Skip to main content
SpringerLink
Log in

Import of Agrobacterium tumefaciens Virulence Proteins and Transferred DNA into Plant Cell Nuclei

  • Chapter
Book cover Plant-Microbe Interactions

Part of the book series: Subcellular Biochemistry ((SCBI,volume 29))

Abstract

Agrobacterium tumefaciens causes crown gall tumors on many dicotyledonous plant species when the bacteria infect wounded tissue (DeCleene and DeLey, 1976). This bacterium harbors a tumor-inducing (Ti) plasmid, where genes essential for tumorigenesis are located (Watson et al., 1975; Van Larebeke et al., 1974). The transferred DNA (T-DNA) portion of the Ti plasmid enters plant cells and integrates into nuclear DNA (Chilton et al., 1977, 1980; Willmitzer et al., 1980). Tumorous growth results from expression of three T-DNA genes that encode biosynthetic enzymes for two plant growth hormones, auxin (indole acetic acid) and cytokinin (isopentenyl adenosine) for reviews see Ream, 1989; Winans, 1992; Zambryski, 1992). There are many excellent reviews of Agrobacterium tumefaciens biology (Zambryski, 1992; Winans, 1992; Hooykaas and Beijersbergen, 1994; Citovsky, and Zambryski, 1993; Dreiseikelmann, 1994; Ream, 1989; Binns and Thomashow, 1988), and the most recent presents an outstanding treatment of nuclear localization of T-DNA (Sheng and Citovsky, 1996), the topic of this chapter.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Albright, L. M., Yanofsky, M. F., Leroux, B., Ma, D., and Nester, E. W., 1987, Processing of the T-DNA of Agrobacterium tumefaciens generates border nicks and linear, single-stranded T-DNA, J. Bacteriol. 169:1046–1055.

    PubMed  CAS  Google Scholar 

  • Binns, A. N., and Thomashow, 1988, Cell biology of Agrobacterium infection and transformation of plants, Annu. Rev. Microbiol. 42:575–606.

    Article  CAS  Google Scholar 

  • Binns, A. N., Beaupre, C. E., and Dale, E. M., 1995, Inhibition of VirB-mediated transfer of diverse substrates from Agrobacterium tumefaciens by the IncQ plasmid RSF1010, J. Bacteriol. 177:4890–4899.

    PubMed  CAS  Google Scholar 

  • Bravo Angel, A. M., Tinland, B., and Hohn, B., 1996, The role of virulence proteins in nuclear targeting and integration of T-DNA, in Crown Gall: Advances in Understanding Interkingdom Genetic Exchange (W. Ream and S. B. Gelvin, eds.), pp. 30–43, APS Press, St. Paul, Minnesota.

    Google Scholar 

  • Buchanan-Wollaston, V., Passiatore, J. E., and Cannon, F., 1987, The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants, Nature 328:172–175.

    Article  CAS  Google Scholar 

  • Buchanan-Wollaston, V., Passiatore, J. E., and Cannon, F., 1988, The effect of vir mutations on plasmid transfer into plants, in Molecular Genetics of plant-Microbe Interactions (R. Palachios and D. P. S. Verma, eds.), pp. 281–282, APS Press, Saint Paul, Minnesota.

    Google Scholar 

  • Chilton, M. D., Drummond, M. H., Merlo, D. J., Sciaky, D., Montoya, A. L., Gordon, M. P., and Nester, E. W., 1977, Stable incorporation of plasmid DNA into higher plant cells: The molecular basis of crown gall tumorigenesis, Cell 11:263–271.

    Article  PubMed  CAS  Google Scholar 

  • Chilton, M. D., Saiki, R. K., Yadav, N., Gordon, M. P., and Quetier, F., 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.

    Article  PubMed  CAS  Google Scholar 

  • Christie, P. J., Ward, J. E., Winans, S. C., and Nester, E. W., 1988, The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA, J. Bacteriol. 170:2659–2667.

    PubMed  CAS  Google Scholar 

  • Citovsky, V., and Zambryski, P., 1993, Transport of nucleic acids through membrane channels: Snaking through small holes, Annu. Rev. Microbiol. 47:167–197.

    Article  PubMed  CAS  Google Scholar 

  • Citovsky, V., De Vos, G., and Zambryski, P., 1988, Single-stranded DNA binding protein encoded by the virE locus of Agrobacterium tumefaciens, Science 240:501–504.

