The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain
10.1128/jb.175.6.1723-1734.1993
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Products of the approximately 9.5-kb virB operon are proposed to direct the export of T-DNA/protein complexes across the Agrobacterium tumefaciens envelope en route to plant cells. The presence of conserved nucleoside triphosphate (NTP)-binding domains in VirB4 and VirB11 suggests that one or both proteins couple energy, via NTP hydrolysis, to T-complex transport. To assess the importance of VirB4 for virulence, a nonpolar virB4 null mutation was introduced into the pTiA6NC plasmid of strain A348. The 2.37-kb virB4 coding sequence was deleted precisely by oligonucleotide-directed mutagenesis in vitro. The resulting delta virB4 mutation was exchanged for the wild-type allele by two sequential recombination events with the counterselectable Bacillus subtilis sacB gene. Two derivatives, A348 delta B4.4 and A348 delta B4.5, sustained a nonpolar deletion of the wild-type virB4 allele, as judged by Southern blot hybridization and immunoblot analyses with antibodies specific for VirB4, VirB5, VirB10, and VirB11. Transcription of wild-type virB4 from the lac promoter restored virulence to the nonpolar null mutants on a variety of dicotyledonous species, establishing virB4 as an essential virulence gene. A substitution of glutamine for Lys-439 and a deletion of Gly-438, Lys-439, and Thr-440 within the glycine-rich NTP-binding domain (Gly-Pro-Iso-Gly-Arg-Gly-Lys-Thr) abolished complementation of A348 delta B4.4 or A348 delta B4.5, demonstrating that an intact NTP-binding domain is critical for VirB4 function. Merodiploids expressing both the mutant and wild-type virB4 alleles exhibited lower virulence than A348, suggesting that VirB4, a cytoplasmic membrane protein, may contribute as a homo- or heteromultimer to A. tumefaciens virulence.

Bibliography

Berger, B. R., & Christie, P. J. (1993). The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. Journal of Bacteriology, 175(6), 1723–1734.

Authors 2
  1. B R Berger (first)
  2. P J Christie (additional)
References 84 Referenced 100
  1. Albano , M. , R. Breitling , and D. A. Dubnau . 1989 . Nucleotide sequence and genetic organization of the Bacillus subtilis comG operon . J. Bacteriol. 171 : 5386 - 5404 . (10.1128/JB.171.10.5386-5404.1989) / J. Bacteriol. / Nucleotide sequence and genetic organization of the Bacillus subtilis comG operon by Albano M. (1989)
  2. Albright , L. M. , M. F. Yanofsky , B. Leroux , D. Ma , and E. W. Nester . 1987 . Processing of the T-DNA ofAgrobactenum tumefaciens generates border nicks and linear, single-stranded T-DNA . J. Bacteriol. 169 : 1046 - 1055 . (10.1128/JB.169.3.1046-1055.1987) / J. Bacteriol. / Processing of the T-DNA ofAgrobactenum tumefaciens generates border nicks and linear, single-stranded T-DNA by Albright L. M. (1987)
  3. Bagdasarian , M. M. , E. Amann , R. Lurz , B. Ruckert , and M. Bagdasarian . 1983 . Activity of the hybrid trp-lac (tac) promoter of Escherichia coli in Pseudomonas putida. Construction of broad-host-range, controlled-expression vectors . Gene 26 : 273 - 282 . (10.1016/0378-1119(83)90197-X) / Gene / Activity of the hybrid trp-lac (tac) promoter of Escherichia coli in Pseudomonas putida. Construction of broad-host-range, controlled-expression vectors by Bagdasarian M. M. (1983)
  4. Becker , K. , W. Koster , and V. Braun . 1990 . Iron(III) hydroxamate transport of Eschenchia coli K12: single amino acid replacements at potential ATP-binding sites inactivate the FhuC protein . Mol. Gen. Genet. 223 : 159 - 162 . (10.1007/BF00315810) / Mol. Gen. Genet. / Iron(III) hydroxamate transport of Eschenchia coli K12: single amino acid replacements at potential ATP-binding sites inactivate the FhuC protein by Becker K. (1990)
