1887

Abstract

The movement function of poa semilatent hordeivirus (PSLV) is mediated by the triple gene block (TGB) proteins, of which two, TGBp2 and TGBp3, are membrane proteins. TGBp3 is localized to peripheral bodies in the vicinity of the plasma membrane and is able to re-direct TGBp2 from the endoplasmic reticulum (ER) to the peripheral bodies. For imaging of TGBp3-mediated protein targeting, PSLV TGBp3 tagged with a red fluorescent protein (DsRed) was used. Coexpression of DsRed-TGBp3 with GFP targeted to the ER lumen (ER-GFP) demonstrated that ER-GFP was contained in typical ER structures and peripheral bodies formed by TGBp3 protein, suggesting an ER origin for these bodies. In transient coexpression with viral membrane proteins tagged with GFP, DsRed-TGBp3 directed to the peripheral bodies the homologous TGBp2 protein and two unrelated membrane proteins, the 6 kDa movement protein of beet yellows closterovirus and the putative movement protein encoded by the genome component 4 of faba bean necrotic yellows nanovirus. However, coexpression of TGBp3 with GFP derivatives targeted to the ER membranes by artificial hydrophobic tail sequences suggested that targeting to the ER membranes per se was not sufficient for TGBp3-directed protein trafficking to peripheral bodies. TGBp3-induced targeting of TGBp2 also occurred in mammalian cells, indicating the universal nature of the protein trafficking signals and the cotargeting mechanism.

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2002-03-01
2020-01-20
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References

  1. Agranovsky, A. A. ( 1996; ). Principles of molecular organization, expression, and evolution of closteroviruses: over the barriers. Advances in Virus Research 47, 119-158.
    [Google Scholar]
  2. Agranovsky, A. A., Boyko, V. P., Karasev, A. V., Lunina, N. A., Koonin, E. V. & Dolja, V. V. ( 1991; ). Nucleotide sequence of the 3′-terminal half of beet yellows closterovirus RNA genome: unique arrangement of eight virus genes. Journal of General Virology 72, 15-23.[CrossRef]
    [Google Scholar]
  3. Agranovsky, A. A., Koonin, E. V., Boyko, V. P., Maiss, E., Frotschl, R., Lunina, N. A. & Atabekov, J. G. ( 1994; ). Beet yellows closterovirus: complete genome structure and identification of a leader papain-like thiol protease. Virology 198, 311-324.[CrossRef]
    [Google Scholar]
  4. Altschuler, Y., Rosenberg, N., Harel, R. & Galili, G. ( 1993; ). The N- and C-terminal regions regulate the transport of wheat gamma-gliadin through the endoplasmic reticulum in Xenopus oocytes. Plant Cell 5, 443-450.
    [Google Scholar]
  5. Alzhanova, D. V., Hagiwara, Y., Peremyslov, V. V. & Dolja, V. V. ( 2000; ). Genetic analysis of the cell-to-cell movement of beet yellows closterovirus. Virology 268, 192-200.[CrossRef]
    [Google Scholar]
  6. Andreeva, A. V., Zheng, H., Saint-Jore, C. M., Kutuzov, M. A., Evans, D. E. & Hawes, C. R. ( 2000; ). Organization of transport from endoplasmic reticulum to Golgi in higher plants. Biochemical Society Transactions 28, 505-512.[CrossRef]
    [Google Scholar]
  7. Atabekov, J. G. & Taliansky, M. E. ( 1990; ). Expression of a plant virus-coded transport function by different virus genomes. Advances in Virus Research 38, 201-248.
