Tracking the green invaders: Advances in imaging virus infection in plants

Biochemical Journal

Volumn 430, Issue 1, 2010, Pages 21-37

  Tilsner, Jens ^a   Oparka, Karl J ^b  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Correlative microscopy; Fluorescent protein; In vivo interaction; Membrane topology; RNA imaging; Super resolution

Indexed keywords

CORRELATIVE MICROSCOPY; FLUORESCENT PROTEIN; IN VIVO INTERACTION; MEMBRANE TOPOLOGY; SUPER RESOLUTION;

FLUORESCENCE; FLUORESCENCE MICROSCOPY; OPTICAL RESOLVING POWER; PROTEINS; RNA; TOPOLOGY;

VIRUSES;

HYBRID PROTEIN; VIRUS PROTEIN; VIRUS RNA; PHOTOPROTEIN;

ATOMIC FORCE MICROSCOPY; BIMOLECULAR FLUORESCENCE COMPLEMENTATION; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; FLUORESCENCE; FLUORESCENCE LOSS IN PHOTOBLEACHING; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUOROMETRY; GENE EXPRESSION; IMAGE ANALYSIS; IMAGE QUALITY; IMAGING; MEMBRANE STRUCTURE; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; RNA TRANSLATION; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING; VIRUS GENOME; VIRUS INFECTION; CHEMISTRY; GENETICS; METHODOLOGY; MOLECULAR IMAGING; PHYSIOLOGY; PLANT; PROTEIN SYNTHESIS; ULTRASTRUCTURE; VIROLOGY;

LUMINESCENT PROTEINS; MOLECULAR IMAGING; PLANT VIRUSES; PLANTS; PROTEIN BIOSYNTHESIS; PROTEIN INTERACTION MAPPING; RECOMBINANT FUSION PROTEINS; RNA, VIRAL; VIRAL PROTEINS;

EID: 77955498856     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100372     Document Type: Review

References (189)

1. Boevink, P. and Oparka, K. J. (2005) Virus-host interactions during movement processes. Plant Physiol. 138, 1815-1821
2. Nelson, R. S. and Citovsky, V. (2005) Plant viruses. Invaders of cells and pirates of cellular pathways. Plant Physiol. 138, 1809-1814
3. Sanfaçon, H. (2005) Replication of positive-strand RNA viruses in plants: contact points between plant and virus components. Can. J. Bot. 83, 1529-1549
4. Lucas, W. J. (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344, 169-184
5. Miller, S. and Krijnse-Locker, J. (2008) Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6, 363-374
6. González-Melendi, P. and Shaw, P. (2002) 3D gold in situlabelling in the EM. Plant J. 29, 237-243
7. Baulcombe, D. C., Chapman, S. and Santa Cruz, S. (1995) Jellyfish green fluorescent protein as a reporter for virus infections. Plant J. 7, 1045-1053
8. Oparka, K. J., Boevink, P. and Santa Cruz, S. (1996) Studying the movement of plant viruses using green fluorescent protein. Trends Plant Sci. 1, 412-417
9. Hell, S. W. (2009) Microscopy and its focal switch. Nat. Methods 6, 24-32
10. Huang, B., Bates, M. and Zhuang, X. (2009) Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 78, 993-1016
11. Patterson, G. H. (2009) Fluorescence microscopy below the diffraction limit. Semin. Cell Dev. Biol. 20, 886-893
12. McDonald, K L, Morphew, M., Verkade, P. and Müller-Reichert, T. (2006) Recent advances in high pressure freezing: equipment and specimen loading methods. In Electron Microscopy Methods and Protocols (Kuo, J., ed.), pp. 143-173, Humana Press, Totowa
13. Subramaniam, S. (2005) Bridging the imaging gap: visualizing subcellular architecture with electron tomography. Curr. Opin. Microbiol. 8, 316-322
14. Hoenger, A. and McIntosh, J. R. (2009) Probing the macromolecular organization of cells by electron tomography. Curr. Opin. Cell Biol. 21, 89-96
15. Cortese, K., Diaspro, A. and Tacchetti, C. (2009) Advanced correlative light/electron microscopy: current methods and new developments using Tokuyasu cryosections. J. Histochem. Cytochem. 57, 1103-1112
16. Plitzko, J. M., Rigort, A. and Leis, A. (2009) Correlative cryo-light microscopy and cryo-electron tomography: from cellular territories to molecular landscapes. Curr. Opin. Biotechnol. 20, 83-89
17. Shaner, N. C., Steinbach, P. A. and Tsien, R. Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909
18. Shaner, N. C., Patterson, G. H. and Davidson, M. W. (2007) Advances in fluorescent protein technology. J. Cell Sci. 120, 4247-4260
19. Karimi, M., Inze, D. and Depicker, A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195 (Pubitemid 36725938)
20. Curtis, M. D. and Grossniklaus, U. (2003) A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469
21. Karimi, M., De Meyer, B. and Hilson, P. (2005) Modular cloning in plant cells. Trends Plant Sci. 10, 103-105