  5. Bejersbergen , A. , A. D. Dulk-Ras , R. A. Schilperoort , and P. J. J. Hooykaas . 1992 . Conjugative transfer by the virulence system of Agrobacterium tumefaciens . Science 256 : 1324 - 1327 . (10.1126/science.256.5061.1324) / Science / Conjugative transfer by the virulence system of Agrobacterium tumefaciens by Bejersbergen A. (1992)
  6. Binns , A. N. , and M. F. Thomashow . 1988 . Cell biology of Agrobacterium infection and transformation of plants. Annu . Rev. Microbiol. 42 : 575 - 606 . (10.1146/annurev.mi.42.100188.003043) / Rev. Microbiol. / Cell biology of Agrobacterium infection and transformation of plants. Annu by Binns A. N. (1988)
  7. Blomfield , I. C. , V. Vaughn , R. F. Rest , and B. I. Eisenstein . 1991 . Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon . Mol. Microbiol. 5 : 1447 - 1457 . (10.1111/j.1365-2958.1991.tb00791.x) / Mol. Microbiol. / Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon by Blomfield I. C. (1991)
  8. 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 (London) 328 : 172 - 175 . (10.1038/328172a0) / Nature (London) / The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants by Buchanan-Wollaston V. (1987)
  9. Cangelosi , G. A. , E. A. Best , G. Martinetti , and E. W. Nester . 1991 . Genetic analysis of Agrobacterium . Methods Enzymol. 204 : 384 - 397 . (10.1016/0076-6879(91)04020-O) / Methods Enzymol. / Genetic analysis of Agrobacterium by Cangelosi G. A. (1991)
  10. Cangelosi , G. A. , and E. W. Nester . 1990 . Sugars induce the Agrobacteinum virulence genes through a periplasmic binding protein and a transmembrane signal protein . Proc. Natl. Acad. Sci. USA 87 : 6708 - 6712 . (10.1073/pnas.87.17.6708) / Proc. Natl. Acad. Sci. USA / Sugars induce the Agrobacteinum virulence genes through a periplasmic binding protein and a transmembrane signal protein by Cangelosi G. A. (1990)
  11. Chen , C. - Y. , and S. C. Winans . 1991 . Controlled expression of the transcriptional activator gene virG in Agrobacterium tumefaciens by using the Escherichia coli lac promoter . J. Bacteriol. 173 : 1139 - 1144 . (10.1128/JB.173.3.1139-1144.1991) / J. Bacteriol. / Controlled expression of the transcriptional activator gene virG in Agrobacterium tumefaciens by using the Escherichia coli lac promoter by Chen C. (1991)
  12. .Christie P. J. Unpublished data.
  13. Christie , P. J. , J. E. Ward , M. P. Gordon , and E. W. Nester . 1989 . A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity . Proc. Nati. Acad. Sci. USA 86 : 9677 - 9681 . (10.1073/pnas.86.24.9677) / Proc. Nati. Acad. Sci. USA / A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity by Christie P. J. (1989)
  14. Christie P. J. J. E. Ward and E. W. Nester. Unpublished data.
  15. Christie , P. J. , J. E. Ward , S. C. Winans , and E. W. Nester . 1988 . The Agrobactenium tumefaciens virE2 gene product is a single-stranded DNA-binding protein that associates with T-DNA . J. Bacteriol. 170 : 2659 - 2667 . (10.1128/JB.170.6.2659-2667.1988) / J. Bacteriol. / The Agrobactenium tumefaciens virE2 gene product is a single-stranded DNA-binding protein that associates with T-DNA by Christie P. J. (1988)
  16. Citovsky , V. , M. L. Wong , and P. Zambryski . 1989 . Cooperative interaction ofAgrobactenum VirE2 protein with single stranded DNA: implication for the T-DNA transfer process . Proc. Natl. Acad. Sci. USA 86 : 1193 - 1197 . (10.1073/pnas.86.4.1193) / Proc. Natl. Acad. Sci. USA / Cooperative interaction ofAgrobactenum VirE2 protein with single stranded DNA: implication for the T-DNA transfer process by Citovsky V. (1989)
  17. Citovsky , V. , J. Zupan , D. Warnick , and P. Zambryski . 1992 . Nuclear localization of Agrobacterium VirE2 protein in plant cells . Science 256 : 1802 - 1805 . (10.1126/science.1615325) / Science / Nuclear localization of Agrobacterium VirE2 protein in plant cells by Citovsky V. (1992)
