Intracellular transport of agrobacterium T-DNA

Agrobacterium: From Biology to Biotechnology

Volumn , Issue , 2008, Pages 365-394

  Lacroix, Benoît ^a   Elbaum, Michael ^b   Citovsky, Vitaly ^a   Tzfira, Tzvi ^c  

^a STONY BROOK UNIVERSITY   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 57849143511     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-72290-0_10     Document Type: Chapter

References (131)

1. Abel S, Theologis A (1994) Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. Plant J 5: 421-427
2. Abu-Arish A, Frenkiel-Krispin D, Fricke T, Tzfira T, Citovsky V, Grayer Wolf S, Elbaum M (2004) Three-dimensional reconstruction of Agrobacterium VirE2 protein with single-stranded DNA. J Biol Chem 279: 25359-25363
3. Afolabi AS, Worland B, Snape JW, Vain P (2004) A large-scale study of rice plants transformed with different T-DNAs provides new insights into locus composition and T-DNA linkage configurations. Theor Appl Genet 109: 815-826
4. Alonso C, Miskin J, Hernaez B, Fernandez-Zapatero P, Soto L, Canto C, Rodri-guez-Crespo I, Dixon L, Escribano JM (2001) African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J Virol 75: 9819-9827
5. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
6. Bakó L, Umeda M, Tiburcio AF, Schell J, Koncz C (2003) The VirD2 pilot protein of Agrobacterium-transferred DNA interacts with the TATA box-binding protein and a nuclear protein kinase in plants. Proc Natl Acad Sci USA 100: 10108-10113
7. Ballas N, Citovsky V (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc Natl Acad Sci USA 94: 10723-10728
8. Briels W (1986) The theory of polymer dynamics. Clarendon Press, Oxford
9. Chilton M-DM, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-strand breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133: 956-965
10. Christie PJ, Ward JE, Winans SC, Nester EW (1988) The Agrobacterium tumefa-ciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J Bacteriol 170: 2659-2667
11. Citovsky V, Guralnick B, Simon MN, Wall JS (1997) The molecular structure of Agrobacterium VirE2-single stranded DNA complexes involved in nuclear import. J Mol Biol 271: 718-727
12. Citovsky V, Kapelnikov A, Oliel S, Zakai N, Rojas MR, Gilbertson RL, Tzfira T, Loyter A (2004) Protein interactions involved in nuclear import of the Agro-bacterium VirE2 protein in vivo and in vitro. J Biol Chem 279: 29528-29533
13. Citovsky V, Warnick D, Zambryski PC (1994) Nuclear import of Agrobacterium VirD2 and VirE2 proteins in maize and tobacco. Proc Natl Acad Sci USA 91: 3210-3214
14. Citovsky V, Wong ML, Zambryski PC (1989) Cooperative interaction of Agro-bacterium VirE2 protein with single stranded DNA: implications for the T-DNA transfer process. Proc Natl Acad Sci USA 86: 1193-1197
15. Citovsky V, Zupan J, Warnick D, Zambryski PC (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256: 1802-1805
16. Dauty E, Verkman AS (2005) Actin cytoskeleton as the principal determinant of size-dependent DNA mobility in cytoplasm: a new barrier for non-viral gene delivery. J Biol Chem 280: 7823-7828
17. Dean DA, Strong DD, Zimmer WE (2005) Nuclear entry of nonviral vectors. Gene Ther 12: 881-890
18. Deng W, Chen L, Peng WT, Liang X, Sekiguchi S, Gordon MP, Comai L, Nester EW (1999) VirE1 is a specific molecular chaperone for the exported single-stranded-DNA-binding protein VirE2 in Agrobacterium. Mol Microbiol 31: 1795-1807
19. Deng W, Chen L, Wood DW, Metcalfe T, Liang X, Gordon MP, Comai L, Nester EW (1998) Agrobacterium VirD2 protein interacts with plant host cyclophil-ins. Proc Natl Acad Sci USA 95: 7040-7045
