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. 1993 Apr 15;90(8):3549–3553. doi: 10.1073/pnas.90.8.3549

VirA, the plant-signal receptor, is responsible for the Ti plasmid-specific transfer of DNA to maize by Agrobacterium.

D M Raineri 1, M I Boulton 1, J W Davies 1, E W Nester 1
PMCID: PMC46338  PMID: 8475103

Abstract

Agrobacteria exhibit marked Ti (tumor-inducing)/Ri (root-inducing) plasmid specificity in their interaction with the Gramineae. In this study, we have used the technique of "agroinfection," in which Agrobacterium-mediated delivery of viral genomes into plants is detected by the development of viral disease symptoms, to identify the region of the Ti plasmid which is responsible for the major differences seen in the ability of nopaline- vs. octopine-type Ti plasmids to transfer maize streak virus (MSV) DNA to maize. Introduction of fragments of the C58 (nopaline-type) Ti plasmid into strains containing an octopine-type Ti plasmid showed that a fragment containing the nopaline-type virA locus was able to complement these normally non-agroinfectious strains to high levels of MSV DNA transfer. Octopine-type virA mutant strains that express vir genes at high levels in the absence of the plant inducing compound acetosyringone also efficiently transferred MSV DNA. These findings imply a functional difference between the virA gene products encoded by octopine- and nopaline-type Ti plasmids which has a profound effect on their ability to mediate DNA transfer to maize.