  18. Das , A. 1988 . Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein . Proc. Natl. Acad. Sci. USA 85 : 2909 - 2913 . (10.1073/pnas.85.9.2909) / Proc. Natl. Acad. Sci. USA / Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein by Das A. (1988)
  19. Dubnau , D. 1991 . Genetic competence in Bacillus subtilis . Microbiol. Rev. 55 : 395 - 424 . (10.1128/MR.55.3.395-424.1991) / Microbiol. Rev. / Genetic competence in Bacillus subtilis by Dubnau D. (1991)
  20. Durrenberger , F. , A. Crameri , B. Hohn , and Z. Koukolikova-Nicola . 1989 . Covalently bound VirD2 protein ofAgrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation . Proc. Natl. Acad. Sci. USA 86 : 9154 - 9158 . (10.1073/pnas.86.23.9154) / Proc. Natl. Acad. Sci. USA / Covalently bound VirD2 protein ofAgrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation by Durrenberger F. (1989)
  21. Ebina , Y. , E. Araki , M. Taira , F. Shimada , M. Mori , C. S. Craik , K. Siddle , S. B. Pierce , R. A. Roth , and W. J. Rutter . 1987 . Replacement of Iysine residue 1030 in the putative ATPbinding region of the insulin receptor abolishes insulin- and antibody-stimulated glucose uptake and receptor kinase activity . Proc. Natl. Acad. Sci. USA 84 : 704 - 708 . (10.1073/pnas.84.3.704) / Proc. Natl. Acad. Sci. USA / Replacement of Iysine residue 1030 in the putative ATPbinding region of the insulin receptor abolishes insulin- and antibody-stimulated glucose uptake and receptor kinase activity by Ebina Y. (1987)
  22. Engstrom , P. , P. Zambryski , M. Van Montagu , and S. Stachel . 1987 . Characterization ofAgrobacterium tumefaciens virulence proteins induced by the plant factor acetosyringone . J. Mol. Biol. 197 : 635 - 645 . (10.1016/0022-2836(87)90470-0) / J. Mol. Biol. / Characterization ofAgrobacterium tumefaciens virulence proteins induced by the plant factor acetosyringone by Engstrom P. (1987)
  23. Feldherr , C. M. , E. Kallenbach , and N. Schultz . 1984 . Movement of a karyophilic protein through the nuclear pore of oocytes . J. Cell Biol. 99 : 2216 - 2222 . (10.1083/jcb.99.6.2216) / J. Cell Biol. / Movement of a karyophilic protein through the nuclear pore of oocytes by Feldherr C. M. (1984)
  24. Fullner K. J. and E. W. Nester. 1992. The role of VirB4 protein in the virulence of Agrobacterium tumefaciens. Sixth International Symposium on Molecular Plant-Microbe Interactions Program abstract no. 18.
  25. Gay , P. , D. Le Coq , M. Steinmetz , E. Ferrari , and J. A. Hoch . 1983 . Cloning structural gene sacB, which codes for exoenzyme levansucrase of Bacillus subtilis: expression of the gene in Escherichia coli . J. Bacteriol. 153 : 1424 - 1431 . (10.1128/JB.153.3.1424-1431.1983) / J. Bacteriol. / Cloning structural gene sacB, which codes for exoenzyme levansucrase of Bacillus subtilis: expression of the gene in Escherichia coli by Gay P. (1983)
  26. Gelvin , S. B. , and L. L. Habeck . 1990 . vir genes influence conjugal transfer of the Ti plasmid of Agrobacterium tumefaciens . J. Bacteriol. 172 : 1600 - 1608 . (10.1128/JB.172.3.1600-1608.1990) / J. Bacteriol. / vir genes influence conjugal transfer of the Ti plasmid of Agrobacterium tumefaciens by Gelvin S. B. (1990)
  27. Ghai , J. , and A. Das . 1989 . The virD operon of Agrobacterium tumefaciens Ti plasmid encodes a DNA-relaxing enzyme . Proc. Natl. Acad. Sci. USA 86 : 3109 - 3113 . (10.1073/pnas.86.9.3109) / Proc. Natl. Acad. Sci. USA / The virD operon of Agrobacterium tumefaciens Ti plasmid encodes a DNA-relaxing enzyme by Ghai J. (1989)
  28. Haber , L. T. , and G. C. Walker . 1991 . Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities . EMBO J. 10 : 2707 - 2715 . (10.1002/j.1460-2075.1991.tb07815.x) / EMBO J. / Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities by Haber L. T. (1991)
  29. 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 . (10.1002/j.1460-2075.1988.tb03299.x) / EMBO J. / VirD proteins of Agrobacterium tumefaciens are required for the formation of a covalent DNA-protein complex at the 5' terminus of T-strand molecules by Herrera-Estrella A. (1988)