22. Koroleva, O. A., Tomlinson, M. L., Leader, D., Shaw, P. and Donnan, J. H. (2005) High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J. 41, 162-174
23. Tzfira, T., Tian, G. W., Lacroix, B., Vyas, S., Li, J., Leitner-Dagan, Y., Krichevsky, A., Taylor, T., Vainstein, A. and Citovsky, V. (2005) pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol. Biol. 57, 503-516
24. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K. and Pikaard, C. S. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629
25. Chakrabarty, R., Banerjee, R., Chung, S. M., Farman, M., Citovsky, V., Hogenhout, S. A., Tzfira, T. and Goodin, M. (2007) pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. Mol. Plant Micr. Interact. 20, 740-750
26. Goodin, M. M., Chakrabarty, R., Banerjee, R., Yelton, S. and DeBolt, S. (2007) New gateways to discovery. Plant Physiol. 145, 1100-1109
27. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T. and Kimura, T. (2007) Development of series of Gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41
28. Nakagawa, T., Suzuki, T., Murata, S., Nakamura, S., Hindo, T., Maeo, K., Tabata, R., Kawai, T., Tanaka, K., Niwa, Y. et al. (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095-2100
29. Dubin, M., Bowler, C. and Benvenuto, G. (2008) A modified Gateway cloning strategy for overexpressing tagged proteins in plants. Plant Methods 4, 3
30. Zhong, S., Lin, Z., Fray, R. and Grierson, D. (2008) Improved plant transformation vectors for fluorescent protein tagging. Transgenic Res. 17, 985-989
31. Martin, K., Kopperud, K., Chakrabarty, R., Banerjee, R., Brooks, R. and Goodin, M. M. (2009) Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J. 59, 150-162
32. Nelson, B. K., Cai, X. and Nebenführ, A. (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136 (Pubitemid 47373577)
33. Geldner, N., Dénervaud-Tendon, V., Hyman, D. L., Mayer, U., Stierhof, Y.-D. and Chory, J. (2009) Rapid, recombinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59, 169-178
34. Schaad, M. C., Jensen, P. E. and Carrington, J. C. (1997) Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J. 16, 4049-4059
35. Wei, T. and Wang, A. (2008) Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 82, 12252-12264
36. Wei, T., Huang, T. S., McNeil, J., Laliberte, J. F., Hong, J., Nelson, R. S. and Wang, A. (2010) Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J. Virol. 84, 799-809
37. Kim, S. H., Ryabov, E. V., Kalinina, N. O., Rakitina, D. V., Gillespie, T., MacFarlane, S., Haupt, S., Brown, J. W. and Taliansky, M. (2007) Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO J. 26, 2169-2179
38. Kim, S. H., MacFarlane, S., Kalinina, N. O., Rakitina, D. V., Ryabov, E. V., Gillespie, T., Haupt, S., Brown, J. W. S. and Taliansky, M. (2007) Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc. Natl. Acad. Sci. U.S.A. 104, 11115-11120
39. Dixit, R., Cyr, R. and Gilroy, S. (2006) Using intrinsically fluorescent proteins for plant cell imaging. Plant J. 45, 599-615 (Pubitemid 43373711)
40. Millar, A. H., Carrie, C., Pogson, B. and Whelan, J. (2009) Exploring the function-location nexus: using multiple lines of evidence in defining the subcellular location of plant proteins. Plant Cell 21, 1625-1631
41. Moore, I. and Murphy, A. (2009) Validating the location of fluorescent protein fusions in the endomembrane system. Plant Cell 21, 1632-1636
42. Dreher, T. W. and Miller, W. A. (2006) Translational control in positive strand RNA plant viruses. Virology 344, 185-197
43. Miller, W. A. and White, K. A. (2006) Long-distance RNA-RNA interactions in plant virus gene expression and replication. Annu. Rev. Phytopathol. 44, 447-467
44. Heinlein, M., Epel, B. L., Padgett, H. S. and Beachy, R. N. (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270, 1983-1985
45. Samuels, T. D., Ju, H. J., Ye, C. M., Motes, C. M., Blancaflor, E. B. and Verchot-Lubicz, J. (2007) Subcellular targeting and interactions among the potato virus X TGB proteins. Virology 367, 375-389
46. Lindbo, J. A. (2007) TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 145, 1232-1240
47. Santa Cruz, S., Chapman, S., Roberts, A. G., Roberts, I. M., Prior, D. A. M. and Oparka, K. J. (1996) Assembly and movement of a plant virus carrying a green fluorescent protein overcoat. Proc. Natl. Acad. Sci. U.S.A. 93, 6286-6290