20. Drouet J, Delteil C, Lefrancois J, Concannon P, Salles B, Calsou P (2005) DNA-dependent protein kinase and XRCC4-DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J Biol Chem 280: 7060-7069
21. Duckely M, Oomen C, Axthelm F, Van Gelder P, Waksman G, Engel A (2005) The VirE1VirE2 complex of Agrobacterium tumefaciens interacts with single-stranded DNA and forms channels. Mol Microbiol 58: 1130-1142
22. Dumas F, Duckely M, Pelczar P, Van Gelder P, Hohn B (2001) An Agrobacte-rium VirE2 channel for transferred-DNA transport into plant cells. Proc Natl Acad Sci USA 98: 485-490
23. Durrenberger F, Crameri A, Hohn B, Koukolikova-Nicola Z (1989) Covalently bound VirD2 protein of Agrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation. Proc Natl Acad Sci USA 86: 9154-9158
24. Fahrenkrog B, Koser J, Aebi U (2004) The nuclear pore complex: a jack of all trades? Trends Biochem Sci 29: 175-182
25. Forbes DJ (1992) Structure and function of the nuclear pore complex. Annu Rev Cell Biol 8: 495-527
26. Frary A, Hamilton CM (2001) Efficiency and stability of high molecular weight DNA transformation: an analysis in tomato. Transgenic Res 10: 121-132
27. Frenkiel-Krispin D, Grayer-Wolf S, Albeck S, Unger T, Peleg Y, Jacobovitch J, Michael Y, Daube S, Sharon M, Robinson CV, Svergun DI, Fass D, Tzfira T, Elbaum M (2006) Plant transformation by Agrobacterium tumefaciens regulation of ssDNA-VirE2 complex assembly by VirE1. 282: 3458-3464
28. Gelvin SB (2003a) Improving plant genetic engineering by manipulating the host. Trends Biotechnol 21: 95-98
29. Gelvin SB (1998) Agrobacterium VirE2 proteins can form a complex with T strands in the plant cytoplasm. J Bacteriol 180: 4300-4302
30. Gelvin SB (2003b) Agrobacterium-mediated plant transformation: the biology behind the "gene-jockeying" tool. Microbiol Mol Biol Rev 67: 16-37
31. Görlich D, Vogel F, Mills AD, Hartmann E, Laskey RA (1995) Distinct functions for the two importin subunits in nuclear protein import. Nature 377: 246-248
32. Greber UF, Fassati A (2003) Nuclear import of viral DNA genomes. Traffic 4: 136-143
33. Greber UF, Way M (2006) A superhighway to virus infection. Cell 124: 741-754
34. Guralnick B, Thomsen G, Citovsky V (1996) Transport of DNA into the nuclei of Xenopus oocytes by a modified VirE2 protein of Agrobacterium. Plant Cell 8: 363-373
35. Hamilton CM, Frary A, Lewis C, Tanksley SD (1996) Stable transfer of intact high molecular weight DNA into plant chromosomes. Proc Natl Acad Sci USA 93: 9975-9979
36. Herrera-Estrella A, Chen Z, Van Montagu M, Wang K (1988) VirD proteins of Agrobacterium tumefaciens are required for the formation of a covalent DNA protein complex at the 5' terminus of T-strand molecules. EMBO J 7: 4055-4062
37. Herrera-Estrella A, Van Montagu M, Wang K (1990) A bacterial peptide acting as a plant nuclear targeting signal: the amino-terminal portion of Agrobacterium VirD2 protein directs a beta-galactosidase fusion protein into tobacco nuclei. Proc Natl Acad Sci USA 87: 9534-9537
38. Hirooka T, Kado CI (1986) Location of the right boundary of the virulence region on Agrobacterium tumefaciens plasmid pTiC58 and a host specifying gene next to the boundary. J Bacteriol 168: 237-243
39. Hodges LD, Cuperus J, Ream W (2004) Agrobacterium rhizogenes GALLS protein substitutes for Agrobacterium tumefaciens single-stranded DNA-binding protein VirE2. J Bacteriol 186: 3065-3077
40. Howard E, Zupan J, Citovsky V, Zambryski PC (1992) The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell 68: 109-118