  30. Higgins , C. F. , I. D. Hiles , G. P. C. Salmond , D. R. Gill , J. A. Downie , I. J. Evans , I. B. Holland , L. Gray , S. D. Buckel , A. W. Bell , and M. A. Hermodson . 1986 . A family of related ATPbinding subunits coupled to many distinct biological processes in bacteria . Nature (London) 323 : 448 - 450 . (10.1038/323448a0) / Nature (London) / A family of related ATPbinding subunits coupled to many distinct biological processes in bacteria by Higgins C. F. (1986)
  31. Horsch , R. B. , H. J. Klee , S. Stachel , S. C. Winans , E. W. Nester , S. G. Rogers , and R. T. Fraley . 1986 . Analysis of Agrobacterium tumefaciens virulence mutants in leaf discs . Proc. Natl. Acad. Sci. USA 83 : 2571 - 2575 . (10.1073/pnas.83.8.2571) / Proc. Natl. Acad. Sci. USA / Analysis of Agrobacterium tumefaciens virulence mutants in leaf discs by Horsch R. B. (1986)
  32. 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 . (10.1073/pnas.86.11.4017) / Proc. Natl. Acad. Sci. USA / 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 by Howard E. A. (1989)
  33. Howard , E. A. , J. R. Zupan , V. Citovsky , and P. C. Zambryski . 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 . (10.1016/0092-8674(92)90210-4) / Cell / The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells by Howard E. A. (1992)
  34. Ippen-Ihler , K. A. , and E. G. Minckley , Jr. 1986 . The conjugation system of F, the fertility factor of Escherichia coli. Annu . Rev. Genet. 20 : 593 - 624 . (10.1146/annurev.ge.20.120186.003113) / Rev. Genet. / The conjugation system of F, the fertility factor of Escherichia coli. Annu by Ippen-Ihler K. A. (1986)
  35. 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 . (10.1128/JB.169.11.5035-5045.1987) / J. Bacteriol. / 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 by Jayaswal R. K. (1987)
  36. Jin , S. , R K . Prusti , T. Roitsch , R. G. Ankenbauer , and E. W. Nester . 1990 . Phosphorylation of the VirG protein of Agrobacterium tumefaciens by the autophosphorylated VirA protein: essential role in biological activity of VirG . J. Bacteriol. 172 : 4945 - 4950 . (10.1128/JB.172.9.4945-4950.1990) / J. Bacteriol. / Phosphorylation of the VirG protein of Agrobacterium tumefaciens by the autophosphorylated VirA protein: essential role in biological activity of VirG by Jin S. (1990)
  37. Jin , S. , T. Roitsch , R. G. Ankenbauer , M. P. Gordon , and E. W. Nester . 1990 . The VirA protein is autophosphorylated and is essential for vir gene regulation . J. Bacteriol. 172 : 525 - 530 . (10.1128/JB.172.2.525-530.1990) / J. Bacteriol. / The VirA protein is autophosphorylated and is essential for vir gene regulation by Jin S. (1990)
  38. Jin , S. , T. Roitsch , P. J. Christie , and E. W. Nester . 1990 . The regulatory VirG protein specifically binds to cis-acting regulatory sequence involved in transcriptional activation ofAgrobactenum tumefaciens virulence genes . J. Bacteriol. 172 : 531 - 537 . (10.1128/JB.172.2.531-537.1990) / J. Bacteriol. / The regulatory VirG protein specifically binds to cis-acting regulatory sequence involved in transcriptional activation ofAgrobactenum tumefaciens virulence genes by Jin S. (1990)
  39. Kado , C. I. 1991 . Molecular mechanisms of crown gall tumorigenesis . Crit. Rev. Plant Sci. 10 : 1 - 32 . (10.1080/07352689109382305) / Crit. Rev. Plant Sci. / Molecular mechanisms of crown gall tumorigenesis by Kado C. I. (1991)
  40. Kamoun , S. , E. T. Tola , H. Kanidar , and C. I. Kado . 1992 . Rapid generation of directed and unmarked deletions in Xanthomonas. Mol. Microbiol. 6 : 809 - 816 . (10.1111/j.1365-2958.1992.tb01531.x) / Xanthomonas. Mol. Microbiol. / Rapid generation of directed and unmarked deletions by Kamoun S. (1992)