    [Google Scholar]
  8. Baird, G. S., Zacharias, D. A. & Tsien, R. Y. ( 2000; ). Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proceedings of the National Academy of Sciences, USA 97, 11984-11989.[CrossRef]
    [Google Scholar]
  9. Batoko, H., Zheng, H. Q., Hawes, C. & Moore, I. ( 2000; ). A rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12, 2201-2218.[CrossRef]
    [Google Scholar]
  10. Beachy, R. N. & Heinlein, M. ( 2000; ). Role of P30 in replication and spread of TMV. Traffic 1, 540-544.[CrossRef]
    [Google Scholar]
  11. Beck, D. L., Guilford, P. J., Voot, D. M., Andersen, M. T. & Forster, R. L. ( 1991; ). Triple gene block proteins of white clover mosaic potexvirus are required for transport. Virology 183, 695-702.[CrossRef]
    [Google Scholar]
  12. 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 Journal 15, 441-447.[CrossRef]
    [Google Scholar]
  13. Boevink, P., Martin, B., Oparka, K., Santa Cruz, S. & 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.[CrossRef]
    [Google Scholar]
  14. Boulton, M. I., Pallaghy, C. K., Chatani, M., MacFarlane, S. & Davies, J. W. ( 1993; ). Replication of maize streak virus mutants in maize protoplasts: evidence for a movement protein. Virology 192, 85-93.[CrossRef]
    [Google Scholar]
  15. Boyko, V., Ferralli, J. & Heinlein, M. ( 2000a; ). Cell-to cell movement of TMV RNA is temperature-dependent and corresponds to the association of movement protein with microtubules. Plant Journal 22, 315-325.[CrossRef]
    [Google Scholar]
  16. Boyko, V., Ferralli, J., Ashby, J., Schellenbaum, P. & Heinlein, M. ( 2000b; ). Function of microtubules in intercellular transport of plant virus RNA. Nature Cell Biology 2, 826-832.[CrossRef]
    [Google Scholar]
  17. Boyko, V., van der Laak, J., Ferralli, J., Suslova, E., Kwon, M. O. & Heinlein, M. ( 2000c; ). Cellular targets of functional and dysfunctional mutants of tobacco mosaic virus movement protein fused to green fluorescent protein. Journal of Virology 74, 11339-11346.[CrossRef]
    [Google Scholar]
  18. Brakke, M. K., Ball, E. M. & Langenberg, W. G. ( 1988; ). A non-capsid protein associated with unencapsidated virus RNA in barley infected with barley stripe mosaic virus. Journal of General Virology 69, 481-491.[CrossRef]
    [Google Scholar]
  19. Brill, L. M., Nunn, R. S., Kahn, T. W., Yeager, M. & Beachy, R. N. ( 2000; ). Recombinant tobacco mosaic virus movement protein is an RNA-binding, α-helical membrane protein. Proceedings of the National Academy of Sciences, USA 97, 7112-7117.[CrossRef]
    [Google Scholar]
  20. Burns, T. M., Harding, R. M. & Dale, J. L. ( 1995; ). The genome organization of banana bunchy top virus: analysis of six ssDNA components. Journal of General Virology 76, 1471-1482.[CrossRef]
    [Google Scholar]
  21. Carrington, J. C., Kasschau, K. D., Mahajan, S. K. & Schaad, M. C. ( 1996; ). Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8, 1669-1681.[CrossRef]
    [Google Scholar]
  22. Chrispeels, M. J. & Herman, E. M. ( 2000; ). Endoplasmic reticulum-derived compartments function in storage and as mediators of vacuolar remodeling via a new type of organelle, precursor protease vesicles. Plant Physiology 123, 1227-1233.[CrossRef]
    [Google Scholar]
  23. Ding, B. ( 1998; ). Intercellular protein trafficking through plasmodesmata. Plant Molecular Biology 38, 279-310.[CrossRef]
    [Google Scholar]
  24. Donald, R. G. K., Lawrence, D. M. & Jackson, A. O. ( 1997; ). The barley stripe mosaic virus 58-kilodalton βb protein is a multifunctional RNA binding protein. Journal of Virology 71, 1538-1546.
    [Google Scholar]
  25. Erhardt, M., Stussi-Garaud, C., Guilley, H., Richards, K. E., Jonard, G. & Bouzoubaa, S. ( 1999; ). The first triple gene block protein of peanut clump virus localizes to the plasmodesmata during virus infection. Virology 264, 220-229.[CrossRef]
    [Google Scholar]
  26. Erhardt, M., Morant, M., Ritzenthaler, C., Stussi-Garaud, C., Guilley, H., Richards, K. E., Jonard, G., Bouzoubaa, S. & 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. Molecular Plant–Microbe Interactions 13, 520-528.[CrossRef]
    [Google Scholar]
  27. Fedorkin, O. N., Solovyev, A. G., Yelina, N. E., Zamyatnin, A. A.Jr., Zinovkin, R. A., Mäkinen, K., Schiemann, J. & Morozov, S. Yu. ( 2001; ). Cell-to-cell movement of potato virus X involves distinct functions of the coat protein. Journal of General Virology 82, 449-458.