48. Lim, H.-S., Bragg, J. N., Ganesan, U., Lawrence, D. M., Yu, J., Isogai, M., Hammond, J. and Jackson, A. O. (2008) Triple gene block protein interactions involved in movement of barley stripe mosaic virus. J. Virol. 82, 4991-5006
49. Goodin, M. M., Chakrabarty, R., Yelton, S., Martin, K., Clark, A. and Brooks, R. (2007) Membrane and protein dynamics in live plant nuclei infected with Sonchus yellow net virus, a plant-adapted rhabdovirus. J. Gen. Virol. 88, 1810-1820
50. Derrick, P. M., Barker, H. and Oparka, K. J. (1992) Increase in plasmodesmatal permeability during cell-to-cell spread of tobacco rattle virus from individually inoculated cells. Plant Cell 4, 1405-1412
51. 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
52. Campbell, E. M. and Hope, T. J. (2008) Live cell imaging of the HIV-1 life cycle. Trends Microbiol. 16, 580-587
53. Khelifa, M., Massé, D., Blanc, S. and Drucker, M. (2010) Evaluation of the minimal replication time of Cauliflower mosaic virus in different hosts. Virology 396, 238-245
54. 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, 1354-1366
55. Lim, H.-S., Bragg, J. N., Ganesan, U., Ruzin, S., Schichnes, D., Lee, M. Y., Vaira, A. M., Ryu, K. H., Hammond, J. and Jackson, A. O. (2009) Subcellular localization of the barley stripe mosaic virus triple gene block proteins. J. Virol. 83, 9432-9448
56. Sztuba-Solinska, J. and Bujarski, J. J. (2008) Insights into the single-cell reproduction cycle of members of the family Bromoviridae: lessons from the use of protoplast systems. J. Virol. 82, 10330-10340
57. Oparka, K. J., Roberts, A. G., Boevink, P., Cruz, S. S., Roberts, I., Pradel, K. S., Imlau, A., Kotlizky, G., Sauer, N. and Epel, B. (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97, 743-754
58. Mohr, D., Frey, S., Fischer, T., Güttler, T. and Görlich, D. (2009) Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 28, 2541-2553
59. Haseloff, J., Siemering, K. R., Prasher, D. C. and Hodge, S. (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. U.S.A. 94, 2122-2127
60. Rebelo, A. R., Niewiadomski, S., Prosser, S. W., Krell, P. and Meng, B. (2008) Subcellular localization of the triple gene block proteins encoded by a foveavirus infecting grapevines. Virus Res. 138, 57-69
61. Tian, G.-W., Mohanty, A., Chary, S. N., Li, S., Paap, B., Drakakaki, G., Kopec, C. D., Li, J., Ehrhardt, D., Jackson, D. et al. (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 135, 25-38
62. Zamyatnin, Jr, A. A., Solovyev, A. G., Bozhkov, P. V., Valkonen, J. P. T., Morozov, S. Y. and Savenkov, E. I. (2006) Assessment of the integral membrane protein topology in living cells. Plant J. 46, 145-154
63. Chapman, S., Faulkner, C., Kaiserli, E., Garcia-Mata, C., Savenkov, E. I., Roberts, A. G., Oparka, K. J. and Christie, J. M. (2008) The photoreversible fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection. Proc. Natl. Acad. Sci. U.S.A. 105, 20038-20043
64. Chapman, S., Oparka, K. J. and Roberts, A. G. (2005) New tools for in vivo fluorescence tagging. Curr. Opin. Plant Biol. 8, 565-573
65. Marks, K. M. and Nolan, G. P. (2006) Chemical labeling strategies for cell biology. Nat. Methods 3, 591-596
66. Lin, M. Z. and Wang, L. (2008) Selective labeling of proteins with chemical probes in living cells. Physiology 23, 131-141
67. Keppler, A., Gendreizig, S., Gronemeyer, T., Pick, H., Vogel, H. and Johnsson, K. (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21, 86-89
68. Gautier, A., Juillerat, A., Heinis, C., Corrêa, Jr, I. R., Kindermann, M., Beaufils, F. and Johnsson, K. (2008) An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15, 128-136
69. Los, G. V. and Wood, K. (2007) The HaloTag®: a novel technology for cell imaging and protein analysis. Methods Mol. Biol. 356, 195-208
70. Miller, L. W., Cai, Y., Sheetz, M. P. and Cornish, V. W. (2005) In vivo protein labeling with trimethoprim conjugates: a flexible chemical tag. Nat. Methods 2, 255-257
71. Lang, C., Schulze, J., Mendel, R. R. and Hansch, R. (2006) HaloTag®: a new versatile reporter gene system in plant cells. J. Exp. Bot. 57, 2985-2992
72. Marks, K. M., Braun, P. D. and Nolan, G. P. (2004) A general approach for chemical labeling and rapid, spatially controlled protein inactivation. Proc. Natl. Acad. Sci. U.S.A. 101, 9982-9987
73. Robers, M., Pinson, P., Leong, L., Batchelor, B. H., Gee, K. R. and Machleidt, T. (2009) Fluorescent labeling of proteins in living cells using the FKBP12 (F36V) tag. Cytometry A 75, 207-224