    Article  PubMed  CAS  Google Scholar 

  • Citovsky, V., Wong, M. L., and Zambryski, P., 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.

    Article  PubMed  CAS  Google Scholar 

  • Citovsky, V., Zupan, J., Warnick, D., and Zambryski, P., 1992, Nuclear localization of Agrobacterium VirE2 protein in plant cells, Science 256:1802–1805.

    Article  PubMed  CAS  Google Scholar 

  • Covacci, A., and Rappuoli, R., 1993, Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon, Mol. Microbiol. 8:429–434.

    Article  PubMed  CAS  Google Scholar 

  • Das, A., 1988, Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein, Proc. Natl. Acad. Sci. USA 85:2909–2913.

    Article  PubMed  CAS  Google Scholar 

  • DeCleene, M., and DeLey, J., 1976, The host range of crown gall, Bot. Rev. 42:389–466.

    Article  Google Scholar 

  • Derbyshire, K. M., Hatfull, G., and Willetts, N., 1987, Mobilization of the non-conjugative plasmid RSF1010: A genetic and DNA sequence analysis of the mobilization region, Mol. Gen. Genet. 206:161–168.

    Article  PubMed  CAS  Google Scholar 

  • Dombek, P., and Ream, W., 1997, Functional domains of Agrobacterium tumefaciens single-stranded DNA-binding protein VirE2, J. Bacteriol. 179:1165–1173.

    PubMed  CAS  Google Scholar 

  • Dreiseikelmann, B., 1994, Translocation of DNA across bacterial membranes, Microbiol. Rev. 58:293–316.

    PubMed  CAS  Google Scholar 

  • Durrenberger, F., Crameri, A., Hohn, B., and Koukolikova-Nicola, Z., 1989, Covalently bound VirD2 protein of Agrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation, Proc. Natl. Acad. Sci. USA 86:9154–9158.

    Article  PubMed  CAS  Google Scholar 

  • Gardner, R. C., and Knauf, V. C., 1986, Transfer of Agrobacterium DNA to plants requires a T-DNA border but not the virE locus, Science 231:725–727.

    Article  PubMed  CAS  Google Scholar 

  • Garfinkel, D. J., and Nester, E. W., 1980, Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism, J. Bacteriol. 144:732–743.

    PubMed  CAS  Google Scholar 

  • Gheysen, G., Van Montagu, M., and Zambryski, P., 1987, Integration of Agrobacterium tumefaciens transfer DNA (T-DNA) involves rearrangements of target plant DNA sequences, Proc. Natl. Acad. Sci. USA 84:6169–6173.

    Article  PubMed  CAS  Google Scholar 

  • Gheysen, G., Villarroel, R., and Van Montagu, M., 1991, Illegitimate recombination in plants: A model for T-DNA integration, Genes Dev. 5:287–297.

    Article  PubMed  CAS  Google Scholar 

  • Gietl, C., Koukolikova-Nicola, Z., and Hohn, B., 1987, Mobilization of T-DNA from Agrobacterium to plant cells involves a protein that binds single-stranded DNA, Proc. Natl. Acad. Sci. USA 84:9006–9010.

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Estrella, A., Chen, Z., Van Montagu, M., and Wang, K., 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.

    PubMed  CAS  Google Scholar 

  • Herrera-Estrella, A., Van Montagu, M., and Wang, K., 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.

    Article  PubMed  CAS  Google Scholar 

  • Hooykaas, P. J. J., and Beijersbergen, G. M., 1994, The virulence system of Agrobacterium tumefaciens, Annu. Rev. Phytopathol. 32:157–179.

    Article  CAS  Google Scholar 

  • Howard, E. A., Winsor, B. A., De Vos, G., and Zambryski, P., 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.

    Article  PubMed  CAS  Google Scholar 

  • Howard, E. A., Zupan, J. R., Citovsky, V., and Zambryski, P. C., 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.

    Article  PubMed  CAS  Google Scholar 

  • Jasper, F., Koncz, C., Schell, J., and Steinbiss, H. H., 1994, Agrobacterium T-strand production in vitro: Sequence-specific cleavage and 5′ protection of single-stranded DNA templates by purified VirD2 protein, Proc. Natl. Acad. Sci. USA 91:694–698.

