Functional domains of Agrobacterium tumefaciens single-stranded DNA- binding protein VirE2

Journal of Bacteriology

Volumn 179, Issue 4, 1997, Pages 1165-1173

  Dombek, Priscilla ^a,b   Ream, Walt ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; SINGLE STRANDED DNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; COVALENT BOND; DNA BINDING; DNA TRANSFER; ENZYME SYNTHESIS; GENE DELETION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STABILITY; RHIZOBIUM RADIOBACTER;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS);

EID: 0031053291     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.4.1165-1173.1997     Document Type: Article

References (81)

1. Albright, L. M., M. F. Yanofsky, B. Leroux, D. Ma, and E. W. Nester. 1987. Processing of the T-DNA of Agrobacterium tumefaciens generates border nicks and linear, single-stranded T-DNA. J. Bacteriol. 169:1046-1055.
2. Amann, E., B. Ochs, and K. J. Abel. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69:301-315.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology. Wiley, New York, N.Y.
4. Binns, A. N., C. E. Beaupre, and E. M. Dale. 1995. Inhibition of VirB-mediated transfer of diverse substrates from Agrobacterium tumefaciens by the IncQ plasmid RSF1010. J. Bacteriol. 177:4890-4899.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Buchanan-Wollaston, V., J. E. Passiatore, and F. Cannon. 1987. The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328:172-175.
7. Buchanan-Wollaston, V., J. E. Passiatore, and F. Cannon. 1988. The effect of vir mutations on plasmid transfer into plants, p. 281-282. In R. Palachios and D. P. S. Verma (ed.), Molecular genetics of plant-microbe interactions. APS Press, St. Paul. Minn.
8. Chilton, M. D., M. H. Drummond, D. J. Merlo, D. Sciaky, A. L. Montoya, M. P. Gordon, and E. W. Nester. 1977. Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263-271.
9. Chilton, M. D., R. K. Saiki, N. Yadav, M. P. Gordon, and F. Quetier. 1980. T-DNA from Agrobacterium Ti plasmid is in the nuclear DNA fraction of crown gall tumor cells. Proc. Natl. Acad. Sci. USA 77:4060-4064.
10. Christie, P. J., J. E. Ward, S. C. Winans, and E. W. Nester. 1988. The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J. Bacteriol. 170:2659-2667.
11. Citovsky, V., G. De Vos, and P. Zambryski. 1988. Single-stranded DNA binding protein encoded by the virE locus of Agrobacterium tumefaciens. Science 240:501-504.
12. Citovsky, V., D. Warnick, and P. Zambryski. 1994. Nuclear import of Agrobacterium VirD2 and VirE2 proteins in maize and tobacco. Proc. Natl. Acad. Sci. USA 91:3210-3214.
13. Citovsky, V., M. L. Wong, and P. Zambryski. 1989. Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: implications for the T-DNA transfer process. Proc. Natl. Acad. Sci. USA 86:1193-1197.
14. Citovsky, V., J. Zupan, D. Warnick, and P. Zambryski. 1992. Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256:1802-1805.
15. Covacci, A., and R. Rappuoli. 1993. Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol. Microbiol. 8:429-434.
16. Csonka, L. N., and A. J. Clark. 1979. Deletions generated by the transposon Tn10 in the srl recA region of the Escherichia coli K-12 chromosome. Genetics 93:321-343.
17. Das, A. 1988. Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-hinding protein. Proc. Natl. Acad. Sci. USA 85:2909-2913.
18. DeCleene, M., and J. DeLey. 1976. The host range of crown gall. Bot. Rev. 42:389-466.
19. Ditta, G., T. Schmidhauser, E. Yakobson, P. Lu, X. Liang, D. R. Finlay, D. Guiney, and D. R. Helinski. 1985. Plasmids related to the broad-host-range vector, pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 13:149-153.
20. 19a. Dombek, P., and W. Ream. Unpublished data.
