At-4/1, an interactor of the Tomato spotted wilt virus movement protein, belongs to a new family of plant proteins capable of directed intra- and intercellular trafficking

Molecular Plant-Microbe Interactions

Volumn 19, Issue 8, 2006, Pages 874-883

  Paape, Martina ^a   Solovyev, Andrey G ^b   Erokhina, Tatyana N ^c   Minina, Elena A ^c   Schepetilnikov, Mikhail V ^b   Lesemann, Dietrich E ^d   Schiemann, Joachim ^d   Morozov, Sergey Yu ^b   Kellmann, Jan W ^a,e  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Cell to cell trafficking

Indexed keywords

ARABIDOPSIS PROTEIN; AT 4 1 PROTEIN, ARABIDOPSIS; AT-4-1 PROTEIN, ARABIDOPSIS; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PLANT VIRUS MOVEMENT PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CYTOLOGY; GENE LIBRARY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PLANT LEAF; PLASMODESMA; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TOBACCO; TOSPOVIRUS; TRANSGENIC PLANT; TWO HYBRID SYSTEM; VIROLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CONSERVED SEQUENCE; GENE LIBRARY; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLANT LEAVES; PLANT VIRAL MOVEMENT PROTEINS; PLANTS, GENETICALLY MODIFIED; PLASMODESMATA; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TOBACCO; TOSPOVIRUS; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; TOMATO SPOTTED WILT VIRUS; TOSPOVIRUS; TRACHEOPHYTA;

EID: 33746220460     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-0874     Document Type: Article

References (70)