41. Hubner S, Smith HMS, Hu W, Chan CK, Rihs HP, Paschal BM, Raikhel NV, Jans DA (1999) Plant importin alpha binds nuclear localization sequences with high affinity and can mediate nuclear import independent of importin beta. J Biol Chem 274: 22610-22617
42. Jans DA, Xiao CY, Lam MH (2000) Nuclear targeting signal recognition: a key control point in nuclear transport? BioEssays 22: 532-544
43. Jasper F, Koncz C, Schell J, Steinbiss HH (1994) Agrobacterium T-strand production in vitro: sequence-specific cleavage and 5' protection of single-stranded DNA templates by purified VirD2 protein. Proc Natl Acad Sci USA 91: 694-698
44. Kalogeraki VS, Zhu J, Stryker JL, Winans SC (2000) The right end of the vir region of an octopine-type Ti plasmid contains four new members of the vir regulon that are not essential for pathogenesis. J Bacteriol 182: 1774-1778
45. Kim SR, Lee J, Jun SH, Park S, Kang HG, Kwon S, An G (2003) Transgene structures in T-DNA-inserted rice plants. Plant Mol Biol 52: 761-773
46. King SM (2002) Dyneins motor on in plants. Traffic 3: 930-931
47. Koukolikova-Nicola Z, Raineri D, Stephens K, Ramos C, Tinland B, Nester EW, Hohn B (1993) Genetic analysis of the virD operon of Agrobacterium tumefa-ciens: a search for functions involved in transport of T-DNA into the plant cell nucleus and in T-DNA integration. J Bacteriol 175: 723-731
48. Krichevsky A, Kozlovsky SV, Gafni Y, Citovsky V (2006) Nuclear import and export of plant virus proteins and genomes. Mol Plant Pathol 7: 131-146
49. Kumar S, Fladung M (2002) Transgene integratin in aspen: structures of integration sites and mechanism of T-DNA integration. Plant J 31: 543-551
50. Lacroix B, Li J, Tzfira T, Citovsky V (2006a) Will you let me use your nucleus? How Agrobacterium gets its T-DNA expressed in the host plant cell. Canadian J Physiol Pharmacol 84: 333-345
51. Lacroix B, Tzfira T, Vainstein A, Citovsky V (2006b) A case of promiscuity: Agrobacterium's endless hunt for new partners. Trends Genet 22: 29-37
52. Lacroix B, Vaidya M, Tzfira T, Citovsky V (2005) The VirE3 protein of Agrobac-terium mimics a host cell function required for plant genetic transformation. EMBO J 24: 428-437
53. Landau L, EM L (1980) Stastitical physics. Pergamon Press, Oxford
54. Lasek RJ, Brady ST (1985) Attachment of transported vesicles to microtubules in axoplasm is facilitated by AMP-PNP. Nature 316: 645-647
55. Lawrence CJ, Morris NR, Meagher RB, Dawe RK (2001) Dyneins have run their course in plant lineage. Traffic 2: 362-363
56. Lechardeur D, Lukacs GL (2002) Intracellular barriers to non-viral gene transfer. Curr Gene Ther 2: 183-194
57. Lechardeur D, Sohn KJ, Haardt M, Joshi PB, Monck M, Graham RW, Beatty B, Squire J, O'Brodovich H, Lukacs GL (1999) Metabolic instability of plasmid DNA in the cytosol: a potential barrier to gene transfer. Gene Ther 6: 482-497
58. Leonetti JP, Mechti N, Degols G, Gagnor C, Lebleu B (1991) Intracellular distribution of microinjected antisense oligonucleotides. Proc Natl Acad Sci USA 88: 2702-2706
59. Lessl M, Lanka E (1994) Common mechanisms in bacterial conjugation and Ti-mediated transfer to plant cells. Cell 77: 321-324
60. Li J, Krichevsky A, Vaidya M, Tzfira T, Citovsky V (2005) Uncoupling of the functions of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc Nat Acad Sci USA 102: 5733-5738
61. Loyter A, Rosenbluh J, Zakai N, Li J, Kozlovsky SV, Tzfira T, Citovsky V (2005) The plant VIP1 protein-A molecular link between the Agrobacterium T-complex and the host cell chromatin? Plant Physiol 138: 1318-1321
62. Luby-Phelps K (2000) Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int Rev Cytol 192: 189-221