    [Google Scholar]
  28. Frigerio, L., Pastres, A., Prada, A. & Vitale, A. ( 2001; ). Influence of KDEL on the fate of trimeric or assembly-defective phaseolin: selective use of an alternative route to vacuoles. Plant Cell 13, 1109-1126.[CrossRef]
    [Google Scholar]
  29. Gilmer, D., Bouzoubaa, S., Hehn, A., 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.[CrossRef]
    [Google Scholar]
  30. Hacker, D. L., Petty, I. T., Wei, N. & Morris, T. J. ( 1992; ). Turnip crinkle virus genes required for RNA replication and virus movement. Virology 186, 1-8.[CrossRef]
    [Google Scholar]
  31. Hadlington, J. L. & Denecke, J. ( 2000; ). Sorting of soluble proteins in the secretory pathway of plants. Current Opinion in Plant Biology 3, 461-468.[CrossRef]
    [Google Scholar]
  32. Hawes, C. R., Brandizzi, F. & Andreeva, A. V. ( 1999; ). Endomembranes and vesicle trafficking. Current Opinion in Plant Biology 2, 454-461.[CrossRef]
    [Google Scholar]
  33. Heinlein, M., Epel, B. L., Padgett, H. S. & Beachy, R. N. ( 1995; ). Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270, 1983-1985.[CrossRef]
    [Google Scholar]
  34. Heinlein, M., Padgett, H. S., Gens, J. S., Pickard, B. G., Casper, S. J., Epel, B. L. & Beachy, R. N. ( 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.[CrossRef]
    [Google Scholar]
  35. Honsho, M., Mitoma, J. Y. & Ito, A. ( 1998; ). Retention of cytochrome b5 in the endoplasmic reticulum is transmembrane and luminal domain-dependent. Journal of Biological Chemistry 273, 20860-20866.[CrossRef]
    [Google Scholar]
  36. Huang, M. & Zhang, L. ( 1999; ). Association of the movement protein of alfalfa mosaic virus with the endoplasmic reticulum and its trafficking in epidermal cells of onion bulb scales. Molecular Plant–Microbe Interactions 12, 680-690.[CrossRef]
    [Google Scholar]
  37. Huang, M., Koh, D. C., Weng, L. J., Chang, M. L., Yap, Y. K., Zhang, L. & Wong, S. M. ( 2000; ). Complete nucleotide sequence and genome organization of hibiscus chlorotic ringspot virus, a new member of the genus carmovirus: evidence for the presence and expression of two novel open reading frames. Journal of Virology 74, 3149-3155.[CrossRef]
    [Google Scholar]
  38. Jackson, D. ( 2000; ). Opening up the communication channels: recent insights into plasmodesmal function. Current Opinion in Plant Biology 3, 394-399.[CrossRef]
    [Google Scholar]
  39. Jiang, L. & Rogers, J. C. ( 1998; ). Integral membrane protein sorting to vacuoles in plant cells: evidence for two pathways. Journal of Cell Biology 143, 1183-1199.[CrossRef]
    [Google Scholar]
  40. Kalinina, N. O., Rakitina, D. A., Yelina, N. E., Zamyatnin, A. A.Jr., Stroganova, T. A., Klinov, D. V., Prokhorov, V. V., Ustinova, S. V., Chernov, B. K., Schiemann, J., Solovyev, A. G. & Morozov, S. Yu. ( 2001; ). RNA binding properties of the 63-kDa protein encoded by triple gene block of poa semilatent hordeivirus. Journal of General Virology 82, 2569-2578.
    [Google Scholar]
  41. Katul, L., Maiss, E., Morozov, S. Yu. & Vetten, H. J. ( 1997; ). Analysis of six DNA components of the faba bean necrotic yellows virus genome and their structural affinity to related plant virus genomes. Virology 233, 247-259.[CrossRef]
    [Google Scholar]
  42. Kikkert, M., Verschoor, A., Kormelink, R., Rottier, P. & Goldbach, R. ( 2001; ). Tomato spotted wilt virus glycoproteins exhibit trafficking and localization signals that are functional in mammalian cells. Journal of Virology 75, 1004-1012.[CrossRef]
    [Google Scholar]
  43. Koenig, R., Pleij, C. W. A., Beier, C. & Commandeur, U. ( 1998; ). Genome properties of beet virus Q, a new furo-like virus from sugarbeet, determined from unpurified virus. Journal of General Virology 79, 2027-2036.