1. Bayer, E., Thomas, C. L., and Maule, A. J. 2004. Plasmodesmata in Arabidopsis thaliana suspension cells. Protoplasma 223:93-102.
2. Blackman, L. M., and Overall, R. L. 2001. Structure and function of plasmodesmata. Aust. J. Plant. Physiol. 28:709-727.
3. Blackman, L. M., Boevink, P., Santa Cruz, S., Palukaitis, P., and Oparka, K. 1998. The movement protein of cucumber mosaic virus traffics into sieve elements in minor veins of Nicotiana clevelandii. Plant Cell 10:525-537.
4. Boevink, P., Oparka, K., Sant Cruz, S., Martin, B., Betteridge, A., and Hawes, C. 1998. Stacks on tracks: The plant Golgi apparatus traffics on an actin/ER network. Plant J. 15:441-447.
5. Boevink, P., Martin, B., Oparka, K., Santa Cruz, S., and Hawes, C. 1999. Transport of virally expressed green fluorescent protein through the secretory pathway in tobacco leaves is inhibited by cold shock and brefeldin A. Planta 208:392-400.
6. Brandizzi, F, Fricker, M., and Hawes, C. 2002a. A greener world: The revolution in plant bioimaging. Nat. Rev. Mol. Cell Biol. 3:520-530.
7. Brandizzi, F., Snapp, E. L., Roberts, A. G., Lippincott-Schwartz, J., and Hawes, C. 2002b. 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.
8. Canto, T., and Palukaitis, P. 2005. Subcellular distribution of mutant movement proteins of Cucumber mosaic virus fused to green fluorescent proteins. J. Gen. Virol. 86:1223-1228.
9. Carrington, J. C., Kasschau, K. D., Mahajan, S. K., and Schaad, M. C. 1996. Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669-1681.
10. Chen, M. H., and Citovsky, V. 2003. Systemic movement of a Tobamovirus requires host cell pectin methylesterase. Plant J. 35:386-392.
11. Chen, M. H., Tian, G.-W., Gafni, Y., and Citovsky, V. 2005. Effects of calreticulin on viral cell-to-cell movement. Plant Physiol. 138:1866-1876.
12. Cilia, M. L., and Jackson, D. 2004. Plasmodesmata form and function. Curr. Opin. Cell Biol. 16:500-506.
13. Citovsky, V., Wong, M. L., Shaw, A. L., Prasad, B. V., and Zambryski, P. 1992. Visualization and characterization of Tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397-411.
14. Cowan, G. H., Lioliopoulou, F., Ziegler, A., and Torrance L. 2002. Subcellular localisation, protein interactions, and RNA binding of Potato mop-top virus triple gene block proteins. Virology 298:106-115.
15. Daniell, H. 1993. Foreign gene expression in chloroplasts of higher plants mediated by tungsten particle bombardment. Methods Enzymol. 217:536-556.
16. Epel, B. L., Padgett, H. S., Heinlein, M., and Beachy, R. N. 1996. Plant virus movement protein dynamics probed with a GFP-protein fusion. Gene 173:75-79.
17. Erhardt, M., Morant, M., Ritzenthaler, C., Stussi-Garaud, C., Guilley, H., Richards, K. E., Jonard, G., Bouzoubaa, S., and Gilmer, D. 2000. P42 movement protein of Beet necrotic yellow vein virus is targeted by the movement proteins p13 and p15 to punctate bodies associated with plasmodesmata. Mol. Plant-Microbe Interact. 13:520-528.
18. Falbel, T. G., Koch, L. M., Nadeau, J. A., Segui-Simarro, J. M., Sack, F. D., and Bednarek, S. Y. 2003. SCD1 is required for cell cytokinesis and polarized cell expansion in Arabidopsis thaliana. Development 130:4011-4024.
19. Faulkner, C., Brandom, J., Maule, A., and Oparka, K. 2005. Plasmodesmata 2004. Surfing the Symplasm. Plant Physiol. 137:607-610.
20. Fridborg, I., Grainger, J., Page, A., Coleman, M., Findlay, K., and Angell, S. 2003. TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X. Mol. Plant-Microbe Interact. 16:132-140.
21. Fu, K., Li, H., and Yang, Z. 2002. The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777-794.
22. Gallagher, K. L., and Benfey, P. N. 2005. Not just another hole in the wall: Understanding intercellular protein trafficking. Genes Dev. 19:189-195.
23. Gorshkova, E. N., Erokhina, T. N., Stroganova, T. A., Yelina, N. E., Zamyatnin, A. A. Jr., Kalinina, N. O., Schiemann, J., Solovyev, A. G., and Morozov, S. Yu. 2003. Immunodetection and fluorescent microscopy of transgenically expressed Hordeivirus TGBp3 movement protein reveals its association with endoplasmic reticulum elements in close proximity to plasmodesmata. J. Gen. Virol. 84:985-994.
24. Haywood, V., Kragler, F., and Lucas, W. J. 2002. Plasmodesmata: Pathways for protein and ribonucleoprotein signaling. Plant Cell 14 (Suppl.):S303-S325.
25. Heinlein, M. 2002. Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Curr. Opin. Plant Biol. 5:543-552.
26. Heinlein, M., and Epel, B. L. 2004. Macromolecular transport and signaling through plasmodesmata. Int. Rev. Cytol. 235:93-164.
27. Huang, Z., Andrianov, V. M., Han, Y., and Howell, S. H. 2001. Identification of Arabidopsis proteins that interact with the Cauliflower mosaic virus (CaMV) movement protein. Plant Mol. Biol. 47:663-675.
28. Itaya, A., Woo, Y.-M., Masuta, C., Bao, Y., Nelson, R. S., and Ding, B. 1998. Developmental regulation of intercellular protein trafficking through plasmodesmata in tobacco leaf epidermis. Plant Physiol. 118:373-385.
29. Jones, M. A., Shen, J.-J., Fu, Y., Li, H., Yang, Z., and Grierson, C.S. 2002. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763-776.
30. Ju, H.-J., Samuels, T. D., Wang, Y.-S., Blancaflor, E., Payton, M., Mitra, R., Krishnamurthy, K., Nelson, R. S., and Verchot-Lubicz, J. 2005. The Potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiol. 138:1877-1895.
31. Kang, B.-H., Busse, J. S., and Bednarek, S.Y. 2003. Members of the Arabidopsis dynamin-like genes family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell 15:899-913.
32. Kellmann, J.-W. 2001. Identification of plant virus movement-host protein interactions. Z. Naturforsch. 56:669-679.
33. Kim, J.-Y. 2005. Regulation of short-distance transport of RNA and protein. Curr. Opin. Plant Biol. 8:45-52.
34. Kim, J.-Y., Yuan, Z., Cilia, M., Khalfan-Jagani, Z., and Jackson, D. 2002. Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc. Nat. Acad. Sci. U.S.A. 99:4103-4108.
35. Kim, J.-Y., Yuan, Z., and Jackson, D. 2003. Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351-4362.