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Selected References

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

  1. Ankenbauer R. G., Best E. A., Palanca C. A., Nester E. W. Mutants of the Agrobacterium tumefaciens virA gene exhibiting acetosyringone-independent expression of the vir regulon. Mol Plant Microbe Interact. 1991 Jul-Aug;4(4):400–406. doi: 10.1094/mpmi-4-400. [DOI] [PubMed] [Google Scholar]
  2. Boulton M. I., King D. I., Markham P. G., Pinner M. S., Davies J. W. Host range and symptoms are determined by specific domains of the maize streak virus genome. Virology. 1991 Mar;181(1):312–318. doi: 10.1016/0042-6822(91)90497-y. [DOI] [PubMed] [Google Scholar]
  3. Bytebier B., Deboeck F., De Greve H., Montagu M. V., Hernalsteens J. P. T-DNA organization in tumor cultures and transgenic plants of the monocotyledon Asparagus officinalis. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5345–5349. doi: 10.1073/pnas.84.15.5345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cangelosi G. A., Best E. A., Martinetti G., Nester E. W. Genetic analysis of Agrobacterium. Methods Enzymol. 1991;204:384–397. doi: 10.1016/0076-6879(91)04020-o. [DOI] [PubMed] [Google Scholar]
  5. Close T. J., Zaitlin D., Kado C. I. Design and development of amplifiable broad-host-range cloning vectors: analysis of the vir region of Agrobacterium tumefaciens plasmid pTiC58. Plasmid. 1984 Sep;12(2):111–118. doi: 10.1016/0147-619x(84)90057-x. [DOI] [PubMed] [Google Scholar]
  6. Dasgupta I., Hull R., Eastop S., Poggi-Pollini C., Blakebrough M., Boulton M. I., Davies J. W. Rice tungro bacilliform virus DNA independently infects rice after Agrobacterium-mediated transfer. J Gen Virol. 1991 Jun;72(Pt 6):1215–1221. doi: 10.1099/0022-1317-72-6-1215. [DOI] [PubMed] [Google Scholar]
  7. Depicker A., De Wilde M., De Vos G., De Vos R., Van Montagu M., Schell J. Molecular cloning of overlapping segments of the nopaline Ti-plasmid pTiC58 as a means to restriction endonuclease mapping. Plasmid. 1980 Mar;3(2):193–211. doi: 10.1016/0147-619x(80)90109-2. [DOI] [PubMed] [Google Scholar]
  8. Ditta G., Stanfield S., Corbin D., Helinski D. R. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347–7351. doi: 10.1073/pnas.77.12.7347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drummond M. H., Chilton M. D. Tumor-inducing (Ti) plasmids of Agrobacterium share extensive regions of DNA homology. J Bacteriol. 1978 Dec;136(3):1178–1183. doi: 10.1128/jb.136.3.1178-1183.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Endoh H., Hirayama T., Aoyama T., Oka A. Characterization of the virA gene of the agropine-type plasmid pRiA4 of Agrobacterium rhizogenes. FEBS Lett. 1990 Oct 1;271(1-2):28–32. doi: 10.1016/0014-5793(90)80364-o. [DOI] [PubMed] [Google Scholar]
  11. Gardner R. C., Knauf V. C. Transfer of Agrobacterium DNA to Plants Requires a T-DNA Border But Not the virE Locus. Science. 1986 Feb 14;231(4739):725–727. doi: 10.1126/science.231.4739.725. [DOI] [PubMed] [Google Scholar]
  12. Graves A. C., Goldman S. L. Agrobacterium tumefaciens-mediated transformation of the monocot genus Gladiolus: detection of expression of T-DNA-encoded genes. J Bacteriol. 1987 Apr;169(4):1745–1746. doi: 10.1128/jb.169.4.1745-1746.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grimsley N., Hohn B., Hohn T., Walden R. "Agroinfection," an alternative route for viral infection of plants by using the Ti plasmid. Proc Natl Acad Sci U S A. 1986 May;83(10):3282–3286. doi: 10.1073/pnas.83.10.3282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grimsley N., Hohn B., Ramos C., Kado C., Rogowsky P. DNA transfer from Agrobacterium to Zea mays or Brassica by agroinfection is dependent on bacterial virulence functions. Mol Gen Genet. 1989 Jun;217(2-3):309–316. doi: 10.1007/BF02464898. [DOI] [PubMed] [Google Scholar]
  15. Hooykaas P. J., Hofker M., den Dulk-Ras H., Schilperoort R. A. A comparison of virulence determinants in an octopine Ti plasmid, a nopaline Ti plasmid, and an Ri plasmid by complementation analysis of Agrobacterium tumefaciens mutants. Plasmid. 1984 May;11(3):195–205. doi: 10.1016/0147-619x(84)90026-x. [DOI] [PubMed] [Google Scholar]
  16. Huffman G. A., White F. F., Gordon M. P., Nester E. W. Hairy-root-inducing plasmid: physical map and homology to tumor-inducing plasmids. J Bacteriol. 1984 Jan;157(1):269–276. doi: 10.1128/jb.157.1.269-276.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jarchow E., Grimsley N. H., Hohn B. virF, the host-range-determining virulence gene of Agrobacterium tumefaciens, affects T-DNA transfer to Zea mays. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10426–10430. doi: 10.1073/pnas.88.23.10426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Klapwijk P. M., van Beelen P., Schilperoort R. A. Isolation of a recombination deficient Agrobacterium tumefaciens mutant. Mol Gen Genet. 1979 Jun 7;173(2):171–175. doi: 10.1007/BF00330307. [DOI] [PubMed] [Google Scholar]
  19. McBride K. E., Summerfelt K. R. Improved binary vectors for Agrobacterium-mediated plant transformation. Plant Mol Biol. 1990 Feb;14(2):269–276. doi: 10.1007/BF00018567. [DOI] [PubMed] [Google Scholar]
  20. Morel P., Powell B. S., Rogowsky P. M., Kado C. I. Characterization of the virA virulence gene of the nopaline plasmid, pTiC58, of Agrobacterium tumefaciens. Mol Microbiol. 1989 Sep;3(9):1237–1246. doi: 10.1111/j.1365-2958.1989.tb00274.x. [DOI] [PubMed] [Google Scholar]
  21. Ooms G., Hooykaas P. J., Van Veen R. J., Van Beelen P., Regensburg-Tuïnk T. J., Schilperoort R. A. Octopine Ti-plasmid deletion mutants of agrobacterium tumefaciens with emphasis on the right side of the T-region. Plasmid. 1982 Jan;7(1):15–29. doi: 10.1016/0147-619x(82)90023-3. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Pazour G. J., Ta C. N., Das A. Mutants of Agrobacterium tumefaciens with elevated vir gene expression. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6941–6945. doi: 10.1073/pnas.88.16.6941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Rogowsky P. M., Powell B. S., Shirasu K., Lin T. S., Morel P., Zyprian E. M., Steck T. R., Kado C. I. Molecular characterization of the vir regulon of Agrobacterium tumefaciens: complete nucleotide sequence and gene organization of the 28.63-kbp regulon cloned as a single unit. Plasmid. 1990 Mar;23(2):85–106. doi: 10.1016/0147-619x(90)90028-b. [DOI] [PubMed] [Google Scholar]
  26. Stachel S. E., An G., Flores C., Nester E. W. A Tn3 lacZ transposon for the random generation of beta-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. EMBO J. 1985 Apr;4(4):891–898. doi: 10.1002/j.1460-2075.1985.tb03715.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Turk S. C., Melchers L. S., den Dulk-Ras H., Regensburg-Tuïnk A. J., Hooykaas P. J. Environmental conditions differentially affect vir gene induction in different Agrobacterium strains. Role of the VirA sensor protein. Plant Mol Biol. 1991 Jun;16(6):1051–1059. doi: 10.1007/BF00016076. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Zambryski P., Tempe J., Schell J. Transfer and function of T-DNA genes from agrobacterium Ti and Ri plasmids in plants. Cell. 1989 Jan 27;56(2):193–201. doi: 10.1016/0092-8674(89)90892-1. [DOI] [PubMed] [Google Scholar]

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