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. 1990 Sep;87(17):6684–6688. doi: 10.1073/pnas.87.17.6684

Control of expression of Agrobacterium vir genes by synergistic actions of phenolic signal molecules and monosaccharides.

N Shimoda 1, A Toyoda-Yamamoto 1, J Nagamine 1, S Usami 1, M Katayama 1, Y Sakagami 1, Y Machida 1
PMCID: PMC54601  PMID: 11607097

Abstract

Most virulence (vir) genes of Agrobacterium tumefaciens that are required for the formation of crown gall tumors are expressed in response to such plant signal molecules as acetosyringone and lignin precursors. The phenolic signals are transduced through a receptor VirA protein in the inner membrane of the bacterial cell. The expression of these genes triggers the transfer of a specific DNA segment, called transferred DNA (T-DNA), from the Ti plasmid to plant cells, and its integration into their nuclear DNA. We show here that a group of aldoses (L-arabinose, D-xylose, D-lyxose, D-glucose, D-mannose, D-idose, D-galactose, and D-talose) can markedly enhance acetosyringone-dependent expression of vir genes when the concentration of acetosyringone is limited (10 microM) but does not enhance the expression of noninducible genes. Likewise, a 2-deoxy-D-glucose, a nonmetabolized sugar, is also effective. When a deletion was introduced into the virA gene in the region encoding the periplasmic portion of the VirA protein, enhancement by glucose disappeared, but vir expression was induced by acetosyringone in this mutant. These results suggest that these sugars directly enhance a signaling process initiated by phenolic inducers that results in an increase in expression of the vir genes.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Das A., Stachel S., Ebert P., Allenza P., Montoya A., Nester E. Promoters of Agrobacterium tumefaciens Ti-plasmid virulence genes. Nucleic Acids Res. 1986 Feb 11;14(3):1355–1364. doi: 10.1093/nar/14.3.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Huang Y., Morel P., Powell B., Kado C. I. VirA, a coregulator of Ti-specified virulence genes, is phosphorylated in vitro. J Bacteriol. 1990 Feb;172(2):1142–1144. doi: 10.1128/jb.172.2.1142-1144.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Jin S. G., Roitsch T., Christie P. J., Nester E. W. The regulatory VirG protein specifically binds to a cis-acting regulatory sequence involved in transcriptional activation of Agrobacterium tumefaciens virulence genes. J Bacteriol. 1990 Feb;172(2):531–537. doi: 10.1128/jb.172.2.531-537.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Jin S., Roitsch T., Ankenbauer R. G., Gordon M. P., Nester E. W. The VirA protein of Agrobacterium tumefaciens is autophosphorylated and is essential for vir gene regulation. J Bacteriol. 1990 Feb;172(2):525–530. doi: 10.1128/jb.172.2.525-530.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Klee H. J., Gordon M. P., Nester E. W. Complementation analysis of Agrobacterium tumefaciens Ti plasmid mutations affecting oncogenicity. J Bacteriol. 1982 Apr;150(1):327–331. doi: 10.1128/jb.150.1.327-331.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Leroux B., Yanofsky M. F., Winans S. C., Ward J. E., Ziegler S. F., Nester E. W. Characterization of the virA locus of Agrobacterium tumefaciens: a transcriptional regulator and host range determinant. EMBO J. 1987 Apr;6(4):849–856. doi: 10.1002/j.1460-2075.1987.tb04830.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Mattanovich D., Rüker F., Machado A. C., Laimer M., Regner F., Steinkellner H., Himmler G., Katinger H. Efficient transformation of Agrobacterium spp. by electroporation. Nucleic Acids Res. 1989 Aug 25;17(16):6747–6747. doi: 10.1093/nar/17.16.6747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Melchers L. S., Regensburg-Tuïnk T. J., Bourret R. B., Sedee N. J., Schilperoort R. A., Hooykaas P. J. Membrane topology and functional analysis of the sensory protein VirA of Agrobacterium tumefaciens. EMBO J. 1989 Jul;8(7):1919–1925. doi: 10.1002/j.1460-2075.1989.tb03595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Niwa Y., Yamamoto A., Machida C., Takebe I., Machida Y. Right-hand border regions of octopine T-DNA are recognized by RNA polymerase of Agrobacterium as well as by VirD1 and VirD2 proteins. Nucleic Acids Res. 1988 Aug 11;16(15):7647–7661. doi: 10.1093/nar/16.15.7647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Pazour G. J., Das A. virG, an Agrobacterium tumefaciens transcriptional activator, initiates translation at a UUG codon and is a sequence-specific DNA-binding protein. J Bacteriol. 