    [Google Scholar]
  44. Kotlizky, G., Boulton, M. I., Pitaksutheepong, C., Davies, J. W. & Epel, B. L. ( 2000; ). Intracellular and intercellular movement of maize streak geminivirus V1 and V2 proteins transiently expressed as green fluorescent protein fusions. Virology 274, 32-38.[CrossRef]
    [Google Scholar]
  45. Kotlizky, G., Katz, A., van der Laak, J., Boyko, V., Lapidot, M., Beachy, R. N., Heinlein, M. & Epel, B. L. ( 2001; ). A dysfunctional movement protein of tobacco mosaic virus interferes with targeting of wild-type movement protein to microtubules. Molecular Plant–Microbe Interactions 14, 895-904.[CrossRef]
    [Google Scholar]
  46. Lawrence, D. M. & Jackson, A. O. ( 2001a; ). Requirements for cell-to-cell movement of barley stripe mosaic virus in monocot and dicot hosts. Molecular Plant Pathology 2, 65-75.[CrossRef]
    [Google Scholar]
  47. Lawrence, D. M. & Jackson, A. O. ( 2001b; ). Interactions of the TGB1 protein during cell-to-cell movement of barley stripe mosaic virus. Journal of Virology 75, 8712-8723.[CrossRef]
    [Google Scholar]
  48. Lazarowitz, S. G. ( 1999; ). Probing plant cell structure and function with viral movement proteins. Current Opinion in Plant Biology 2, 332-338.[CrossRef]
    [Google Scholar]
  49. Lazarowitz, S. G. & Beachy, R. N. ( 1999; ). Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11, 535-548.[CrossRef]
    [Google Scholar]
  50. Letourneur, F. & Cosson, P. ( 1998; ). Targeting to the endoplasmic reticulum in yeast cells by determinants present in transmembrane domains. Journal of Biological Chemistry 273, 33273-33278.[CrossRef]
    [Google Scholar]
  51. Liu, H., Boulton, M. I., Oparka, K. J. & Davies, J. W. ( 2001; ). Interaction of the movement and coat proteins of maize streak virus: implications for the transport of viral DNA. Journal of General Virology 82, 35-44.
    [Google Scholar]
  52. Mas, P. & Beachy, R. N. ( 2000; ). Role of microtubules in the intracellular distribution of tobacco mosaic virus movement protein. Proceedings of the National Academy of Sciences, USA 97, 12345-12349.[CrossRef]
    [Google Scholar]
  53. Matz, M. V., Fradkov, A. F., Labas, Yu. A., Savitsky, A. P., Zaraisky, A. G., Markelov, M. L. & Lukyanov, S. A. ( 1999; ). Fluorescent proteins from nonbioluminescent Anthozoa species. Nature Biotechnology 17, 969-973.[CrossRef]
    [Google Scholar]
  54. McLean, B. G., Zupan, J. & Zambryski, P. C. ( 1995; ). Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7, 2101-2114.[CrossRef]
    [Google Scholar]
  55. Melcher, U. ( 2000; ). The ‘30K’ superfamily of viral movement proteins. Journal of General Virology 81, 257-266.
    [Google Scholar]
  56. Mezitt, L. A. & Lucas, W. J. ( 1996; ). Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Molecular Biology 32, 251-273.[CrossRef]
    [Google Scholar]
  57. Mitsuhashi, N., Hayashi, Y., Koumoto, Y., Shimada, T., Fukasawa-Akada, T., Nishimura, M. & Hara-Nishimura, I. ( 2001; ). A novel membrane protein that is transported to protein storage vacuoles via precursor-accumulating vesicles. Plant Cell 13, 2361-2372.[CrossRef]
    [Google Scholar]
  58. Molnar, A., Havelda, Z., Dalmay, T., Szutorisz, H. & Burgyan, J. ( 1997; ). Complete nucleotide sequence of tobacco necrosis virus strain DH and genes required for RNA replication and virus movement. Journal of General Virology 78, 1235-1239.
