YS, Yoo CM, Blancaflor EB (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actin-binding domain 2. New Phytol 177: 525-536
80. Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci USA 102: 3147-3152
81. Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of Tobaccomosaic virus modifies plasmodesmatal size exclusion limit. Science 246: 377-379
82. Wright KM, Wood NT, Roberts AG, Chapman S, Boevink P, Mackenzie KM, Oparka KJ (2007) Targeting of TMV movement protein to plasmodes-mata requires the actin/ER network: evidence from FRAP. Traffic 8: 21-31
83. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17: 525-536
84. Yokota E, Ueda S, Tamura K, Orii H, Uchi S, Sonobe S, Hara-Nishimura I, Shimmen T (2009) An isoform of myosin XI is responsible for the translocation of endoplasmic reticulum in tobacco cultured BY-2 cells. J Exp Bot 60: 197-212