1990 Mar;172(3):1241–1249. doi: 10.1128/jb.172.3.1241-1249.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Powell B. S., Rogowsky P. M., Kado C. I. virG of Agrobacterium tumefaciens plasmid pTiC58 encodes a DNA-binding protein. Mol Microbiol. 1989 Mar;3(3):411–419. doi: 10.1111/j.1365-2958.1989.tb00186.x. [DOI] [PubMed] [Google Scholar]
  12. Rogowsky P. M., Close T. J., Chimera J. A., Shaw J. J., Kado C. I. Regulation of the vir genes of Agrobacterium tumefaciens plasmid pTiC58. J Bacteriol. 1987 Nov;169(11):5101–5112. doi: 10.1128/jb.169.11.5101-5112.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ronson C. W., Nixon B. T., Ausubel F. M. Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell. 1987 Jun 5;49(5):579–581. doi: 10.1016/0092-8674(87)90530-7. [DOI] [PubMed] [Google Scholar]
  14. Stachel S. E., Nester E. W. The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J. 1986 Jul;5(7):1445–1454. doi: 10.1002/j.1460-2075.1986.tb04381.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Stachel S. E., Nester E. W., Zambryski P. C. A plant cell factor induces Agrobacterium tumefaciens vir gene expression. Proc Natl Acad Sci U S A. 1986 Jan;83(2):379–383. doi: 10.1073/pnas.83.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Stachel S. E., Zambryski P. C. virA and virG control the plant-induced activation of the T-DNA transfer process of A. tumefaciens. Cell. 1986 Aug 1;46(3):325–333. doi: 10.1016/0092-8674(86)90653-7. [DOI] [PubMed] [Google Scholar]
  17. Usami S., Okamoto S., Takebe I., Machida Y. Factor inducing Agrobacterium tumefaciens vir gene expression is present in monocotyledonous plants. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3748–3752. doi: 10.1073/pnas.85.11.3748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Usami S, Morikawa S, Takebe I, Machida Y. Absence in monocotyledonous plants of the diffusible plant factors inducing T-DNA circularization and vir gene expression in Agrobacterium. Mol Gen Genet. 1987 Sep;209(2):221–226. doi: 10.1007/BF00329646. [DOI] [PubMed] [Google Scholar]
  19. Veluthambi K., Krishnan M., Gould J. H., Smith R. H., Gelvin S. B. Opines stimulate induction of the vir genes of the Agrobacterium tumefaciens Ti plasmid. J Bacteriol. 1989 Jul;171(7):3696–3703. doi: 10.1128/jb.171.7.3696-3703.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Vernade D., Herrera-Estrella A., Wang K., Van Montagu M. Glycine betaine allows enhanced induction of the Agrobacterium tumefaciens vir genes by acetosyringone at low pH. J Bacteriol. 1988 Dec;170(12):5822–5829. doi: 10.1128/jb.170.12.5822-5829.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ward J. E., Akiyoshi D. E., Regier D., Datta A., Gordon M. P., Nester E. W. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J Biol Chem. 1988 Apr 25;263(12):5804–5814. [PubMed] [Google Scholar]
  22. Winans S. C., Kerstetter R. A., Nester E. W. Transcriptional regulation of the virA and virG genes of Agrobacterium tumefaciens. J Bacteriol. 1988 Sep;170(9):4047–4054. doi: 10.1128/jb.170.9.4047-4054.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Winans S. C., Kerstetter R. A., Ward J. E., Nester E. W. A protein required for transcriptional regulation of Agrobacterium virulence genes spans the cytoplasmic membrane. J Bacteriol. 1989 Mar;171(3):1616–1622. doi: 10.1128/jb.171.3.1616-1622.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Yanofsky M. F., Nester E. W. Molecular characterization of a host-range-determining locus from Agrobacterium tumefaciens. J Bacteriol. 1986 Oct;168(1):244–250. doi: 10.1128/jb.168.1.244-250.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

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