63. Lukacs GL, Haggie P, Seksek O, Lechardeur D, Freedman N, Verkman AS (2000) Size-dependent DNA mobility in cytoplasm and nucleus. J Biol Chem 275: 1625-1629
64. Mathur J, Koncz C (1998) PEG-mediated protoplast transformation with naked DNA. Methods Mol Biol 82: 267-276
65. Merkle T (2001) Nuclear import and export of proteins in plants: a tool for the regulation of signalling. Planta 213: 499-517
66. Mirzoeva OK, Petrini JH (2001) DNA damage-dependent nuclear dynamics of the Mre11 complex. Mol Cell Biol 21: 281-288
67. Mysore KS, Bassuner B, Deng XB, Darbinian NS, Motchoulski A, Ream LW, Gelvin SB (1998) Role of the Agrobacterium tumefaciens VirD2 protein in T-DNA transfer and integration. Mol Plant-Microbe Interact 11: 668-683
68. Mysore KS, Nam J, Gelvin SB (2000) An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. Proc Natl Acad Sci USA 97: 948-953
69. Nagai H, Roy CR (2003) Show me the substrates: modulation of host cell function by type IV secretion systems. Cell Microbiol 5: 373-383
70. Narasimhulu SB, Deng X-B, Sarria R, Gelvin SB (1996) Early transcription of Agrobacterium T-DNA genes in tobacco and maize. Plant Cell 8: 873-886
71. Otten L, DeGreve H, Leemans J, Hain R, Hooykass P, Schell J (1984) Restoration of virulence of vir region mutants of A. tumefaciens strain B6S3 by coinfec-tion with normal and mutant Agrobacterium strains. Mol Gen Genet 195: 159-163
72. Pante N, Kann M (2002) Nuclear pore complex is able to transport macromole-cules with diameters of about 39 nm. Mol Biol Cell 13: 425-434
73. Phair RD, Misteli T (2000) High mobility of proteins in the mammalian cell nucleus. Nature 404: 604-609
74. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM (2003) Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 81: 123-129
75. Pollard H, Toumaniantz G, Amos JL, Avet-Loiseau H, Guihard G, Behr JP, Escande D (2001) Ca2+-sensitive cytosolic nucleases prevent efficient delivery to the nucleus of injected plasmids. J Gene Med 3: 153-164
76. Puchta H (1998) Repair of genomic double-strand breaks in somatic plant cells by one-sided invasion of homologous sequences. Plant J 13: 77-78
77. Relic B, Andjelkovic M, Rossi L, Nagamine Y, Hohn B (1998) Interaction of the DNA modifying proteins VirD1 and VirD2 of Agrobacterium tumefaciens: analysis by subcellular localization in mammalian cells. Proc Natl Acad Sci USA 95: 9105-9110
78. Rhee Y, Gurel F, Gafni Y, Dingwall C, Citovsky V (2000) A genetic system for detection of protein nuclear import and export. Nat Biotechnol 18: 433-437
79. Romano PG, Horton P, Gray JE (2004) The Arabidopsis cyclophilin gene family. Plant Physiol 134: 1268-1282
80. Rossi L, Hohn B, Tinland B (1993) The VirD2 protein of Agrobacterium tumefa-ciens carries nuclear localization signals important for transfer of T-DNA to plant. Mol Gen Genet 239: 345-353
81. Salman H, Abu-Arish A, Oliel S, Loyter A, Klafter J, Granel R, Elbaum M (2005) Nuclear localization signal peptides induce molecular delivery along micro-tubules. Biophys J 89: 2134-2145
82. Scali M, Vignani R, Moscatelli A, Jellbauer S, Cresti M (2003) Molecular evidence for a cytoplasmic dynein heavy chain from Nicotiana tabacum L. Cell Biol Int 27: 261-262
83. Schrammeijer B, den Dulk-Ras A, Vergunst AC, Jurado Jacome E, Hooykaas PJJ (2003) Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: evidence for transport of a novel effector protein VirE3. Nucleic Acids Res 31: 860-868
84. Sen P, Pazour GJ, Anderson D, Das A (1989) Cooperative binding of Agrobacte-rium tumefaciens VirE2 protein to single-stranded DNA. J Bacteriol 171: 2573-2580
85. Sheng J, Citovsky V (1996) Agrobacterium-plant cell interaction: have virulence proteins-will travel. Plant Cell 8: 1699-1710