21. Durrenberger, F., A. Crameri, B. Hohn, and Z. Koukolikova-Nicola. 1989. Covalently bound VirD2 protein of Agrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation. Proc. Natl. Acad. Sci. USA 86: 9154-9158.
22. Gardner, R. C., and V. C. Knauf. 1986. Transfer of Agrobacterium DNA to plants requires a T-DNA border but not the virE locus. Science 231:725-727.
23. Garfinkel, D. J., and E. W. Nester. 1980. Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J. Bacteriol. 144:732-743.
24. Garfinkel, D. J., R. B. Simpson, L. W. Ream, F. F. While, M. P. Gordon, and E. W. Nester. 1981. Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27:143-153.
25. Gietl, C., Z. Knukolikova-Nicola, and B. Hohn. 1987. Mobilization of TDNA from Agrobacterium to plant cells involves a protein that binds single-stranded DNA. Proc. Natl. Acad. Sci. USA 84:9006-9010.
26. Herrera-Estrella, A., Z. Chen, M. Van Montagu, and K. Wang. 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.
27. Herrera-Estrella, A., M. Van Montagu, and K. Wang. 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.
28. Holsters, M., D. deWaele, A. Depicker, E. Messens, M. Van Montagu, and J. Schell. 1978. Transfection and transformation of Agrobacterium tumefaciens. Mol. Gen. Genet. 163:181-187.
29. Hooykaas, P. J. J., and G. M. Beijersbergen. 1994. The virulence system of Agrobacterium tumefaciens. Annu. Rev. Phytopathol. 32:157-179.
30. Howard, E. A., B. A. Winsor, G. De Vos, and P. Zambryski. 1989. Activation of the T-DNA transfer process in Agrobacterium results in the generation of a T-strand-protein complex: tight association of VirD2 with the 5′ ends of T-strands. Proc. Natl. Acad. Sci. USA 86:4017-4021.
31. Howard, E. A., J. R. Zupan, V. Citovsky, and P. C. Zambryski. 1992. The VirD2 protein of Agrobacterium tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell 68:109-118.
32. Hurley, J. M., S. A. Chervitz, T. C. Jarvis, B. S. Singer, and L. Gold. 1993. Assembly of the bactcriophage T4 replication machine requires the acidic carboxy terminus of gene 32 protein. J. Mol. Biol. 229:398-418.
33. Jayaswal, R. K., K. Veluthambi, S. B. Gelvin, and J. L. Slightom. 1987. Double-stranded cleavage of T-DNA and generation of single-stranded T-DNA molecules in Escherichia coli by a virD-encoded border-specific endonuclease from Agrobacterium tumefaciens. J. Bacteriol. 169:5035-5045.
34. Jorgensen, R. A., S. J. Rothstein, and W. S. Reznikoff. 1979. A restriction enzyme cleavage map of Tn5 and location of a region encoding neomycin resistance. Mol. Gen. Genet. 177:65-72.
35. Krassa, K. B., L. S. Green, and L. Gold. 1991. Protein-protein interactions with the acidic COOH terminus of the single-stranded DNA-binding protein of the bacteriophage T4. Proc. Natl. Acad. Sci. USA 88:4010-4014.
36. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
37. Langley, R. 1970. Practical statistics, p. 160-165. Dover Publications, New York, N.Y.
38. Lessl, M., D. Balzer, W. Pansegrau, and E. Lanka. 1992. Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J. Biol. Chem. 267:20471-204811.
39. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
40. McBride, K. E., and V. C. Knauf. 1988. Genetic analysis of the virE operon of the Agrobacterium Ti plasmid pTiA6. J. Bacteriol. 170:1430-1437.
41. Okamoto, S., A. Toyoda-Yamamoto, K. Ito, I. Takebe, and Y. Machida. 1991. Localization and orientation of the VirD4 protein of Agrobacterium tumefaciens in the cell membrane. Mol. Gen. Genet. 228:24-32.
