The geminivirus BL1 movement protein is associated with endoplasmic reticulum-derived tubules in developing phloem cells

Journal of Virology

Volumn 71, Issue 5, 1997, Pages 3726-3733

  Ward, Brian M ^a   Medville, Richard ^b   Lazarowitz, Sondra G ^a   Turgeon, Robert ^c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Electron Microscopy Services   (United States)

^c Department of Population Medicine and Diagnostic Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ARTICLE; CELL FRACTIONATION; CELL MOTION; ENDOPLASMIC RETICULUM; GEMINIVIRUS; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VIRUS PATHOGENESIS;

EID: 0030935012     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.5.3726-3733.1997     Document Type: Article

References (66)

1. Anderson, J. V., Q.-B. Li, D. W. Haskell, and C. L. Guy. 1994. Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat shock genes during cold acclimation. Plant Physiol. 104:1359-1370.
2. Atabekov, J. G., and Y. L. Dorokhov. 1984. Plant virus-specific transport function and resistance of plants to viruses. Adv. Virus Res. 29:313-363.
3. Beebe, D. U., and R. Turgeon. 1991. Current perspectives on plasmodesmata: structure and function. Physiol. Plant. 83:194-199.
4. Ben-Ze'ev, A., R. Abulafia, and Y. Aloni. 1982. SV40 virions and viral RNA metabolism are associated with cell substructures. EMBO J. 1:1225-1231.
5. Brough, C. L., R. J. Hayes, A. J. Morgan, R. H. Coutts, and K. W. Buck. 1988. Effects of mutagenesis in vitro on the ability of cloned tomato golden mosaic virus DNA to infect Nicotiana benthamiana plants. J. Gen. Virol. 69:503-514.
6. Bush, D. R. 1989. Proton-coupled sucrose transport in plasmalemma vesicles isolated from sugar beet leaves. Plant Physiol. 89:1318-1323.
7. Chatterjee, P., M. Cervera, and S. Penman. 1984. Formation of vesicular stomatitis virus nucleocapsid cytoskeleton framework-bound N protein: possible model for structure assembly. Mol. Cell. Biol. 4:2231-2234.
8. Citovsky, V., D. Knorr, G. Schuster, and P. Zambryski. 1990. The P30 movement protein of tobacco mosaic virus is a single-stranded nucleic acid binding protein. Cell 60:637-647.
9. Citovsky, V., M. L. Wong, A. L. Shaw, B. V. Venkataram Prasad, and P. Zambryski. 1992. Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397-411.
10. Citovsky, V., and P. Zambryski. 1993. Transport of nucleic acids through membrane channels: snaking through small holes. Annu. Rev. Microbiol. 47:167-197.
11. Denecke, J., M. H. S. Goldman, J. Demolder, J. Seurinck, and J. Botterman. 1991. The tobacco luminal binding protein is encoded hy a multigene family. Plant Cell 3:1025-1035.
12. Epel, B. L. 1994. Plasmodesmata: composition, structure and trafficking. Plant Mol. Biol. 26:1343-1356.
13. Etessami, P., R. Callis, S. Ellwood, and J. Stanley. 1988. Delimitation of the essential genes of the cassava latent virus DNA 2. Nucleic Acids Res. 16: 4811-4829.
14. Fontes, E. B. P., B. B. Shank, R. L. Wrobel, S. P. Moose, G. R. OBrian, E. T. Wurtzel, and R. S. Boston. 1991. Characterization of an immunoglobulin binding protein homolog in the Maize floury-2 endosperm mutant. Plant Cell 3:483-496.
15. Fujiwara, T., D. Giesman-Cookmeyer, B. Ding, S. A. Lommel, and W. J. Lucas. 1993. Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red clover necrotic virus movement protein. Plant Cell 5:1783-1794.
16. Gilikin, J. W., E. P. B. Fontes, and R. S. Boston. 1995. Protein-protein interactions within the endoplasmic reticulum. Methods Cell Biol. 50:309-323.
17. Goldbach, R., J. Wellink, J. Verver, A. van Kammen, D. Kasteel, and J. van Lent. 1994. Adaptation of positive-strand RNA viruses to plants. Arch. Virol. Suppl. 9:87-97.
18. Goodman, R. M. 1981. Geminiviruses, p. 879-910. In E. Kurstak (ed.), Handbook of plant virus infection and comparative diagnosis. Elsevier/North Holland Biomedical Press, New York, N.Y.