  41. Kaniga , K. , I. Delor , and G. R. Cornelis . 1991 . A wide-host range suicide vector for improving reverse genetics in Gramnegative bacteria: inactivation of the blaA gene of Yersinia enterocolitica . Gene 109 : 137 - 141 . (10.1016/0378-1119(91)90599-7) / Gene / A wide-host range suicide vector for improving reverse genetics in Gramnegative bacteria: inactivation of the blaA gene of Yersinia enterocolitica by Kaniga K. (1991)
  42. Kuldau , G. A. , G. De Vos , J. Owen , G. McCaffrey , and P. Zambryski . 1990 . The virB operon of Agrobactenium tumefaciens pTiC58 encodes 11 open reading frames . Mol. Gen. Genet. 221 : 256 - 266 . (10.1007/BF00261729) / Mol. Gen. Genet. / The virB operon of Agrobactenium tumefaciens pTiC58 encodes 11 open reading frames by Kuldau G. A. (1990)
  43. Leroux , B. , M. F. Yanofsky , S. C. Winans , J. E. Ward , S. F. Ziegler , and E. W. Nester . 1987 . Characterization of the virA locus ofAgrobactenum tumefaciens: a transcriptional regulator and host range determinant . EMBO J. 6 : 849 - 856 . (10.1002/j.1460-2075.1987.tb04830.x) / EMBO J. / Characterization of the virA locus ofAgrobactenum tumefaciens: a transcriptional regulator and host range determinant by Leroux B. (1987)
  44. Lessl , M. , D. Balzer , W. Pansegrau , and E. Lanka . 1992 . Sequence similarities between the RP4 Tra 2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer . J. Biol. Chem. 267 : 20471 - 20480 . (10.1016/S0021-9258(19)88726-4) / J. Biol. Chem. / Sequence similarities between the RP4 Tra 2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer by Lessl M. (1992)
  45. 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 . (10.1128/JB.170.4.1430-1437.1988) / J. Bacteriol. / Genetic analysis of the virE operon of the Agrobacterium Ti plasmid pTiA6 by McBride K. E. (1988)
  46. Miller , V. L. , and J. J. Mekalanos . 1988 . A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR . J. Bacteriol. 170 : 2575 - 2583 . (10.1128/JB.170.6.2575-2583.1988) / J. Bacteriol. / A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR by Miller V. L. (1988)
  47. Ooms , G. , P. J. J. Hooykaas , R. J. M. Van Veen , P. Van Beelen , T. Regensburg-Tunik , and R. A. Schilperoort . 1982 . Octopine Ti-plasmid deletion mutants ofAgrobacterium tumefaciens with emphasis on the right side of the T-region . Plasmid 7 : 15 - 19 . (10.1016/0147-619X(82)90023-3) / Plasmid / Octopine Ti-plasmid deletion mutants ofAgrobacterium tumefaciens with emphasis on the right side of the T-region by Ooms G. (1982)
  48. Otten , L. , H. DeGreve , J. Leemans , R. Hain , P. Hooykaas , and J. Schell . 1984 . Restoration of virulence of vir region mutants of Agrobacterium tumefaciens strain B53 by coinfection with normal and mutant Agrobacterium strains . Mol. Gen. Genet. 195 : 159 - 163 . (10.1007/BF00332739) / Mol. Gen. Genet. / Restoration of virulence of vir region mutants of Agrobacterium tumefaciens strain B53 by coinfection with normal and mutant Agrobacterium strains by Otten L. (1984)
  49. Panicker , M. M. , and E. G. Minckley , Jr. 1992 . Purification and properties of the F sex factor TraD protein, an inner membrane conjugal transfer protein . J. Biol. Chem. 267 : 12761 - 12766 . (10.1016/S0021-9258(18)42341-1) / J. Biol. Chem. / Purification and properties of the F sex factor TraD protein, an inner membrane conjugal transfer protein by Panicker M. M. (1992)
  50. Peralta , E. G. , R. Hellmiss , and L. W. Ream . 1986 . overdrive, a T-DNA transmission enhancer on the A. tumefaciens tumorinducing plasmid . EMBO J. 5 : 1137 - 1142 . (10.1002/j.1460-2075.1986.tb04338.x) / EMBO J. / overdrive, a T-DNA transmission enhancer on the A. tumefaciens tumorinducing plasmid by Peralta E. G. (1986)
  51. Ream , W. 1989 . Agrobacterium tumefaciens and interkingdom genetic exchange. Annu . Rev. Phytopathol. 27 : 583 - 618 . (10.1146/annurev.py.27.090189.003055) / Rev. Phytopathol. / Agrobacterium tumefaciens and interkingdom genetic exchange. Annu by Ream W. (1989)