74. Marks, K. M., Rosinov, M. and Nolan, G. P. (2004) In vivo targeting of organic calcium sensors via genetically selected peptides. Chem. Biotechnol. 11, 347-356
75. Griffin, B. A., Adams, S. R. and Tsien, R. Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272
76. Griffin, B. A., Adams, S. R., Jones, J. and Tsien, R. Y. (2000) Fluorescent labeling of recombinant proteins in living cells with FlAsH. Methods Enzymol. 327, 565-578
77. Martin, B. R., Giepmans, B. N. G., Adams, S. R. and Tsien, R. Y. (2005) Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity. Nat. Biotechnol. 23, 1308-1314
78. Adams, S. R., Campbell, R. E., Gross, L. A., Martin, B. R., Walkup, G. K., Yao, Y., Llopis, J. and Tsien, R. Y. (2002) New biarsenical ligands and tetracysteine motifs for protein labeling in vitroand in vivo: synthesis and biological applications. J. Am. Chem. Soc. 124, 6063-6076
79. Estevez, J. M. and Somerville, C. (2006) FlAsH-based live-cell fluorescent imaging of synthetic peptides expressed in Arabidopsis and tobacco. Biotechniques 41, 569-574
80. Stroffekova, K., Proenza, C. and Beam, K. (2001) The protein-labeling reagent FLASH-EDT2 binds not only to CCXXCC motifs but also non-specifically to endogenous cysteine-rich proteins. Pflügers Arch. Eur. J. Physiol. 442, 859-866
81. Lippincott-Schwartz, J., Altan-Bonnet, N. and Patterson, G. H. (2003) Photobleaching and photoactivation: following protein dynamics in living cells. Nat. Cell Biol. 5, S7-S14
82. Presley, J F. (2006) Measurement of protein motion by photobleaching. In Cell Imaging (Stephens, D., ed.), pp. 119-142, Scion, Bloxham
83. Wright, K. M., Wood, N. T., Roberts, A. G., Chapman, S., Boevink, P., MacKenzie, K. M. and Oparka, K. J. (2007) Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8, 21-31 (Pubitemid 44921880)
84. Karpova, O. V., Zayakina, O. V., Arkhipenko, M. V., Sheval, E. V., Kiselyova, O. I., Poljakov, V. Y., Yaminsky, I. V., Rodionova, N. P. and Atabekov, J. G. (2006) Potato virus X RNA-mediated assembly of single-tailed ternary 'coat protein-RNA-movement protein' complexes. J. Gen. Virol. 87, 2731-2740
85. Lukyanov, K. A., Chudakov, D. M., Lukyanov, S. and Verkhusha, V. V. (2005) Photoactivatable fluorescent proteins. Nat. Rev. Mol. Cell Biol. 6, 885-890
86. Lippincott-Schwartz, J. and Patterson, G. H. (2009) Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol. 19, 555-565
87. Kremers, G.-J., Hazelwood, K. L., Murphy, C. S., Davidson, M. W. and Piston, D. W. (2009) Photoconversion in orange and red fluorescent proteins. Nat. Methods 6, 355-358
88. Valentin, G., Verheggen, C., Piolot, T., Neel, H., Coppey-Moisan, M. and Bertrand, E. (2005) Photoconversion of YFP into a CFP-like species during acceptor photobleaching FRET experiments. Nat. Methods 2, 801 (Pubitemid 41741520)
89. Raab-Graham, K. F., Haddick, P. C. G., Jan, Y. N. and Jan, L. Y. (2006) Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314, 144-148
90. Gretton, S. N., Taylor, A. I. and McLauchlan, J. (2005) Mobility of the hepatitis C virus NS4B protein on the endoplasmic reticulum membrane and membrane-associated foci. J. Gen. Virol. 86, 1415-1421
91. Jones, D. M., Gretton, S. N., McLauchlan, J. and Targett-Adams, P. (2007) Mobility analysis of an NS5A-GFP fusion protein in cells actively replicating hepatitis C virus subgenomic RNA. J. Gen. Virol. 88, 470-475
92. Rodriguez, A. J., Shenoy, S. M., Singer, R. H. and Condeelis, J. (2006) Visualization of mRNA translation in living cells. J. Cell Biol. 175, 67-76 (Pubitemid 44537199)
93. Lin, M. Z., Glenn, J. S. and Tsien, R. Y. (2008) A drug-controllable tag for visualizing newly synthesized proteins in cells and whole animals. Proc. Natl. Acad. Sci. U.S.A. 105, 7744-7749
94. Lalonde, S., Ehrhardt, D. W., Loqué, D., Chen, J., Rhee, S. Y. and Frommer, W. B. (2008) Molecular and cellular approaches for the detection of protein-protein interactions: latest techniques and current limitations. Plant J. 53, 610-635
95. Shyu, Y. J. and Hu, C.-D. (2008) Fluorescence complementation: an emerging tool for biological research. Trends Biotechnol. 26, 622-630
96. Weinthal, D. and Tzfira, T. (2009) Imaging protein-protein interactions in plant cells by bimolecular fluorescence complementation assay. Trends Plant Sci. 14, 59-63
97. Bracha-Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S. and Ohad, N. (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40, 419-427
98. Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C. et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438
99. Citovsky, V., Lee, L. Y., Vyas, S., Glick, E., Chen, M. H., Vainstein, A., Gafni, Y., Gelvin, S. B. and Tzfira, T. (2006) Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 362, 1120-1131
100. Lee, L.-Y., Fang, M. J., Kuang, L.-Y. and Gelvin, S. (2008) Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods 4, 24
101. Waadt, R., Schmidt, L. K., Lohse, M., Hashimoto, K., Bock, R. and Kudla, J. (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505-516
102. Gehl, C., Waadt, R., Kudla, J., Mendel, R. R. and Hänsch, R. (2009) New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Mol. Plant 2, 1051-1058
103. Hu, C.-D. and Kerppola, T. K. (2003) Simultaneous visualization of multiple protein interactions in living cells using multicolour fluorescence complementation analysis. Nat. Biotechnol. 21, 539-545
104. Li, M., Doll, J., Weckermann, K., Oecking, C., Berendzen, K. W. and Schöffl, F. (2010) Detection of in vivo interactions between Arabidopsis class A-HSFs, using a novel BiFC fragment, and identification of novel class B-HSF interacting proteins. Eur. J. Cell Biol. 89, 126-132
105. Tilsner, J., Linnik, O., Christensen, N. M., Bell, K., Roberts, I. M., Lacomme, C. and Oparka, K. J. (2009) Live-cell imaging of viral RNA genomes using a pumilio-based reporter. Plant J. 57, 758-770
106. Piston, D. W. and Kremers, G. J. (2007) Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem. Sci. 32, 407-414
107. Lorenz, M. (2009) Visualizing protein-RNA interactions inside cells by fluorescence resonance energy transfer. RNA 15, 97-103
108. Sakon, J. J. and Weninger, K. R. (2010) Detecting the conformation of individual proteins in live cells. Nat. Methods 7, 203-205
109. Suhling, K. (2006) Fluorescence lifetime imaging. In Cell Imaging (Stephens, D., ed.), pp. 219-245, Scion, Bloxham
110. Padilla-Parra, S., Audugé, N., Coppey-Moisan, M. and Tramier, M. (2008) Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells. Biophys. J. 95, 2976-2988
111. Padilla-Parra, S., Audugé, N., Lalucque, H., Mevel, J. C., Coppey-Moisan, M. and Tramier, M. (2009) Quantitative comparison of different fluorescent protein couples for fast FRET-FLIM acquisition. Biophys. J. 97, 2368-2376
112. Verrier, S. E. and Soling, H. D. (2006) Photobleaching of YFP does not produce a CFP-like species that affects FRET measurements. Nat. Methods 3, 491-492
113. Tramier, M., Gautier, I., Piolot, T., Ravalet, S., Kemnitz, K., Coppey, J., Durieux, C., Mignotte, V. and Coppey-Moisan, M. (2002) Picosecond-hetero- FRET microscopy to probe protein-protein interactions in live cells. Biophys. J. 83, 3570-3577 (Pubitemid 36041974)
114. Goedhart, J., van Weeren, L., Hink, M. A., Vischer, N. O. E., Jalink, K. and Gadella, Jr, T. W. J. (2010) Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat. Methods 7, 137-139
115. Shcherbo, D., Souslova, E., Goedhart, J., Chepurnykh, T., Gaintzeva, A., Shemiakina, I., Gadella, T., Lukyanov, S. and Chudakov, D. (2009) Practical and reliable FRET/FLIM pair of fluorescent proteins. BMC Biotechnol. 9, 24
116. Ganesan, S., Arneer-beg, S. M., Ng, T. T. C., Vojnovic, B. and Wouters, F. S. (2006) A dark yellow fluorescent protein (YFP)-based resonance energy-accepting chromoprotein (REACh) for Förster resonance energy transfer with GFP. Proc. Natl. Acad. Sci. U.S.A. 103, 4089-4094
117. Kwaaitaal, M., Keinath, N. F., Pajonk, S., Biskup, C. and Panstruga, R. (2010) Combined bimolecular fluorescence complementation and Förster resonance energy transfer reveals ternary SNARE complex formation in living plant cells. Plant Physiol. 152, 1135-1147
118. Li, N., Cui, Z.-Q., Wen, J.-K., Zhang, Z.-P., Wei, H.-P., Zhou, Y.-F. and Zhang, X.-E. (2008) Live cell imaging of protein interactions in poliovirus RNA replication complex using fluorescence resonance energy transfer (FRET). Biochem. Biophys. Res. Commun. 368, 489-494
119. Nickerson, J. A. (2009) The biochemistry of RNA metabolism studied in situ. RNA Biol. 6, 25-30
120. Voss, D., Pfefferle, S., Drosten, C., Stevermann, L., Traggiai, E., Lanzavecchia, A. and Becker, S. (2009) Studies on membrane topology, N-glycosylation and functionality of SARS-CoV membrane protein. Virol. J. 6, 79