19. Heinlein, M., B. L. Epel, H. S. Padgett, and R. N. Beachy. 1996. Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270:1983-1985.
20. Hepler, P. K. 1982. Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111:121-133.
21. Hull, R. 1991. The movement of viruses within plants. Semin. Virol. 2:89-95.
22. Ingham, D. J., E. Pascal, and S. G. Lazarowitz. 1995. Both geminivirus movement proteins define viral host range, but only BL1 determines viral pathogenicity. Virology 207:191-204.
23. Kim, K.-S., and K.-W. Lee. 1992. Geminivirus-induced macrotubules and their suggested role in cell-to-cell movement. Phytopathology 82:664-669.
24. M protein of tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology 200:56-65.
25. Kozutsumi, Y., M. Segal, K. Normington, M. J. Gething, and J. Sambrook. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332:462-464.
26. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
27. Lapidot, M., R. Gafny, B. Ding, S. Wolf, W. J. Lucas, and R. N. Beachy. 1993. A dysfunctional movement protein of tobacco mosaic virus that partially modifies the plasmodesmata and limits virus spread in transgenic plants. Plant J. 4:959-970.
28. Larsson, C. 1985. Plasma membranes, p. 85-104. In H. F. Linskens and J. F. Jackson (ed.), Modern methods of plant analysis, vol. 1. Springer-Verlag, Berlin, Germany.
29. 28a. Laukaitis, C. M., and S. G. Lazarowitz, Unpublished results.
30. Lazarowitz, S. G. 1992. Geminiviruses: genome structure and gene function. Crit. Rev. Plant Sci. 11:327-349.
31. Lazarowitz, S. G. 1991. Molecular characterization of two bipartite geminiviruses causing squash leaf curl disease: role of viral replication and movement functions in determining host range. Virology 180:70-80.
32. Lazarowitz, S. G., and I. B. Lazdins. 1991. Infectivity and complete nucleotide sequence of the cloned genomic components of a bipartite squash leaf curl ceminivirus with a broad host range phenotype. Virology 180:58-69.
33. Linstead, P. J., G. J. Hills, K. A. Plaskitt, I. G. Wilson, C. L. Harker, and A. J. Maule. 1988. The subcellular localization of the gene 1 product of cauliflower mosaic virus is consistent with a function associated with virus spread. J. Gen. Virol. 69:1809-1818.
34. Lucas, W. J., B. Ding, and C. van der Schoot. 1993. Plasmodesmata and the supracellular nature of plants. New Phytol. 125:435-476.
35. Lucas, W. J., and R. L. Gilbertson. 1994. Plasmodesmata in relation to viral movement within leaf tissues. Annu. Rev. Phytopathol. 32:387-411.
36. Malyshenko, S. I., O. A. Kondakova, J. V. Nazarova, I. B. Kaplan, M. E. Taliansky, and J. G. Atabekov. 1993. Reduction of tobacco mosaic virus accumulation in transgenic plants producing non-functional viral transport proteins. J. Gen. Virol. 74:1149-1156.
37. McLean, B. G., J. Zupan, and P. C. Zambryski. 1996. Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell. 7:2101-2114.
38. McMillan, D. R., M. J. Gething, and J. Sambrook. 1994. The cellular response to unfolded proteins: intercompartmental signaling. Curr. Opin. Biotechnol. 5:540-545.
39. Noueiry, A. O., W. J. Lucas, and R. L. Gilbertson. 1994. Two proteins of a plant DNA virus coordinate nuclear and plasmodesmatal transport. Cell 76:925-932.
40. Overall, R. L., J. Wolf, and B. E. S. Gunning. 1982. Intercellular communication in Azolla roots. I. Ultrastructure of plasmodesmata. Protoplasma 111:134-150.
41. Padidam, M., R. N. Beachy, and C. M. Fauquet. 1995. Classification and identification of geminiviruses using sequence comparisons. J. Gen. Virol. 76:249-263.
42. Pascal, E., P. E. Goodlove, L. C. Wu, and S. G. Lazarowitz. 1993. Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell 5:795-807.
43. Pascal, E., A. A. Sanderfoot, B. M. Ward, R. Medville, R. Turgeon, and S. G. Lazarowitz. 1994. The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6:995-1006.
