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2001 | 48 | 3 | 623-635
Article title

Odyssey of Agrobacterium T-DNA.

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Agrobacterium tumefaciens, a plant pathogen, is characterized by the unique feature of interkingdom DNA transfer. This soil bacterium is able to transfer a fragment of its DNA, called T-DNA (transferred DNA), to the plant cell where T-DNA is integrated into the plant genome leading to "genetic colonization" of the host. The fate of T-DNA, its processing, transfer and integration, resembles the journey of Odysseus, although our hero returns from its long trip in a slightly modified form.The soil bacterium, Agrobacterium tumefaciens, is a plant pathogen responsible for tumor induction on dicotyledonous plants due to its ability to transfer DNA to the plant cell (reviewed in: de la Cruz & Lanka, 1998; Gelvin, 2000; Hansen & Chilton, 1999; Lartey & Citovsky, 1997; Rossi et al., 1998; Zupan & Zambryski, 1997). In biotechnology this ability is widely used for plant transformation. During tumor induction Agrobacterium attaches to plant cells and then transfers part of its DNA to some of these cells. The transferred DNA (T-DNA) which resides on a large Ti (tumor inducing) plasmid, is processed within the bacterium and is exported to the plant where it becomes integrated into the plant genome (reviewed in: Sheng & Citovsky, 1996; Tinland & Hohn, 1995; Tinland, 1996). Proteins encoded by the virulence (vir) region of the Ti plasmid regulate T-DNA processing and transfer. Phenolic compounds derived from a wounded plant cell wall induce expression of the vir region genes. Virulence proteins recognize 25 bp imperfect direct repeats (border sequences) that define the T-DNA. In the presence of VirD1 protein, VirD2 cleaves the border sequence in a site- and strand-specific manner and subsequently becomes covalently attached to the 5' end of the nicked DNA. The nicked DNA is then displaced from the plasmid producing single-stranded T-DNA. The T-DNA-VirD2 complex and the VirE2 protein are believed to be transferred to the plant through a pilus-like structure containing VirB and VirD4 proteins. In the plant cell, T-DNA becomes coated with the single-stranded DNA-binding protein, VirE2. The T-DNA-protein complex is imported into the nucleus where the T-DNA is integrated into the nuclear genome. Expression of genes located on T-DNA leads to the formation of proteins involved in the production of auxins and cytokinins. These plant hormones cause the tumorous phenotype that is characterized by the ability of the plant cells to proliferate limitlessly and autonomously even in the absence of added phytohormones. Crown gall tumors are characterized by the production of opines (amino-acid derivatives). The biosynthesis of opines is catalyzed by opine synthases, which are encoded by the T-DNA. Opines formed in the tumors can be metabolized by the tumorigenic agrobacteria, but not by most of the other soil organisms. Thus, Agrobacterium creates for itself a favorable niche by genetic modification of plant cells, a process called "genetic colonization". All stages of this colonization, including chemotaxis, attachment, induction of virulence region, processing of T-DNA, T-DNA transfer, T-DNA integration, expression of T-DNA genes and changes in the plant phenotype, will be discussed in the following chapters. This will be an odyssey of T-DNA that leaves the Agrobacterium cell in the form of nucleic acid and returns from its journey in the form of opines, derivatives of amino acids (Fig. 1).
Keywords
Publisher