    Article  PubMed  CAS  Google Scholar 

  • Jayaswal, R. K., Veluthambi, K., Gelvin, S. B., and Slightom, J. L., 1987, Double-stranded T-DNA cleavage and the generation of single-stranded T-DNA molecules in E. coli by a virD encoded border specific endonuclease from Agrobacterium tumefaciens, J. Bacteriol. 169:5035–5045.

    PubMed  CAS  Google Scholar 

  • Lessl, M., Balzer, D., Pansegrau, W., and Lanka, E., 1992, Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer, J. Biol. Chem. 267:20471–20480.

    PubMed  CAS  Google Scholar 

  • Matsumoto, S., Ito, Y., Hosoi, T., Takahashi, Y., and Machida, Y., 1990, Integration of Agrobacterium T-DNA into a tobacco chromosome: Possible involvement of DNA homology between T-DNA and plant DNA, Mol. Gen. Genet. 224:309–316.

    Article  PubMed  CAS  Google Scholar 

  • Mayerhofer, R., Koncz-Kalman, Z., Nawrath, C., Bakkeren, G., Crameri, A., Angelis, K., Redei, G. P., Schell, J., Hohn, B., and Koncz, C., 1991, T-DNA integration: A mode of illegitimate recombination in plants, EMBO J. 10:697–704.

    PubMed  CAS  Google Scholar 

  • Narasimhulu, S. B., Deng, X., Sarria, R., and Gelvin, S. B., 1996, Early transcription of Agrobacterium T-DNA genes in tobacco and maize, Plant Cell 8:873–886.

    PubMed  CAS  Google Scholar 

  • Okamoto, S., Toyoda-Yamamoto, A., Ito, K., Takebe, I., and Machida, Y., 1991, Localization and orientation of the VirD4 protein of Agrobacterium tumefaciens in the cell membrane, Mol. Gen. Genet. 228:24–32.

    Article  PubMed  CAS  Google Scholar 

  • Otten, L., DeGreve, H., Leemans, J., Hain, R., Hooykaas, P. J. J., and Schell, J., 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.

    Article  Google Scholar 

  • Pansegrau, W., Schoumacher, F., Hohn, B., and Lanka, E., 1993, Site-specific cleavage and joining of single-stranded DNA by VirD2 protein of Agrobacterium tumefaciens Ti plasmids: Analogy to bacterial conjugation, Proc. Natl. Acad. Sci. USA 90:11538–11542.

    Article  PubMed  CAS  Google Scholar 

  • Peralta, E. G., and Ream, L. W., 1985, T-DNA border sequences required for crown gall tumor-igenesis, Proc. Natl. Acad. Sci. USA 82:5112–5116.

    Article  PubMed  CAS  Google Scholar 

  • Peralta, E. G., Hellmiss, R., and Ream, W., 1986, Overdrive, a T-DNA transmission enhancer on the A. tumefaciens tumour-inducing plasmid, EMBO J. 5:1137–1142.

    PubMed  CAS  Google Scholar 

  • Pohlman, R. F., Genetti, H. D., and Winans, S. C., 1994, Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens, Mol. Microbiol. 14:655–668.

    Article  PubMed  CAS  Google Scholar 

  • Radding, C. M., 1991, Helical interactions in a homologous pairing and strand exchange driven by RecA protein, J. Biol Chem. 266:5355–5358.

    PubMed  CAS  Google Scholar 

  • Ream, W., 1989, Agrobacterium tumefaciens and interkingdom genetic exchange, Annu. Rev. Phytopathol. 27:583–618.

    Article  Google Scholar 

  • Rees, C. E. D., and Wilkins, B. M., 1990, Protein transfer into the recipient cell during bacterial conjugation: Studies with F and RP4, Mol. Microbiol. 4:1199–1205.

    Article  PubMed  CAS  Google Scholar 

  • Regensburg-Tuink, A. J. G., 1993, Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens, Nature 363:69–71.

    Article  PubMed  CAS  Google Scholar 

  • Robbins, J., Dilworth, S. M., Laskey, R. A., and Dingwall, C., 1991, Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: Identification of a class of bipartite nuclear targeting sequence, Cell 64:615–623.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, L., Hohn, B., and Tinland, B., 1993, The VirD2 protein of Agrobacterium tumefaciens carries nuclear localization signals important for transfer of T-DNA to plants, Mol. Gen. Genet. 239:345–353.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, L., Hohn, B., and Tinland, B., 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.