    [Google Scholar]
  59. Mora, R., Bonilha, V. L., Marmorstein, A., Scherer, P. E., Brown, D., Lisanti, M. P. & Rodriguez-Boulan, E. ( 1999; ). Caveolin-2 localizes to the Golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. Journal of Biological Chemistry 274, 25708-25717.[CrossRef]
    [Google Scholar]
  60. Morozov, S. Yu., Lukasheva, L. I., Chernov, B. K., Skryabin, K. G. & Atabekov, J. G. ( 1987; ). Nucleotide sequence of the open reading frames adjacent to the coat protein cistron in potato virus X genome. FEBS Letters 213, 438-442.[CrossRef]
    [Google Scholar]
  61. Morozov, S. Yu., Dolja, V. V. & Atabekov, J. G. ( 1989; ). Probable reassortment of genomic elements among elongated RNA-containing plant viruses. Journal of Molecular Evolution 29, 52-62.[CrossRef]
    [Google Scholar]
  62. Morozov, S. Yu., Miroshnichenko, N. A., Zelenina, D. A., Fedorkin, O. N., Solovijev, A. G., Lukasheva, L. I. & Atabekov, J. G. ( 1990; ). Expression of RNA transcripts of potato virus X full-length and subgenomic cDNAs. Biochimie 72, 677-684.[CrossRef]
    [Google Scholar]
  63. Morozov, S. Yu., Fedorkin, O. N., Juttner, G., Schiemann, J., Baulcombe, D. C. & Atabekov, J. G. ( 1997; ). Complementation of a potato virus X mutant mediated by bombardment of plant tissues with cloned viral movement protein genes. Journal of General Virology 78, 2077-2083.
    [Google Scholar]
  64. Mullineaux, P. M., Boulton, M. I., Bowyer, P., van der Vlugt, R., Marks, M., Donson, J. & Davies, J. W. ( 1988; ). Detection of a non-structural protein of MW 11000 encoded by the virion DNA of maize streak virus. Plant Molecular Biology 11, 57-66.[CrossRef]
    [Google Scholar]
  65. Nebenführ, A. & Staehelin, L. A. ( 2001; ). Mobile factories: Golgi dynamics in plant cells. Trends in Plant Science 6, 160-167.[CrossRef]
    [Google Scholar]
  66. Okamoto, T., Schlegel, A., Scherer, P. E. & Lisanti, M. P. ( 1998; ). Caveolins, a family of scaffolding proteins for organizing ‘preassembled signaling complexes’ at the plasma membrane. Journal of Biological Chemistry 273, 5419-5422.[CrossRef]
    [Google Scholar]
  67. Oparka, K. J. & Roberts, A. G. ( 2001; ). Plasmodesmata. A not so open-and-shut case. Plant Physiology 125, 123-126.[CrossRef]
    [Google Scholar]
  68. Parolini, I., Sargiacomo, M., Galbiati, F., Rizzo, G., Grignani, F., Engelman, J. A., Okamoto, T., Ikezu, T., Scherer, P. E., Mora, R., Rodriguez-Boulan, E., Peschle, C. & Lisanti, M. P. ( 1999; ). Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the Golgi complex. Journal of Biological Chemistry 274, 25718-25725.[CrossRef]
    [Google Scholar]
  69. Pedrazzini, E., Villa, A. & Borgese, N. ( 1996; ). A mutant cytochrome b5 with a lengthened membrane anchor escapes from the endoplasmatic reticulum and reaches the plasma membrane. Proceedings of the National Academy of Sciences, USA 93, 4207-4212.[CrossRef]
    [Google Scholar]
  70. Pedrazzini, E., Villa, A., Longhi, R., Bulbarelli, A. & Borgese, N. ( 2000; ). Mechanism of residence of cytochrome b5, a tail-anchored protein, in the endoplasmic reticulum. Journal of Cell Biology 148, 899-914.[CrossRef]
    [Google Scholar]
  71. Petty, I. T. & Jackson, A. O. ( 1990; ). Mutational analysis of barley stripe mosaic virus RNA beta. Virology 179, 712-718.[CrossRef]
    [Google Scholar]
  72. Rayner, J. C. & Pelham, H. R. ( 1997; ). Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO Journal 16, 1832-1841.[CrossRef]
    [Google Scholar]
  73. Razani, B., Rubin, C. S. & Lisanti, M. P. ( 1999; ). Regulation of cAMP-mediated signal transduction via interaction of caveolins with the catalytic subunit of protein kinase A. Journal of Biological Chemistry 274, 26353-26360.[CrossRef]