121. Brach, T., Soyk, S., Müller, C., Hinz, G., Hell, R., Brandizzi, F. and Meyer, A. J. (2009) Non-invasive topology analysis of membrane proteins in the secretory pathway. Plant J. 57, 534-541
122. Hanson, G. T., Aggeler, R., Oglesbee, D., Cannon, M., Capaldi, R. A., Tsien, R. Y. and Remington, S. J. (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13044-13053
123. Dunoyer, P., Ritzenthaler, C., Hemmer, O., Michler, P. and Fritsch, C. (2002) Intracellular localization of the peanut clump virus replication complex in tobacco BY-2 protoplasts containing green fluorescent protein-labeled endoplasmic reticulum or Golgi apparatus. J. Virol. 76, 865-874
124. Ritzenthaler, C., Laporte, C., Gaire, F., Dunoyer, P., Schmitt, C., Duval, S., Piéquet, A., Loudes, A. M., Rohfritsch, O., Stussi-Garaud, C. and Pfeiffer, P. (2002) Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76, 8808-8819
125. Tyagi, S. (2009) Imaging intracellular RNA distribution and dynamics in living cells. Nat. Methods 6, 331-338
126. Christensen, N. M., Oparka, K. J. and Tilsner, J. (2010) Advances in imaging RNA in plants. Trends Plant Sci. 15, 196-203
127. Bertrand, E., Chartrand, P., Schaefer, M., Shenoy, S. M., Singer, R. H. and Long, R. M. (1998) Localization of ASH1mRNA particles in living yeast. Mol. Cell 2, 437-445
128. N-GFP: an RNA reporter system for live-cell imaging. Nat. Methods 4, 633-636
129. Lange, S., Katayama, Y., Schmid, M., Burkacky, O., Bräuchle, C., Lamb, D. C. and Jansen, R.-P. (2008) Simultaneous transport of different localized mRNA species revealed by live-cell imaging. Traffic 9, 1256-1267 (Pubitemid 352034202)
130. Zhang, F. and Simon, A. E. (2003) A novel procedure for the localization of viral RNAs in protoplasts and whole plants. Plant J. 35, 665-673
131. Sambade, A., Brandner, K., Hofmann, C., Seemanpillai, M., Mutterer, J. and Heinlein, M. (2008) Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9, 2073-2088
132. Ozawa, T., Natori, Y., Sato, M. and Umezawa, Y. (2007) Imaging dynamics of endogenous mitochondrial RNA in single living cells. Nat. Methods 4, 413-419
133. Cheong, C.-G. and Hall, T. M. T. (2006) Engineering RNA sequence specificity of Pumilio repeats. Proc. Natl. Acad. Sci. U.S.A. 103, 13635-13639
134. Lu, G., Dolgner, S. J. and Hall, T. M. T. (2009) Understanding and engineering RNA sequence specificity of PUF proteins. Curr. Opin. Struct. Biol. 19, 110-115
135. Christensen, N. M., Tilsner, J., Bell, K., Hammann, P., Parton, R., Lacomme, C. and Oparka, K. J. (2009) The 5′ cap of tobacco mosaic virus (TMV) is required for virion attachment to the actin/endoplasmic reticulum network during early infection. Traffic 10, 536-551
136. Kim, S. and Coulombe, P. A. (2010) Emerging role for the cytoskeleton as an organizer and regulator of translation. Nat. Rev. Mol. Cell Biol. 11, 75-81
137. Brandenburg, B., Lee, L. Y., Lakadamyali, M., Rust, M. J., Zhuang, X. and Hogle, J. M. (2007) Imaging poliovirus entry in live cells. PLoS Biol. 5, e183
138. Li, Y., Zhou, X. and Ye, D. (2008) Molecular beacons: an optimal multifunctional biological probe. Biochem. Biophys. Res. Commun. 373, 457-461
139. Tyagi, S. and Kramer, F. R. (1996) Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 14, 303-308
140. Bernacchi, S. and Mély, Y. (2001) Exciton interaction in molecular beacons: a sensitive sensor for short range modifications of the nucleic acid structure. Nucleic Acids Res. 29, e62
141. Reichelt, M., Brady, J. and Arvin, A. M. (2009) The replication cycle of varicella-zoster virus: analysis of the kinetics of viral protein expression, genome synthesis, and virion assembly at the single-cell level. J. Virol. 83, 3904-3918
142. Brandenburg, B. and Zhuang, X. W. (2007) Virus trafficking: learning from single-virus tracking. Nat. Rev. Microbiol. 5, 197-208
143. Melikyan, G. B., Barnard, R. J. O., Abrahamyan, L. G., Mothes, W. and Young, J. A. T. (2005) Imaging individual retroviral fusion events: from hemifusion to pore formation and growth. Proc. Natl. Acad. Sci. U.S.A. 102, 8728-8733
144. Jouvenet, N., Simon, S. M. and Bieniasz, P. D. (2009) Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc. Natl. Acad. Sci. U.S.A. 106, 19114-19119
145. Hübner, W., McNerney, G. P., Chen, P., Dale, B. M., Gordon, R. E., Chuang, F. Y. S., Li, X. D., Asmuth, D. M., Huser, T. and Chen, B. K. (2009) Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323, 1743-1747