    Article  PubMed  CAS  Google Scholar 

  • Scholz, P., Haring, V., Wittmann-Liebold, B., Ashman, K., Bagdasarian, M., and Scherzinger, E., 1989, Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010, Gene 75:271–288.

    Article  PubMed  CAS  Google Scholar 

  • Sen, P., Pazour, G. J., Anderson, D., and Das, A., 1989, Cooperative binding of the VirE2 protein to single-stranded DNA, J. Bacteriol. 171:2573–2580.

    PubMed  CAS  Google Scholar 

  • Shaw, C. H., Watson, M., and Carter, G., 1984, The right hand copy of the nopaline Ti plasmid 25 bp repeat is required for tumour formation, Nucleic Acids Res. 12:6031–6041.

    Article  PubMed  CAS  Google Scholar 

  • Sheng, J., and Citovsky, V., 1996, Agrobacterium-plant cell DNA transport: Have virulence proteins, will travel, Plant Cell 8:1699–1710.

    PubMed  CAS  Google Scholar 

  • Shurvinton, C. E., Hodges, L., and Ream, W., 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.

    Article  PubMed  CAS  Google Scholar 

  • Silver, P. A., 1991, How proteins enter the nucleus, Cell 64:489–497.

    Article  PubMed  CAS  Google Scholar 

  • Stachel, S. E., and Nester, E. W., 1986, The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens, EMBO J. 5:1445–1454.

    PubMed  CAS  Google Scholar 

  • Stachel, S. E., and Zambryski, P., 1986, Agrobacterium tumefaciens and the susceptible plant cell: A novel adaptation of extracellular recognition and DNA conjugation, Cell 47:155–157.

    Article  PubMed  CAS  Google Scholar 

  • Stachel, S. E., Messens, E., Van Montagu, M., and Zambryski, P., 1985, Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens, Nature 318:624–629.

    Article  Google Scholar 

  • Stachel, S. E., Timmerman, B., and Zambryski, P., 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.

    Article  CAS  Google Scholar 

  • Stachel, S. E., Timmerman, B., and Zambryski, P., 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.

    PubMed  CAS  Google Scholar 

  • Sundberg, C., Meek, L., Carroll, K., Das, A., and Ream, W., 1996, VirEl protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells, J. Bacteriol. 178:1207–1212.

    PubMed  CAS  Google Scholar 

  • Tinland, B., Koukolikova-Nicola, Z., Hall, M. N., and Hohn, B., 1992, The T-DNA-linked VirD2 protein contains two distinct functional nuclear localization signals, Proc. Natl. Acad. Sci. USA 89:7442–7446.

    Article  PubMed  CAS  Google Scholar 

  • Tinland, B., Hohn, B., and Puchta, H., 1994, Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus, Proc. Natl. Acad. Sci. USA 91:8000–8004.

    Article  PubMed  CAS  Google Scholar 

  • Tinland, B., Schoumacher, F., Gloeckler, V., Bravo-Angel, A., and Hohn, B., 1995, The Agrobacterium tumefaciens virulence D2 protein is responsible for precise integration of T-DNA into the plant genome, EMBO J. 14:3585–3595.

    PubMed  CAS  Google Scholar 

  • Toro, N., Datta, A., Carmi, O. A., Young, C., Prusti, R. K., and Nester, E. W., 1989, The Agrobacterium tumefaciens virC1 gene products binds to Overdrive, a T-DNA transfer enhancer, J. Bacteriol. 171:6845–6849.

    PubMed  CAS  Google Scholar 

  • Van Larebeke, N., Engler, G., Holsters, M., Van den Eisacker, S., Zaenen, I., Schilperoort, R. A., and Schell, J., 1974, Large plasmid in Agrobacterium tumefaciens essential for crown gall inducing activity, Nature 252:169–170.

    Article  PubMed  Google Scholar 

  • Van Slogteren, G. M. S., Hooykaas, P. J. J., and Schilperoort, R. A., 1984, Tumor formation on plants by mixtures of attenuated Agrobacterium tumefaciens T-DNA mutants, Plant Mol. Biol. 3:337–344.

    Article  Google Scholar 

  • Veluthambi, K., Jayaswal, R. K., and Gelvin, S. B., 1987, Virulence genes A, G, and D mediate the double-stranded border cleavage of T-DNA from the Agrobacterium Ti plasmid, Proc. Natl. Acad. Sci. USA 84:1881–1885.