  52. Ried , J. L. , and A. Collmer . 1987 . An nptl-sacB-sacR cartridge for constructing directed, unmarked mutations in Gram-negative bacteria by marker exchange-eviction mutagenesis . Gene 57 : 239 - 246 . (10.1016/0378-1119(87)90127-2) / Gene / An nptl-sacB-sacR cartridge for constructing directed, unmarked mutations in Gram-negative bacteria by marker exchange-eviction mutagenesis by Ried J. L. (1987)
  53. Rogowsky , P. M. , T. J. Close , J. A. Chimera , J. J. Shaw , and C. I. Kado . 1987 . Regulation of the vir genes of Agrobacterium tumefaciens plasmid pTiC58 . J. Bacteriol. 169 : 5101 - 5112 . (10.1128/JB.169.11.5101-5112.1987) / J. Bacteriol. / Regulation of the vir genes of Agrobacterium tumefaciens plasmid pTiC58 by Rogowsky P. M. (1987)
  54. Scheer , U. , M. -C. Dabauvalle , H. Merkert , and R. Benavente . 1988 . The nuclear envelope and the organization of the pore complexes . Cell Biol. Int. Rep. 12 : 669 - 689 . (10.1016/0309-1651(88)90083-5) / Cell Biol. Int. Rep. / The nuclear envelope and the organization of the pore complexes by Scheer U. (1988)
  55. Schweizer , H. P. 1992 . Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker . Mol. Microbiol. 6 : 1195 - 1204 . (10.1111/j.1365-2958.1992.tb01558.x) / Mol. Microbiol. / Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker by Schweizer H. P. (1992)
  56. Shimoda , N. , A. Toyoda-Yamamoto , J. Nagamine , S. Usami , M. Katayama , Y. Sakagami , and Y. Machida . 1990 . Control of expression of Agrobactenium vir genes by synergistic actions of phenolic signal molecules and monosaccharides . Proc. Natl. Acad. Sci. USA 87 : 6684 - 6688 . (10.1073/pnas.87.17.6684) / Proc. Natl. Acad. Sci. USA / Control of expression of Agrobactenium vir genes by synergistic actions of phenolic signal molecules and monosaccharides by Shimoda N. (1990)
  57. Shirasu K. Z. Koukolikova-Nicola and C. I. Kado. 1992. Sixth International Symposium on Molecular Plant-Microbe Interactions Program abstract no. 33.
  58. Shirasu , K. , P. Morel , and C. I. Kado . 1990 . Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis . Mol. Microbiol. 4 : 1153 - 1163 . (10.1111/j.1365-2958.1990.tb00690.x) / Mol. Microbiol. / Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis by Shirasu K. (1990)
  59. 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 (London) 318 : 624 - 629 . (10.1038/318624a0) / Nature (London) / Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens by Stachel S. E. (1985)
  60. 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 . (10.1002/j.1460-2075.1986.tb04381.x) / EMBO J. / The genetic and transcriptional organization of the vir region of the A6 Ti-plasmid of Agrobacterium tumefaciens by Stachel S. E. (1986)
  61. 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 (London) 322 : 706 - 712 . (10.1038/322706a0) / Nature (London) / Generation of single-stranded T-DNA molecules during the initial stages of T-DNA transfer from Agrobacterium tumefaciens to plant cells by Stachel S. E. (1986)
  62. 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 for 5' virD gene products . EMBO J. 6 : 857 - 863 . (10.1002/j.1460-2075.1987.tb04831.x) / EMBO J. / Activation of Agrobacterium tumefaciens vir gene expression generates multiple single-stranded T-strand molecules from the pTiA6 T-region: requirement for 5' virD gene products by Stachel S. E. (1987)
  63. Stachel , S. E. , and P. C. Zambryski . 1986 . virA and virG control the plant-induced activation of the T-DNA transfer process of Agrobacterium tumefaciens . Cell 46 : 325 - 333 . (10.1016/0092-8674(86)90653-7) / Cell / virA and virG control the plant-induced activation of the T-DNA transfer process of Agrobacterium tumefaciens by Stachel S. E. (1986)
  64. Stachel , S. E. , and P. C. Zambryski . 1986 . Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation . Cell 47 : 155 - 157 . (10.1016/0092-8674(86)90437-X) / Cell / Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation by Stachel S. E. (1986)
  65. Steck , T. R. , T. J. Close , and C. I. Kado . 1989 . High levels of double-stranded transferred DNA (T-DNA) processing from an intact nopaline Ti plasmid . Proc. Natl. Acad. Sci. USA 86 : 2133 - 2137 . (10.1073/pnas.86.7.2133) / Proc. Natl. Acad. Sci. USA / High levels of double-stranded transferred DNA (T-DNA) processing from an intact nopaline Ti plasmid by Steck T. R. (1989)
  66. Sung , P. , D. H. Higgins , L. Prakash , and S. Prakash . 1988 . Mutation of Iysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activities but not the ability to bind ATP . EMBO J. 7 : 3263 - 3269 . (10.1002/j.1460-2075.1988.tb03193.x) / EMBO J. / Mutation of Iysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activities but not the ability to bind ATP by Sung P. (1988)
  67. Thompson , D. V. , L. S. Melchers , K. B. Idler , R. A. Schilperoort , and P. J. J. Hooykaas . 1988 . Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon . Nucleic Acids Res. 16 : 4621 - 4636 . (10.1093/nar/16.10.4621) / Nucleic Acids Res. / Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon by Thompson D. V. (1988)
  68. Toro , N. , A. Datta , 0. A. Carmi , C. Young , R. K. Prusti , and E. W. Nester . 1989 . The Agrobactenum tumefaciens virCl gene product binds to overdrive, a T-DNA transfer enhancer . J. Bacteriol. 171 : 6845 - 6849 . (10.1128/JB.171.12.6845-6849.1989) / J. Bacteriol. / The Agrobactenum tumefaciens virCl gene product binds to overdrive, a T-DNA transfer enhancer by Toro N. (1989)
  69. Toro , N. , A. Datta , M. Yanofsky , and E. Nester . 1988 . Role of the overdrive sequence in T-DNA border cleavage in Agrobactenum . Proc. Natl. Acad. Sci. USA 85 : 8558 - 8562 . (10.1073/pnas.85.22.8558) / Proc. Natl. Acad. Sci. USA / Role of the overdrive sequence in T-DNA border cleavage in Agrobactenum by Toro N. (1988)
  70. Vogel , A. M. , and A. Das . 1992 . The Agrobacterium tumefaciens virD3 gene is not essential for tumorigenicity on plants . J. Bacteriol. 174 : 5161 - 5164 . (10.1128/JB.174.15.5161-5164.1992) / J. Bacteriol. / The Agrobacterium tumefaciens virD3 gene is not essential for tumorigenicity on plants by Vogel A. M. (1992)
  71. Walker , J. E. , M. Saraste , M. J. Runswick , and N. J. Gay . 1982 . Distantly related sequences in the a- and 1-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold . EMBO J. 1 : 945 - 951 . (10.1002/j.1460-2075.1982.tb01276.x) / EMBO J. / Distantly related sequences in the a- and 1-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold by Walker J. E. (1982)
  72. 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 . (10.1126/science.235.4788.587) / Science / Site-specific nick in the T-DNA border sequence as a result of Agrobacterium vir gene expression by Wang K. (1987)
  73. Ward , E. R. , and W. M. Barnes . 1988 . VirD2 protein of Agrobacterium very tightly linked to the 5' end of T-strand DNA . Science 242 : 927 - 930 . (10.1126/science.242.4880.927) / Science / VirD2 protein of Agrobacterium very tightly linked to the 5' end of T-strand DNA by Ward E. R. (1988)
  74. Ward , J. E. , D. E. Akiyoshi , D. Regier , A. Datta , M. P. Gordon , and E. W. Nester . 1988 . Characterization of the virB operon from anAgrobacterium tumefaciens Ti plasmid . J. Biol. Chem. 263 : 5804 - 5814 . (10.1016/S0021-9258(18)60637-4) / J. Biol. Chem. / Characterization of the virB operon from anAgrobacterium tumefaciens Ti plasmid by Ward J. E. (1988)
  75. Ward , J. E. , D. E. Akiyoshi , D. Regier , A. Datta , M. P. Gordon , and E. W. Nester . 1990 . Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid . J. Biol. Chem. 265 : 4768 . (10.1016/S0021-9258(19)39628-0) / J. Biol. Chem. / Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid by Ward J. E. (1990)