146. Cotton, S., Grangeon, R., Thivierge, K., Mathieu, I., Ide, C., Wei, T., Wang, A. and Laliberté, J. F. (2009) Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 83, 10460-10471
147. Zamyatnin, Jr, A. A., Solovyev, A. G., Savenkov, E. I., Germundsson, A., Sandgren, M., Valkonen, J. P. T. and Morozov, S. Y. (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
148. Lough, T. J., Shash, K., Xoconostle-Cázares, B., Hofstra, K. R., Beck, D. L., Balmori, E., Forster, R. L. S. and Lucas, W. J. (1998) Molecular dissection of the mechanism by which potexvirus triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol. Plant Microbe Interact. 11, 801-814
149. Liu, D. Y., Kuhlmey, B. T., Smith, P. M., Day, D. A., Faulkner, C. R. and Overall, R. L. (2008) Reflection across plant cell boundaries in confocal laser scanning microscopy. J. Microsc. 231, 349-357
150. Donohoe, B. S., Mogelsvang, S. and Staehelin, L. A. (2006) Electron tomography of ER, Golgi and related membrane systems. Methods 39, 154-162
151. Bartesaghi, A. and Subramaniam, S. (2009) Membrane protein structure determination using cryo-electron tomography and 3D image averaging. Curr. Opin. Struct. Biol. 19, 402-407
152. Kopek, B. G., Perkins, G., Miller, D. J., Ellisman, M. H. and Ahlquist, P. (2007) Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5, e220
153. Knoops, K., Kikkert, M., Worm, S. H. E., Zevenhoven-Dobbe, J. C., van der Meer, Y., Koster, A. J., Mommaas, A. M. and Snijder, E. J. (2008) SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 6, e226
154. Spagnolo, J. F., Rossignol, E., Bullitt, E. and Kirkegaard, K. (2010) Enzymatic and nonenzymatic functions of viral RNA-dependent RNA polymerases within oligomeric arrays. RNA 16, 382-393
155. Sougrat, R., Bartesaghi, A., Lifson, J. D., Bennett, A. E., Bess, J. W., Zabransky, D. J. and Subramaniam, S. (2007) Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog. 3, e63
156. Maurer, U. E., Sodeik, B. and Grünewald, K. (2008) Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc. Natl. Acad. Sci. U.S.A. 105, 10559-10564
157. Schelhaas, M., Malmström, J., Pelkmans, L., Haugstetter, J., Ellgaard, L., Grünewald, K. and Helenius, A. (2007) Simian virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131, 516-529 (Pubitemid 350017762)
158. Chlanda, P., Carbajal, M. A., Cyrklaff, M., Griffiths, G. and Krijnse-Locker, J. (2009) Membrane rupture generates single open membrane sheets during vaccinia virus assembly. Cell Host Microbe 6, 81-90
159. Carlson, L. A., Briggs, J. A. G., Glass, B., Riches, J. D., Simon, M. N., Johnson, M. C., Müller, B., Grünewald, K. and Kräusslich, H. G. (2008) Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis. Cell Host Microbe 4, 592-599
160. Subramaniam, S., Bartesaghi, A., Liu, J., Bennett, A. E. and Sougrat, R. (2007) Electron tomography of viruses. Curr. Opin. Struct. Biol. 17, 596-602
161. Bennett, A. E., Narayan, K., Shi, D., Hartnell, L. M., Gousset, K., He, H., Lowekamp, B. C., Yoo, T. S., Bliss, D., Freed, E. O. and Subramaniam, S. (2009) Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLoS Pathog. 5, e1000591
162. Seguí-Simarro, J. M., Austin, II, J. R., White, E. A. and Staehelin, L. A. (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16, 836-856
163. Staehelin, L. A. and Kang, B.-H. (2008) Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol. 147, 1454-1468
164. Katayama, S., Wei, T., Omura, T., Takagi, J. and Iwasaki, K. (2007) Three-dimensional architecture of virus-packed tubule. J. Electron Microsc. (Tokyo) 56, 77-81
165. Wei, T., Uehara-Ichiki, T., Miyazaki, N., Hibino, H., Iwasaki, K. and Omura, T. (2009) Association of rice gall dwarf virus with microtubules is necessary for viral release from cultured insect vector cells. J. Virol. 83, 10830-10835
166. Medalia, O., Weber, I., Frangakis, A. S., Nicastro, D., Gerisch, G. and Baumeister, W. (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298, 1209-1213
167. Beck, M., Malmström, J. A., Lange, V., Schmidt, A., Deutsch, E. W. and Aebersold, R. (2009) Visual proteomics of the human pathogen Leptospira interrogans. Nat. Methods 6, 817-823
168. Snijder, E. J., van der Meer, Y., Zevenhoven-Dobbe, J., Onderwater, J. J. M., van der Meulen, J., Koerten, H. K. and Mommaas, A. M. (2006) Ultrastructure
169. van Donselaar, E., Posthuma, G., Zeuschner, D., Humbel, B. M. and Slot, J. W. (2007) Immunogold labeling of cryosections from high-pressure frozen cells. Traffic 8, 471-485