86. Shimizu T (1995) Inhibitors of the dynein ATPase and ciliary or flagellar motility. Methods Cell Biol 47: 497-501
87. Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM, Petrini JH, Haber JE, Lichten M (2004) Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr Biol 14: 1703-1711
88. Shurvinton CE, Hodges L, Ream LW (1992) A nuclear localization signal and the C-terminal omega sequence in the Agrobacterium tumefaciens VirD2 en-donuclease are important for tumor formation. Proc Natl Acad Sci USA 89: 11837-11841
89. Smith HMS, Raikhel NV (1998) Nuclear localization signal receptor importin alpha associates with the cytoskeleton. Plant Cell 10: 1791-1799
90. Stachel SE, An G, Flores C, Nester EW (1985) A Tn3 lacZ transposon for the random generation of beta-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. EMBO J 4: 891-898
91. Stahl R, Horvath H, Van Fleet J, Voetz M, von Wettstein D, Wolf N (2002) T-DNA integration into the barley genome from single and double cassette vectors. Proc Natl Acad Sci USA 99: 2146-2151
92. Sundberg C, Meek L, Carrol K, Das A, Ream LW (1996) VirE1 protein mediates export of single-stranded DNA binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J Bacteriol 178: 1207-1212
93. Sundberg CD, Ream LW (1999) The Agrobacterium tumefaciens chaperone-like protein, VirE1, interacts with VirE2 at domains required for single-stranded DNA binding and cooperative interaction. J Bacteriol 181: 6850-6855
94. Suntharalingam M, Wente SR (2003) Peering through the pore. Nuclear pore complex structure, assembly, and function. Dev Cell 4: 775-789
95. Tao Y, Rao PK, Bhattacharjee S, Gelvin SB (2004) Expression of plant protein phosphatase 2C interferes with nuclear import of the Agrobacterium T-complex protein VirD2. Proc Natl Acad Sci USA 101: 5164-5169
96. Taylor NJ, Fauquet CM (2002) Microparticle bombardment as a tool in plant science and agricultural biotechnology. DNA Cell Biol 21: 963-977
97. Tinland B (1996) The integration of T-DNA into plant genomes. Trends Plant Sci 1: 178-184
98. Tzfira T (2006) On tracks and locomotives: the long route of DNA to the nucleus. Trends Microbiol 14: 61-63
99. Tzfira T, Citovsky V (2001) Comparison between nuclear import of nopaline-and octopine-specific VirE2 protein of Agrobacterium in plant and animal cells. Mol Plant Pathol 2: 171-176
100. Tzfira T, Citovsky V (2002) Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol 12: 121-129
101. Tzfira T, Citovsky V (2006) Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 17: 147-154
102. Tzfira T, Frankmen L, Vaidya M, Citovsky V (2003) Site-specific integration of Agrobacterium T-DNA via double-stranded intermediates. Plant Physiol 133: 1011-1023
103. Tzfira T, Lacroix B, Citovsky V (2005) Nuclear Import of Agrobacterium T-DNA. In T Tzfira, V Citovsky, eds, Nuclear Import and Export in Plants and Animals. Eurekah.com and Kluwer Academic/Plenum, pp 83-99
104. Tzfira T, Li J, Lacroix B, Citovsky V (2004a) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20: 375-383
105. Tzfira T, Rhee Y, Chen M-H, Citovsky V (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54: 187-219
106. Tzfira T, Vaidya M, Citovsky V (2001) VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J 20: 3596-3607
107. Tzfira T, Vaidya M, Citovsky V (2002) Increasing plant susceptibility to Agrobac-terium infection by overexpression of the Arabidopsis VIP1 gene. Proc Natl Acad Sci USA 99: 10435-10440
108. Tzfira T, Vaidya M, Citovsky V (2004b) Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431: 87-92
109. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16: 991-1002
110. van Attikum H, Fritsch O, Hohn B, Gasser SM (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119: 777-788
111. Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CMT, Regensburg-Tuink TJ, Hooykaas PJJ (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979-982
112. Vergunst AC, van Lier MCM, den Dulk-Ras A, Hooykaas PJJ (2003) Recognition of the Agrobacterium VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol 133: 978-988
113. Vergunst AC, van Lier MCM, den Dulk-Ras A, Stüve TA, Ouwehand A, Hooykaas PJJ (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Nat Acad Sci USA 102: 832-837
114. Verkman AS (2002) Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem Sci 27: 27-33
115. 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
116. Ward D, Zupan J, Zambryski PC (2002) Agrobacterium VirE2 gets the VIP1 treatment in plant nuclear import. Trends Plant Sci 7: 1-3
117. Ward E, Barnes W (1988) VirD2 protein of Agrobacterium tumefaciens very tightly linked to the 5' end of T-strand DNA. Science 242: 927-930
118. Whittaker GR (2003) Virus nuclear import. Adv Drug Deliv Rev 55: 733-747
119. Whittaker GR, Helenius A (1998) Nuclear import and export of viruses and virus genomes. Virology 246: 1-23
120. Whittaker GR, Kann M, Helenius A (2000) Viral entry into the nucleus. Annu Rev Cell Dev Biol 16: 627-651
121. Winans SC, Allenza P, Stachel SE, McBride KE, Nester EW (1987) Characterization of the virE operon of the Agrobacterium Ti plasmid pTiA6. Nucleic Acids Res 15: 825-837
122. Yi H, Mysore KS, Gelvin SB (2002) Expression of the Arabidopsis histone H2A-1 gene correlates with susceptibility to Agrobacterium transformation. Plant J 32: 285-298
123. Young C, Nester EW (1988) Association of the VirD2 protein with the 5' end of T-strands in Agrobacterium tumefaciens. J Bacteriol 170: 3367-3374
124. Yusibov VM, Steck TR, Gupta V, Gelvin SB (1994) Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc Natl Acad Sci USA 91: 2994-2998
125. Zaidi SK, Young DW, Choi JY, Pratap J, Javed A, Montecino M, Stein JL, Lian JB, van Wijnen AJ, Stein GS (2004) Intranuclear trafficking: organization and assembly of regulatory machinery for combinatorial biological control. J Biol Chem 279: 43363-43366
126. Zaidi SK, Young DW, Choi JY, Pratap J, Javed A, Montecino M, Stein JL, van Wijnen AJ, Lian JB, Stein GS (2005) The dynamic organization of gene-regulatory machinery in nuclear microenvironments. EMBO Rep 6: 128-133
127. Zhu Y, Nam J, Humara JM, Mysore K, Lee LY, Cao H, Valentine L, Li J, Kaiser A, Kopecky A, Hwang HH, Bhattacharjee S, Rao P, Tzfira T, Rajagopal J, Yi HC, Yadav VBS, Crane Y, Lin K, Larcher Y, Gelvin M, Knue M, Zhao X, Davis S, Kim SI, Kumar CTR, Choi YJ, Hallan V, Chattopadhyay S, Sui X, Ziemienowitz A, Matthysse AG, Citovsky V, Hohn B, Gelvin SB (2003) Identification of Arabidopsis rat mutants. Plant Physiol 132: 494-505
128. Ziemienowicz A, Görlich D, Lanka E, Hohn B, Rossi L (1999) Import of DNA into mammalian nuclei by proteins originating from a plant pathogenic bacterium. Proc Natl Acad Sci USA 96: 3729-3733
129. Ziemienowicz A, Merkle T, Schoumacher F, Hohn B, Rossi L (2001) Import of Agrobacterium T-DNA into plant nuclei: two distinct functions of VirD2 and VirE2 proteins. Plant Cell 13: 369-384
130. Zupan J, Citovsky V, Zambryski PC (1996) Agrobacterium VirE2 protein mediates nuclear uptake of ssDNA in plant cells. Proc Natl Acad Sci USA 93: 2392-2397
131. Zupan J, Muth TR, Draper O, Zambryski PC (2000) The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J 23: 11-28