42. Otten, L., H. DeGreve, J. Leemans, R. Hain, P. J. J. Hooykaas, and J. Schell. 1984. Restoration of virulence of vir region mutants of Agrobacterium tumefaciens strain B653 by coinfection with normal and mutant Agrobacterium strains. Mol. Gen. Genet. 175:159-163.
43. Peralta, E. G., R. Hellmiss, and W. Ream. 1986. overdrive, a T-DNA transmission enhancer on the A. tumefaciens tumour-inducing plasmid. EMBO J. 5:1137-1142.
44. Peralta, E. G., and L. W. Ream. 1985. T-DNA border sequences required for crown gall tumorigenesis. Proc. Natl. Acad. Sci. USA 82:5112-5116.
45. Pohlman, R. F., H. D. Genetti, and S. C. Winans. 1994. Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol. Microbiol. 14:655-668.
46. Pueppke, S. C., and U. K. Benny. 1981. Induction of tumors on Solanum tuberosum L. by Agrobacterium: quantitative analysis, inhibition by carbohydrates, and virulence of selected strains. Physiol. Plant Pathol. 18:169-179.
47. Ream, W. 1989. Agrobacterium tumefaciens and interkingdom genetic exchange. Annu. Rev. Phytopathol. 27:583-618.
48. Robbins, J., S. M. Dilworth, R. A. Laskey, and C. Dingwall. 1991. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64:615-623.
49. Rossi, L., B. Hohn, and B. Tinland. 1996. Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 93:126-130.
50. Ruvkun, G. B., and F. M. Ausubel. 1981. A general method for site-directed mutagenesis in prokaryotes. Nature 289:85-88.
51. Sen, P., G. J. Pazour, D. Anderson, and A. Das. 1989. Cooperative binding of the VirE2 protein to single-stranded DNA. J. Bacteriol. 171:2573-2580.
52. Shaw, C. H., M. Watson, and G. Carter. 1984. The right hand copy of the nopaline Ti plasmid 25 bp repeat is required for tumour formation. Nucleic Acids Res. 12:6031-6041.
53. Shurvinton, C. E., L. Hodges, and W. Ream. 1992. A nuclear localization signal and the C-terminal omega sequence in the Agrobacterium tumefaciens VirD2 endonuclease are important for tumor formation. Proc. Natl. Acad. Sci. USA 89:11837-11841.
54. Shurvinton, C. E., and W. Ream. 1991. Stimulation of Agrobacterium tumefaciens T-DNA transfer by overdrive depends on a flanking sequence but not on helical position with respect to the border repeat. J. Bacteriol. 173:5558-5563.
55. Silver, P. A. 1991. How proteins enter the nucleus. Cell 64:489-497.
56. Stachel, S. E., E. Messens, M. Van Montagu, and P. Zambryski. 1985. Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens. Nature 318:624-629.
57. Stachel, S. E., and E. W. Nester. 1986. The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J. 5:1445-1454.
58. Stachel, S. E., B. Timmerman, and P. Zambryski. 1986. Generation of single-stranded T-DNA molecules during the initial stages of T-DNA transfer from Agrobacterium tumefaciens to plant cells. Nature 322:706-712.
59. Stachel, S. E., B. Timmerman, and P. Zambryski. 1987. Activation of Agrobacterium tumefaciens vir gene expression generates multiple single-stranded T-strand molecules from the pTiA6 T-region: requirement of 5′ virD gene products. EMBO J. 6:857-863.
60. Stachel, S. E., and P. Zambryski. 1986. Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation. Cell 47:155-157.
61. Sundberg, C., L. Meek, K. Carroll, A. Das, and W. Ream. 1996. VirE1 protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 178:1207-1212.
62. Tinland, B., Z. Koukolikova-Nicola, M. N. Hall, and B. Hohn. 1992. The T-DNA-linked VirD2 protein contains two distinct functional nuclear localization signals. Proc. Natl. Acad. Sci. USA 89:7442-7446.