    Article  PubMed  CAS  Google Scholar 

  • Veluthambi, K., Ream, W., and Gelvin, S. B., 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.

    PubMed  CAS  Google Scholar 

  • Vogel, A. M., and Das, A., 1992, Mutational analysis of Agrobacterium tumefaciens virD2: Tyrosine 29 is essential for endonuclease activity, J. Bacteriol. 174:303–308.

    PubMed  CAS  Google Scholar 

  • Wang, K., Herrera-Estrella, L., Van Montagu, M., and Zambryski, P., 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.

    Article  PubMed  CAS  Google Scholar 

  • Wang, K., Stachel, S. E., Timmerman, B., Van Montagu, M., and Zambryski, P., 1987, Site-specific nick in the T-DNA border sequence as a result of Agrobacterium vir gene expression, Science 235:587–591.

    Article  PubMed  CAS  Google Scholar 

  • Ward, E. R., and Barnes, W. M., 1988, VirD2 protein of Agrobacterium tumefaciens very tightly linked to the 5′ end of T-strand DNA, Science 242:927–930.

    Article  CAS  Google Scholar 

  • Ward, J. E., Dale, E. M., and Binns, A. N., 1991, Activity of the Agrobacterium T-DNA transfer machinery is affected by virB gene products, Proc. Natl. Acad. Sci. USA 88:9350–9354.

    Article  PubMed  CAS  Google Scholar 

  • Watson, B., Currier, T. C., Gordon, M. P., Chilton, M. D., and Nester, E. W., 1975, Plasmid required for virulence of Agrobacterium tumefaciens, J. Bacteriol. 123:255–264.

    PubMed  CAS  Google Scholar 

  • Weiss, A. A., Johnson, F. D., and Burns, D. L., 1993, Molecular characterization of an operon required for pertussis toxin secretion, Proc. Natl. Acad. Sci. USA 90:2970–2974.

    Article  PubMed  CAS  Google Scholar 

  • Willmitzer, L., Debeuckeleer, M., Lemmers, M., Van Montagu, M., and Schell, J., 1980, DNA from Ti plasmid present in nucleus and absent from plastids of crown gall plant cells, Nature 287:359–361.

    Article  CAS  Google Scholar 

  • Winans, S. C., 1992, Two-way chemical signaling in Agrobacterium-plant interactions, Microbiol. Rev. 56:12–31.

    PubMed  CAS  Google Scholar 

  • Yanofsky, M. F., Porter, S. G., Young, C., Albright, L. M., Gordon, M. P., and Nester, E. W., 1986, The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease, Cell 47:471–477.

    Article  PubMed  CAS  Google Scholar 

  • Young, C., and Nester, E. W., 1988, Association of the VirD2 protein with the 5′ end of T strands in Agrobacterium tumefaciens, J. Bacteriol. 170:3367–3374.

    PubMed  CAS  Google Scholar 

  • Yusibov, V. M., Steck, T. R., Gupta, V., and Gelvin, S. B., 1994, Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells, Proc. Natl. Acad. Sci. USA 91:2994–2998.

    Article  PubMed  CAS  Google Scholar 

  • Zambryski, P. C., 1992, Chronicles from the Agrobacterium-plant cell DNA transfer story, Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:465–490.

    Article  CAS  Google Scholar 

  • Zupan, J. R., Citovsky, V., and Zambryski, P., 1996, Agrobacterium VirE2 protein mediates nuclear uptake of single-stranded DNA in plant cells, Proc. Natl. Acad. Sci. USA 93:2392–2397.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular and Cellular Biology Program and Department of Microbiology, Oregon State University, Corvallis, Oregon, 97331, USA

    Walt Ream

Authors
  1. Walt Ream
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Calcutta, Calcutta, India

    B. B. Biswas

  2. Jawaharlal Nehru University, New Delhi, India

    H. K. Das

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media New York

About this chapter

Cite this chapter

Ream, W. (1998). Import of Agrobacterium tumefaciens Virulence Proteins and Transferred DNA into Plant Cell Nuclei. In: Biswas, B.B., Das, H.K. (eds) Plant-Microbe Interactions. Subcellular Biochemistry, vol 29. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-1707-2_12

Download citation

  • DOI: https://doi.org/10.1007/978-1-4899-1707-2_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4899-1709-6

  • Online ISBN: 978-1-4899-1707-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation