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PMID: 11607226 Published · ppublish English Journal Article

Activity of the Agrobacterium T-DNA transfer machinery is affected by virB gene products.

Ward JE, Dale EM, Binns AN

Abstract

The oriT (origin of transfer) sequence and mob (mobilization) genes of plasmid RSF1010 can functionally replace transfer DNA (T-DNA) borders to generate an RSF1010 intermediate transferable to plants through activities of the tumor-inducing (Ti)-plasmid virulence (vir) genes of Agrobacterium tumefaciens. Because the Ti plasmid virB gene products are hypothesized to form a membrane-localized T-DNA transport apparatus, we investigated whether specific virB genes were needed for RSF1010 transfer. Here we report that transformation of Nicotiana tabacum leaf explants by an RSF1010-derivative plasmid (pJW323) requires the essential virulence genes virB9, virB10, and virB11, consistent with the hypothesis that both the T-DNA and RSF1010 transfer intermediates utilize the same transport machinery. Further, while pJW323 is transferred into plant cells by Agrobacterium strains harboring both pJW323 and pTiA6, the initiation of crown gall tumors (i.e., T-DNA transfer) is greatly suppressed. Coordinate overexpression of the virB9, virB10, and virB11 gene products relieves pJW323-mediated oncogenic suppression and restores tumorigenicity, but does not increase the transfer frequency of pJW323 into plant cells. We propose that the virB9, virB10, and virB11 gene products function coordinately and stoichiometrically to enhance DNA transfer in a fashion specific for the T-DNA intermediate.

Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ward J E
Plant Sciences Institute, Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018, USA.
Dale E M
Binns A N
References (32)
32 references, click to expand
  1. 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 U S A. 1989 Jun;86(11):4017-21 PMID: 16594047
  2. Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis.
    Mol Microbiol. 1990 Jul;4(7):1153-63 PMID: 2233252
  3. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid.
    J Biol Chem. 1988 Apr 25;263(12):5804-14 PMID: 3281947
  4. Association of the virD2 protein with the 5' end of T strands in Agrobacterium tumefaciens.
    J Bacteriol. 1988 Aug;170(8):3367-74 PMID: 3403506
  5. Mutagenesis of the Tra1 core region of RK2 by using Tn5: identification of plasmid-specific transfer genes.
    J Bacteriol. 1989 Jul;171(7):4100-3 PMID: 2544570
  6. Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region.
    J Bacteriol. 1985 Mar;161(3):850-60 PMID: 2982791
  7. Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein.
    Proc Natl Acad Sci U S A. 1988 May;85(9):2909-13 PMID: 2452439
  8. The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA.
    J Bacteriol. 1988 Jun;170(6):2659-67 PMID: 2836366
  9. Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon.
    Nucleic Acids Res. 1988 May 25;16(10):4621-36 PMID: 2837739
  10. The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens.
    EMBO J. 1986 Jul;5(7):1445-54 PMID: 3017694
  11. Basic processes underlying Agrobacterium-mediated DNA transfer to plant cells.
    Annu Rev Genet. 1988;22:1-30 PMID: 3071244
  12. A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9677-81 PMID: 2532360
  13. Nucleotide sequence and genetic organization of the Bacillus subtilis comG operon.
    J Bacteriol. 1989 Oct;171(10):5386-404 PMID: 2507524
  14. Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: implications for the T-DNA transfer process.
    Proc Natl Acad Sci U S A. 1989 Feb;86(4):1193-7 PMID: 2919168
  15. Mobilization of T-DNA from Agrobacterium to plant cells involves a protein that binds single-stranded DNA.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):9006-10 PMID: 3480525
  16. 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. 1987 Apr;6(4):857-63 PMID: 3595560
  17. Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions.
    J Bacteriol. 1987 May;169(5):2086-91 PMID: 3571162
  18. Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation.
    Cell. 1986 Oct 24;47(2):155-7 PMID: 3768954
  19. Regions of broad-host-range plasmid RK2 involved in replication and stable maintenance in nine species of gram-negative bacteria.
    J Bacteriol. 1985 Oct;164(1):446-55 PMID: 4044529
  20. Overexpression of virD1 and virD2 genes in Agrobacterium tumefaciens enhances T-complex formation and plant transformation.
    J Bacteriol. 1990 Aug;172(8):4432-40 PMID: 2165478
  21. Complementation analysis of Agrobacterium tumefaciens Ti plasmid virB genes by use of a vir promoter expression vector: virB9, virB10, and virB11 are essential virulence genes.
    J Bacteriol. 1990 Sep;172(9):5187-99 PMID: 2203743
  22. Covalent association of the traI gene product of plasmid RP4 with the 5'-terminal nucleotide at the relaxation nick site.
    J Biol Chem. 1990 Jun 25;265(18):10637-44 PMID: 2191955
  23. Identification of a virB10 protein aggregate in the inner membrane of Agrobacterium tumefaciens.
    J Bacteriol. 1990 Sep;172(9):5200-10 PMID: 2394684
  24. The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames.
    Mol Gen Genet. 1990 Apr;221(2):256-66 PMID: 2370849
  25. Correction: characterization of the virB operon from Agrobacterium tumefaciens Ti plasmid.
    J Biol Chem. 1990 Mar 15;265(8):4768 PMID: 2307685
  26. Agrobacterium tumefaciens mutants affected in attachment to plant cells.
    J Bacteriol. 1982 Dec;152(3):1265-75 PMID: 6292165
  27. Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis.
    Cell. 1981 Nov;27(1 Pt 2):143-53 PMID: 6276020
  28. A general method for site-directed mutagenesis in prokaryotes.
    Nature. 1981 Jan 1;289(5793):85-8 PMID: 6256652
  29. Genetic map of the crown gall suppressive IncW plasmid pSa.
    Mol Gen Genet. 1982;186(1):10-5 PMID: 6287164
  30. Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas.
    Gene. 1981 Dec;16(1-3):237-47 PMID: 6282695
  31. Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors.
    Proc Natl Acad Sci U S A. 1974 Sep;71(9):3672-6 PMID: 4530328
  32. A complementation analysis of the restriction and modification of DNA in Escherichia coli.
    J Mol Biol. 1969 May 14;41(3):459-72 PMID: 4896022
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1991-10-15
Pages
9350-4
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC52712
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