    [Google Scholar]
  74. Reichel, C. & Beachy, R. N. ( 1998; ). Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proceedings of the National Academy of Sciences, USA 95, 11169-11174.[CrossRef]
    [Google Scholar]
  75. Reichel, C., Mas, P. & Beachy, R. N. ( 1999; ). The role of the ER and cytoskeleton in plant viral trafficking. Trends in Plant Science 4, 458-452.[CrossRef]
    [Google Scholar]
  76. Rupasov, V. V., Morozov, S. Yu., Kanyuka, K. V. & Zavriev, S. K. ( 1989; ). Partial nucleotide sequence of potato virus M RNA shows similarities to potexviruses in gene arrangement and the encoded amino acid sequences. Journal of General Virology 70, 1861-1869.[CrossRef]
    [Google Scholar]
  77. Sääf, A., Wallin, E. & von Heijne, G. ( 1998; ). Stop-transfer function of pseudo-random amino acid segments during translocation across prokaryotic and eukaryotic membranes. European Journal of Biochemistry 251, 821-829.[CrossRef]
    [Google Scholar]
  78. Sambrook, J., Fritsch, E. F. & Maniatis, T. A. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  79. Sato, K., Ueda, T. & Nakano, A. ( 1999; ). The Arabidopsis thaliana RER1 gene family: its potential role in the endoplasmic reticulum localization of membrane proteins. Plant Molecular Biology 141, 815-824.
    [Google Scholar]
  80. Sato, K., Sato, M. & Nakano, A. ( 2001; ). Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. Journal of Cell Biology 152, 935-944.[CrossRef]
    [Google Scholar]
  81. Skryabin, K. G., Morozov, S. Yu., Kraev, A. S., Rozanov, M. N., Chernov, B. K., Lukasheva, L. I. & Atabekov, J. G. ( 1988; ). Conserved and variable elements in RNA genomes of potexviruses. FEBS Letters 240, 33-40.[CrossRef]
    [Google Scholar]
  82. Solovyev, A. G., Stroganova, T. A., Zamyatnin, A. A.Jr, Fedorkin, O. N., Schiemann, J. & Morozov, S. Yu. ( 2000; ). Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269, 113-127.[CrossRef]
    [Google Scholar]
  83. Tamai, A. & Meshi, T. ( 2001; ). Cell-to-cell movement of potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Molecular Plant–Microbe Interactions 14, 1158-1167.[CrossRef]
    [Google Scholar]
  84. Töpfer, R., Matzeit, V., Gronenborn, B., Schell, J. & Steinbiss, H.-H. ( 1987; ). A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Research 15, 5890.[CrossRef]
    [Google Scholar]
  85. Vitale, A. & Raikhel, N. V. ( 1999; ). What do proteins need to reach different vacuoles? Trends in Plant Science 4, 149-155.[CrossRef]
    [Google Scholar]
  86. Volonté, D., Galbiati, F. & Lisanti, M. P. ( 1999; ). Visualization of caveolin-1, a caveolar marker protein, in living cells using green fluorescent protein (GFP) chimeras. The subcellular distribution of caveolin-1 is modulated by cell-cell contact. FEBS Letters 445, 431-439.[CrossRef]
    [Google Scholar]
  87. Wall, M. A., Socolich, M. & Ranganathan, R. ( 2000; ). The structural basis for red fluorescence in the tetrameric GFP homolog DsRed. Nature Structural Biology 7, 1133-1138.[CrossRef]
    [Google Scholar]
  88. Wanitchakorn, R., Hafner, G. J., Harding, R. M. & Dale, J. L. ( 2000; ). Functional analysis of proteins encoded by banana bunchy top virus DNA-4 to -6. Journal of General Virology 81, 299-306.
    [Google Scholar]
  89. Zambryski, P. & Crawford, K. ( 2000; ). Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annual Review of Cell and Developmental Biology 16, 393-421.[CrossRef]
    [Google Scholar]
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