36. Kiselyova, O. I., Yaminsky, I. V., Karger, E. M., Frolova, O. Yu., Dorokhov, Y. L., and Atabekov, J. G. 2001. Visualization by atomic force microscopy of Tobacco mosaic virus movement protein-RNA complexes formed in vitro. J. Gen. Virol. 82:1503-1508.
37. Kragler, F., Lucas, W. J., and Monzer, J. 1998. Plasmodesmata: dynamics, domains and patterning. Ann. Bot. 81:1-10.
38. Kragler, F., Curin, M., Trutnyeva, K., Gansch, A., and 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.
39. Laporte, C., Vetter, G., Loudes, A.-M., Robinson, D. G., Hillmer, S., Stussi-Garaud, C., and 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.
40. Lawrence, D. M., and Jackson, A. O. 2001. Interactions of the TGB1 protein during cell-to-cell movement of Barley stripe mosaic virus. J. Virol. 75:8712-8723.
41. Lazarowitz, S. G., and Beachy, R. N. 1999. Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11:535-548.
42. Lee, J.-Y., Yoo, B.-C., Rojas, M. R., Gomez-Ospina, N., Staehelin, L. A., and Lucas, W. J. 2003. Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392-396.
43. Lucas, W. J. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169-184.
44. Lucas, W. J., and Lee, J.-Y. 2004. Plasmodesmata as a supracellular control network in plants. Nat. Rev. Mol. Cell Biol. 5:712-726.
45. Lupas, A. 1996. Coiled-coiles: New structures and new functions. Trends Biochem Sci. 21:375-382.
46. Lupas, A., Van Dyke, M., and Stock, J. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
47. Melcher, U. 2000. The '30K' superfamily of viral movement proteins. J. Gen. Virol. 81:257-266.
48. Morozov, S. Y., and Solovyev, A. G. 1999. Genome organization in RNA viruses. Pages 47-98 in: Molecular Biology of Plant Viruses. C. L. Mandahar, ed. Kluwer Academic Publishers, Dordrecht, The Netherlands.
49. Morozov, S. Yu., and Solovyev, A. G. 2003. Triple gene block: modular design of a multifunctional machine for plant virus movement. J. Gen. Virol. 84:1351-1366.
50. Nelson, R. S. 2005. Movement of viruses to and through plasmodesmata. Pages 188-209 in: Plasmodesmata. K. Oparka, ed. Blackwell Publishing Ltd., Oxford, U.K.
51. Oparka, K. J. 2004. Getting the message across: How do plant cells exchange macromolecular complexes? Trends Plant Sci. 9:33-41.
52. Oparka, K. J., Prior, D. A. M., Santa Cruz, S., Padgett, H. S., and Beachy, R. N. 1997. Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus (TMV). Plant J. 12:781-789.
53. Rinne, P. L. H., van den Boogaard, R., Mensink, M. G. J., Kopperud, C., Kormelink, R., Goldbach, R., and van der Schoot, C. 2005. Tobacco plants respond to the constitutive expression of the Tospovirus movement protein NSm with a heat-reversible sealing of plasmodesmata that impairs development. Plant J. 43:688-707.
54. Roberts, A. G., and Oparka, K. J. 2003. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 26:103-124.
55. Ruiz-Medrano, R., Xoconostle-Cazares, B., and Kragler, F. 2004. The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses. Curr. Opin. Plant Biol. 7:641-650.
56. Sakamoto, K., and Briggs, W. R. 2002. Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723-1735.
57. Schepetilnikov, M. V., Manske, U., Solovyev, A. G., Zamyatnin Jr., A. A., Schiemann, J., and Morozov, S. Yu. 2005. The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J. Gen. Virol. 86:2379-2391.
58. Scholthof, H. B. 2005. Plant virus transport: Motions of functional equivalence. Trends Plant Sci. 10:376-382.
59. Solovyev, A. G., Stroganova, T. A., Zamyatnin, A. A., Jr., Fedorkin, O. N., Schiemann, J., and Morozov, S. Yu. 2000. Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269:113-127.
60. Töpfer, R., Matzeit, V., Gronenborn, B., Schell, J., and Steinbiss, H.-H. 1987. A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res. 15:5890.
61. Tremblay, D., Vaewhongs, A. A., Turner, K. A., Sit, T. L., and Lommel, S. A. 2005. Cell wall localization of Red clover necrotic mosaic virus movement protein is required for cell-to-cell movement. Virology 333:10-21.
62. Tzfira, T., Rhee, Y., Chen, M. H., Kunik, T., and Citovsky, V. 2000. Nucleic acid transport in plant-microbe interactions: The molecules that walk through the walls. Annu. Rev. Microbiol. 54:187-219.
63. Ueki, S., and Citovsky, V. 2005. Control improves with age: Intercellular transport in plant embryos and adults. Proc. Natl. Acad. Sci. U.S.A. 102:1817-1818.
64. Verchot-Lubicz, J. 2005. A new cell-to-cell transport model for Potexviruses. Mol. Plant-Microbe Interact. 18:283-290.
65. von Bargen, S., Salchert, K., Paape, M., Piechulla, B., and Kellmann, J.-W. 2001. Interactions between the Tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin and DnaJ-like chaperones. Plant Physiol. Biochem. 39:1083-1093.
66. Waigmann, E., Ueki, S., Trutnyeva, K., and 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.
67. Yelina, N. E., Erokhina, T. N., Lukhovitskaya, N. I., Minina, E. A., Schepetilnikov, M. V., Lesemann, D. E., Schiemann, J., Solovyev, A. G., and Morozov, S. Yu. 2005. Localization of Poa semilatent virus cysteine-rich protein in peroxisomes is dispensable for its ability to suppress RNA silencing. J. Gen. Virol. 86:479-489.
68. Zamyatnin, A. A., Jr., Solovyev, A. G., Sablina, A. A., Agranovsky, A. A., Katul, L., Vetten, H. J., Schiemann, J., Hinkkanen, A. E., Lehto, K., and Morozov, S. Yu. 2002. Dual-color imaging of membrane protein targeting directed by poa semilatent virus movement protein TGBp3 in plant and mammalian cells. J. Gen. Virol. 83:651-662.
69. Zamyatnin, A. A., Jr., Solovyev, A. G., Savenkov, E. I., Germundsson, A., Sandgren, M., Valkonen, J. P. T., and Morozov, S. Yu. 2004. Transient coexpression of individual genes encoded by the triple gene block of Potato mop-top virus reveals requirements for TGBp1 trafficking. Mol. Plant-Microbe Interact. 17:921-930.
70. Zuo, J., Niu, Q., Nishizawa, N., Wu, Y., Kost, B., and Chua, N. 2000. KORRIGAN, an Arabidopsis endo-1,4-β-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12:1137-1152.