170. Huang, B. (2010) Super-resolution optical microscopy: multiple choices. Curr. Opin. Chem. Biol. 14, 10-14
171. Willig, K. I., Kellner, R. R., Medda, R., Hein, B., Jakobs, S. and Hell, S. W. (2006) Nanoscale resolution in GFP-based microscopy. Nat. Methods 3, 721-723
172. Schermelleh, L., Carlton, P. M., Haase, S., Shao, L., Winoto, L., Kner, P., Burke, B., Cardoso, M. C., Agard, D. A., Gustafsson, M. G. L. et al. (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332-1336
173. Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S., Bonifacino, J. S., Davidson, M. W., Lippincott-Schwartz, J. and Hess, H. F. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645
174. Patterson, G., Davidson, M., Manley, S. and Lippincott-Schwartz, J. (2010) Superresolution imaging using single-molecule localization. Annu. Rev. Phys. Chem. 61, 345-367
175. Flors, C., Hotta, J., Uji-i, H., Dedecker, P., Ando, R., Mizuno, H., Miyawaki, A. and Hofkens, J. (2007) A stroboscopic approach for fast photoactivation-localization microscopy with dronpa mutants. J. Am. Chem. Soc. 129, 13970-13977
176. Drepper, T., Eggert, T., Circolone, F., Heck, A., Krauss, U., Guterl, J.-K., Wendorff, M., Losi, A., Gärtner, W. and Jaeger, K.-E. (2007) Reporter proteins for in vivo fluorescence without oxygen. Nat. Biotechnol. 25, 443-445
177. Meisslitzer-Ruppitsch, C., Röhrl, C., Neumüller, J., Pavelka, M. and Ellinger, A. (2009) Photooxidation technology for correlated light and electron microscopy. J. Microsc. 235, 322-335
178. Meisslitzer-Ruppitsch, C., Vetterlein, M., Stangl, H., Maier, S., Neumüller, J., Freissmuth, M., Pavelka, M. and Ellinger, A. (2008) Electron microscopic visualization of fluorescent signals in cellular compartments and organelles by means of DAB-photoconversion. Histochem. Cell Biol. 130, 407-419
179. Grabenbauer, M., Geerts, W. J. C., Fernadez-Rodriguez, J., Hoenger, A., Koster, A. J. and Nilsson, T. (2005) Correlative microscopy and electron tomography of GFP through photooxidation. Nat. Methods 2, 857-862 (Pubitemid 41741537)
180. Gaietta, G., Deerinck, T. J., Adams, S. R., Bouwer, J., Tour, O., Laird, D. W., Sosinsky, G. E., Tsein, R. Y. and Ellisman, M. H. (2002) Multicolor and electron microscopic imaging of connexin trafficking. Science 296, 503-507
181. Nisman, R., Dellaire, G., Ren, Y., Li, R. and Bazett-Jones, D. P. (2004) Application of quantum dots as probes for correlative fluorescence, conventional, and energy-filtered transmission electron microscopy. J. Histochem. Cytochem. 52, 13-18
182. Gross, L., Mohn, F., Moll, N., Liljeroth, P. and Meyer, G. (2009) The chemical structure of a molecule resolved by atomic force microscopy. Science 325, 1110-1114
183. Torrance, L., Andreev, I. A., Gabrenaite-Verhovskaya, R., Cowan, G., Mäkinen, K. and Taliansky, M. E. (2006) An unusual structure at one end of potato potyvirus particles. J. Mol. Biol. 357, 1-8
184. Atabekov, J. G., Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V. and Poljakov, V. Y. (2000) The movement protein-triggered in situconversion of potato virus X virion RNA from a nontranslatable into a translatable form. Virology 271, 259-263
185. Peremyslov, V. V., Andreev, I. A., Prokhnevsky, A. I., Duncan, G. H., Taliansky, M. E. and Dolja, V. V. (2004) Complex molecular architecture of beet yellows virus particles. Proc. Natl. Acad. Sci. U.S.A. 101, 5030-5035
186. Gabrenaite-Verkhovskaya, R., Andreev, I. A., Kalinina, N. O., Torrance, L., Taliansky, M. E. and Mäkinen, K. (2008) Cylindrical inclusion protein of potato virus A is associated with a subpopulation of particles isolated from infected plants. J. Gen. Virol. 89, 829-838
187. Taliansky, M., Roberts, I. M., Kalinina, N., Ryabov, E. V., Raj, S. K., Robinson, D. J. and Oparka, K. J. (2003) An umbraviral protein, involved in long-distance RNA movement, binds viral RNA and forms unique, protective ribonucleoprotein complexes. J. Virol. 77, 3031-3040
188. Canetta, E., Kim, S. H., Kalinina, N. O., Shaw, J., Adya, A. K., Gillespie, T., Brown, J. W. S. and Taliansky, M. (2008) A plant virus movement protein forms ringlike complexes with the major nucleolar protein, fibrillarin, in vitro. J. Mol. Biol. 376, 932-937
189. Ribeiro, D., Borst, J. W., Goldbach, R. and Kormelink, R. (2009) Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology 383, 121-130