  76. Ward , J. E. , Jr. , E. M. Dale , and E. N. Binns . 1991 . Activity of the Agrobacterium T-DNA machinery is affected by virB gene products . Proc. Natl. Acad. Sci. USA 88 : 9350 - 9354 . (10.1073/pnas.88.20.9350) / Proc. Natl. Acad. Sci. USA / Activity of the Agrobacterium T-DNA machinery is affected by virB gene products by Ward J. E. (1991)
  77. Ward , J. E. , Jr. , E. M. Dale , P. J. Christie , E. W. Nester , and A. N. Binns . 1990 . Complementation analysis of Agrobactenium tumefaciens Ti plasmid virB genes by use of a vir promoter expression vector: virB9, virBiO, and virBll are essential virulence genes . J. Bacteriol. 172 : 5187 - 5199 . (10.1128/JB.172.9.5187-5199.1990) / J. Bacteriol. / Complementation analysis of Agrobactenium tumefaciens Ti plasmid virB genes by use of a vir promoter expression vector: virB9, virBiO, and virBll are essential virulence genes by Ward J. E. (1990)
  78. Ward , J. E. , Jr. , E. M. Dale , E. W. Nester , and A. N. Binns . 1990 . Identification of a VirB10 protein aggregate in the inner membrane of Agrobacterium tumefaciens . J. Bacteriol. 172 : 5200 - 5210 . (10.1128/JB.172.9.5200-5210.1990) / J. Bacteriol. / Identification of a VirB10 protein aggregate in the inner membrane of Agrobacterium tumefaciens by Ward J. E. (1990)
  79. Winans , S. C. 1992 . Two-way chemical signaling in Agrobacterium-plant interactions . Microbiol. Rev. 56 : 12 - 31 . (10.1128/MR.56.1.12-31.1992) / Microbiol. Rev. / Two-way chemical signaling in Agrobacterium-plant interactions by Winans S. C. (1992)
  80. Winans , S. C. , P. R. Ebert , S. E. Stachel , M. P. Gordon , and E. W. Nester . 1986 . A gene essential for Agrobacterium virulence is homologous to a family of positive regulatory loci . Proc. Natl. Acad. Sci. USA 83 : 8278 - 8282 . (10.1073/pnas.83.21.8278) / Proc. Natl. Acad. Sci. USA / A gene essential for Agrobacterium virulence is homologous to a family of positive regulatory loci by Winans S. C. (1986)
  81. Yanofsky , M. F. , S. G. Porter , C. Young , L. Albright , M. P. Gordon , and E. W. Nester . 1986 . The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease . Cell 47 : 471 - 477 . (10.1016/0092-8674(86)90604-5) / Cell / The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease by Yanofsky M. F. (1986)
  82. 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 . (10.1128/JB.170.8.3367-3374.1988) / J. Bacteriol. / Association of the virD2 protein with the 5' end of T-strands in Agrobacterium tumefaciens by Young C. (1988)
  83. Zambryski , P. C. 1989 . Basic processes underlying Agrobacterium-mediated DNA transfer to plants. Annu . Rev. Genet. 22 : 1 - 30 . / Rev. Genet. / Basic processes underlying Agrobacterium-mediated DNA transfer to plants. Annu by Zambryski P. C. (1989)
  84. Zambryski , P. C. 1992 . Chronicles from the Agrobacteriumplant cell DNA transfer story. Annu . Rev. Plant Physiol. Plant Mol. Biol. 43 : 465 - 490 . (10.1146/annurev.pp.43.060192.002341) / Rev. Plant Physiol. Plant Mol. Biol. / Chronicles from the Agrobacteriumplant cell DNA transfer story. Annu by Zambryski P. C. (1992)
Dates
Type When
Created 8 years, 9 months ago (Nov. 7, 2016, 10:22 a.m.)
Deposited 4 years ago (July 29, 2021, 1:53 p.m.)
Indexed 1 year, 1 month ago (July 17, 2024, 4:29 a.m.)
Issued 32 years, 5 months ago (March 1, 1993)
Published 32 years, 5 months ago (March 1, 1993)
Published Print 32 years, 5 months ago (March 1, 1993)
Funders 0

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@article{Berger_1993, title={The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain}, volume={175}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.175.6.1723-1734.1993}, DOI={10.1128/jb.175.6.1723-1734.1993}, number={6}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Berger, B R and Christie, P J}, year={1993}, month=mar, pages={1723–1734} }