63. Tinland, B., F. Schoumacher, V. Gloeckler, A. Bravo-Angel, and B. Hohn. 1995. The Agrobacterium tumefaciens virulence D2 protein is responsible for precise integration of T-DNA into the plant genome. EMBO J. 14:3585-3595.
64. Toro, N., A. Datta, O. A. Carmi, C. Young, R. K. Prusti, and E. W. Nester. 1989. The Agrobacterium tumefadens virC1 gene product binds to overdrive, a T-DNA transfer enhancer. J. Bacteriol. 171:6845-6849.
65. Van Larebeke, N., G. Engler, M. Holsters, S. Van den Elsacker, I. Zaenen, R. A. Schilperoort, and J. Schell. 1974. Large plasmid in Agrobacterium tumefaciens essential for crown gall inducing activity. Nature 252:169-170.
66. Veluthambi, K., W. Ream, and S. B. Gelvin. 1988. Virulence genes, borders, and overdrive generate single-stranded T-DNA molecules from the A6 Ti plasmid of Agrobacterium tumefaciens. J. Bacteriol. 170:1523-1532.
67. Wang, K., L. Herrera-Estrella, M. Van Montagu, and P. Zambryski. 1984. Right 25 bp terminus sequence of the nopaline T-DNA is essential for and determines direction of DNA transfer from Agrobacterium to the plant genome. Cell 38:455-462.
68. Wang, K., S. E. Stachel, B. Timmerman, M. Van Montagu, and P. Zambryski. 1987. Site-specific nick in the T-DNA border sequence as a result of Agrobacterium vir gene expression. Science 235:587-591.
69. Ward, E. R., and W. M. Barnes. 1988. VirD2 protein of Agrobacterium tumefaciens very tightly linked to the 5′ end of T-strand DNA. Science 242:927-930.
70. Ward, J. E., E. M. Dale, and A. N. Binns. 1991. Activity of the Agrobacterium T-DNA transfer machinery is affected by virB gene products. Proc. Natl. Acad. Sci. USA 88:9350-9354.
71. Watson, B., T. C. Currier, M. P. Gordon, M. D. Chilton, and E. W. Nester. 1975. Plasmid required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 123:255-264.
72. Weiss, A. A., F. D. Johnson, and D. L. Burns. 1993. Molecular characterization of an operon required for pertussis toxin secretion. Proc. Natl. Acad. Sci. USA 90:2970-2974.
73. Willmitzer, L., M. Debeuckeleer, M. Lemmers, M. Van Montagu, and J. Schell. 1980. DNA from Ti plasmid present in nucleus and absent from plastids of crown gall plant cells. Nature 287:359-361.
74. Winans, S. C. 1992. Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol. Rev. 56:12-31.
75. Winans, S. C., P. Allenza, S. E. Stachel, K. E. McBride, and E. W. Nester. 1987. Characterization of the virE operon of the Agrobacterium Ti plasmid pTiA6. Nucleic Acids Res. 15:825-838.
76. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
77. Yanofsky, M. F., S. G. Porter, C. Young, L. M. Albright, M. P. Gordon, and E. W. Nester. 1986. The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease. Cell 47:471-477.
78. Young, C., and E. W. Nester. 1988. Association of the VirD2 protein with the 5′ end of T strands in Agrobacterium tumefaciens. J. Bacteriol. 170:3367-3374.
79. Yusibov, V. M., T. R. Steck, V. Gupta, and S. B. Gelvin. 1994. Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc. Natl. Acad. Sci. USA 91:2994-2998.
80. Zambryski, P. C. 1992. Chronicles from the Agrobacterium-plant cell DNA transfer story. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:465-490.
81. Zupan, J. R., V. Citovsky, and P. Zambryski. 1996. Agrobacterium VirE2 protein mediates nuclear uptake of single-stranded DNA in plant cells. Proc. Natl. Acad. Sci. USA 93:2392-2397.