44. Penfold, M. E., P. Armati, and A. L. Cunningham. 1994. Axonal transport of herpes simplex virions to epidermal cells: evidence for a specialized mode of virus transport and assembly. Proc. Natl. Acad. Sci. USA 91:6529-6533.
45. Perbal, M.-C., C. L. Thomas, and A. J. Maule. 1993. Cauliflower mosaic virus gene 1 product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195:281-285.
46. Quinlan, M. P., and D. M. Knipe. 1983. Nuclear localization of herpes viral proteins: potential role for the cellular framework. Mol. Cell. Biol. 3:315-324.
47. Ritzenthaler, C., A.-C. Schmit, P. Michler, C. Stussi-Garaud, and L. Pinck. 1995. Grapevine fanleaf nepoviruse P38 putative movement protein is located on tubules in vivo. MPMI 8:379-387.
48. Sanderfoot, A. A., D. J. Ingham, and S. G. Lazarowitz. 1996. A viral movement protein as a nuclear shuttle: the geminivirus BR1 movement protein contains domains essential for interaction with BL1 and nuclear localization. Plant Physiol. 110:23-33.
49. Sanderfoot, A. A., and S. G. Lazarowitz. 1995. Cooperation in viral movement: the geminivirus BL1 movement protein interacts with BR1 and redirects it from the nucleus to the cell periphery. Plant Cell 7:1185-1194.
50. Sanderfoot, A. A., and S. G. Lazarowitz. 1996. Getting it together in plant virus movement: cooperative interactions between bipartite geminivirus movement proteins. Trends Cell Biol. 6:353-358.
51. Stanley, J. 1985. The molecular biology of geminiviruses. Adv. Virus Res. 30:139-177.
52. Storms, M. M. H., R. Kormelink, D. Peters, J. W. M. Van Lent, and R. W. Goldbach. 1995. The nonstructural NSm protein of tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214:485-493.
53. Topp, K. S., L. B. Meade, and J. H. La La Vail. 1994. Microtubule polarity in the peripheral processes of trigeminal ganglion cells: relevance for the retrograde transport of herpes simplex virus. J. Neurosci. 14:318-325.
54. Turgeon, R. 1989. The sink-source transition in leaves. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:119-138.
55. Turgeon, R., and P. K. Hepler. 1989. Symplastic continuity between mesophyll and companion cells in minor veins of mature Cucurbita pepo L. leaves. Planta 179:24-31.
56. Turgeon, R., and J. A. Webb. 1976. Leaf development and phloem transport in Cucurbita pepo: maturation of the minor veins. Planta 129:265-269.
57. van Lent, J., M. Storms, F. van der Meer, J. Wellink, and R. Goldbach. 1991. Tubular structures involved in movement of cowpea mosaic virus are also formed in infected cowpea protoplasts. J. Gen. Virol. 72:2615-2623.
58. van Lent, J., J. Wellink, and R. Goldbach. 1990. Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. J. Gen. Virol. 71:219-223.
59. Vitale, A., A. Ceriotti, and J. Denecke. 1993. The role of the endoplasmic reticulum in protein synthesis, modification and intracellular transport. J. Exp. Bot. 44:1417-1444.
60. Volk, G. M., R. Turgeon, and D. U. Beebe. 1996. Secondary plasmodesmata formation in the minor vein phloem of Cucumis melo L. and Cucurbita pepo L. Planta 199:425-432.
61. Waigmann, E., W. J. Lucas, V. Citovsky, and P. Zambryski. 1994. 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. USA 91:1433-1437.
62. 60a. Ward, B. M., and S. G. Lazarowitz. Unpublished results.
63. Weiczorek, A., and H. Sanfacon. 1993. Characterization and subcellular localization of tomato ringspot nepovirus putative movement protein. Virology 194:734-742.
64. Wellink, J., J. W. M. van Lent, J. Verver, T. Sijen, R. W. Goldbach, and A. van Kammen. 1993. The cowpea mosaic virus M RNA-encoded 48-kilodalton protein is responsible for induction of tubular structures in protoplasts. J. Virol. 67:3660-3664.
65. Wolf, S., C. M. Deom, R. N. Beachy, and W. J. Lucas. 1989. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377-379.
66. Zhang, F., and R. S. Boston. 1992. Increases in binding protein (BiP) accompany changes in protein body morphology in three high-lysine mutants of maize. Protoplasma 171:142-152.