Year
Volume
48
Issue
3
Pages
623-635
Physical description
Dates
published
2001
received
2001-05-17
accepted
2001-06-7
Contributors
  • Plant Protection and Biotechnology Laboratory, Department of Biotechnology, Intercollegiate Faculty of Biotechnology, University of Gdańsk, Gdańsk, Poland
References
  • Ashby, A.M., Watson, M.D., Loake, G.J. & Shaw, C.H. (1988) Ti plasmid-specified chemotaxis of Agrobacterium tumefaciens C58 toward vir-inducing phenolic compounds and soluble factors from monocotyledonous and dicotyledonous plants. J. Bacteriol. 170, 4181-4187.
  • Ballas, N. & Citovsky, V. (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc. Natl. Acad. Sci. U.S.A. 94, 10723-10728.
  • Berger, B.R. & Christie, P.J. (1994) Genetic complementation analysis of the Agrobacterium thumefaciens virB operon: virB2 through virB11 are essential virulence proteins. J. Bacteriol. 176, 3646-3660.
  • Binns, A.N. & Costantino, P. (1998) The Agrobacterium oncogenes; in The Rhizobiaceae (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 251-266, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Bouzar, H. & Moore, L.W. (1987) Isolation of different Agrobacterium biovars from a natural oak savanna and tallgrass prairie. Appl. Environ. Microbiol. 53, 717-721.
  • Bundock, P. & Hooykaas, P.J. (1996) Integration of Agrobacterium tumefaciens T-DNA in the Saccharomyces cerevisiae genome by illegitimate recombination. Proc. Natl. Acad. Sci. U.S.A. 93, 15272-15275.
  • Cangelosi, G.A., Martinetti, G., Leigh, J.A., Lee, C.C., Theines, C. & Nester, E.W. (1989) Role of Agrobacterium tumefaciens ChvA protein in export of β-1,2-glucan. J. Bacteriol. 171, 1609- 1615.
  • Christie, P.J. (1997) Agrobacterium tumefaciens T-complex transport apparatus: A paradigm for a new family of multifunctional transporters in eubacteria. J. Bacteriol. 179, 3085- 3094.
  • Citovsky, V., Guralnick, B., Simon, M.N. & Wall, J.S. (1997) The molecular structure of Agrobacterium VirE2-single-stranded DNA complexes involved in nuclear import. J. Mol. Biol. 271, 718-727.
  • de la Cruz, F. & Lanka, E. (1998) Function of the Ti-plasmid Vir proteins:T-complex formation and transfer to the plant cell; in The Rhizobiaceae (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 281-301, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Das, A. (1994) Regulation of Agrobacterium tumefaciens virulence gene expression; in: Molecular Mechanisms of Bacterial Virulence (Kado, C.I. & Crosa, J.H., eds.) pp. 477-489, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Dessaux, Y., Petit, A., Farrand, S.K. & Murphy, P.J. (1998) Opines and opine-like molecules involved in plant-Rhizobiaceae interactions; in The Rhizobiaceae (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 173-197, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Dumas, F., Duckely, M., Pelczar, P., Van Gelder, P. & Hohn, B. (2001) An Agrobacterium VirE2 channel for transferred-DNA transport into plant cells. Proc. Natl. Acad. Sci. U.S.A. 98, 485-490.
  • Filichkin, S.A. & Gelvin, S.B. (1993) Formation of a putative relaxation intermediate during T-DNA processing directed by the Agrobacterium tumefaciens VirD1, D2 endonuclease. Mol. Microbiol. 8, 915-926.
  • Fullner, K.J., Lara, C.J. & Nester, E.W. (1996) Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273, 1107-1109.
  • Gelvin, S.B. (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 223-256.
  • Ghai, J. & Das, A. (1989) The virD operon of Agrobacterium Ti plasmid encodes a DNA relaxing enzyme. Proc. Natl. Acad. Sci. U.S.A. 86, 3109-3113.
  • Gheysen, G., Villarroel, R. & Van Montagu, M. (1991) Illegitimate recombination in plants: A model for T-DNA integration. Genes Dev. 5, 287-297.
  • de Groot, M.J., Bundock, P., Hooykaas, P.J. & Beijersbergen, A.G. (1998) Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat. Biotechnol. 16, 839-842.
  • Guralnick, B., Thomsen, G. & Citovsky, V. (1996) Transport of DNA into the nuclei of Xenopus oocytes by a modified VirE2 protein of Agrobacterium. Plant Cell 8, 363-373.
  • Guyon, P., Chilton, M.D., Petit, A. & Tempe, J. (1980) Agropine in null-type crown gall tumors: Evidence for generality of the opine concept. Proc. Natl. Acad. Sci. U.S.A. 65, 2693-2697.
  • Hansen, G. & Chilton, M.D. (1999) Lessons in gene transfer to plants by a gifted microbe. Curr. Top. Microbiol. Immunol. 240, 21-57.
  • Hawes, M.C., Smith, L.Y. & Howarth, A.J. (1988) Agrobacterium tumefaciens mutants deficient in chemotaxis to root exudates. Mol. Plant-Microbe Interact. 1, 182-186.
  • Hooykaas, P.J.J., den Dulk-Ras, H. & Schilperoort, R.A. (1988) The Agrobacterium tumefaciens T-DNA gene 6b is an onc gene. Plant Mol. Biol. 11, 791-794.
  • Hooykaas, P.J.J. & Schilperoort, R.A. (1992) Agrobacterium and plant genetic engineering. Plant Mol. Biol. 19, 15-38.
  • Jin, S., Prusti, R.K., Roitsch, T., Ankenbauer, R.G. & Nester, E.W. (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.
  • Kim, K.S. & Farrand, S.K. (1998) Opine catabolic loci from Agrobacterium plasmids confer chemotaxis to their cognate substrates. Mol. Plant-Microbe Interact. 11, 131-143.
  • Korber, H., Strizhov, N., Staiger, D., Feldwish, J., Olsson, O., Sandberg, G., Palme, K., Schell, J., & Koncz, C. (1991) T-DNA gene 5 of Agrobacterium modulates auxin response by autoregulated synthesis of a growth hormone antagonist in plants. EMBO J. 10, 3983-3991.
  • Kunik, T., Tzfira, T., Kapulnik, Y. Gafni, Y., Dingwall, C. & Citovsky, V. (2001) Genetic transformation of HeLa cells by Agrobacterium. Proc. Natl. Acad. Sci. U.S.A. 98, 1871- 1876.
  • Lartey, R. & Citovsky, V. (1997). Nucleic acid transport in plant-pathogen interactions. Genet. Eng. (N Y) 19, 201-214.
  • Matsumoto, S., Ito, Y., Hosoi, T., Takahashi, Y. & 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.
  • Matthysse, A.G. (1983) Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J. Bacteriol. 154, 906-915.
  • Matthysse, A.G. & Kijne, J.W. (1998) Attachment of Rhizobiaceae to plant cells; in The Rhizobiaceae (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 235-249, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Matthysse, A.G., Yarnall, H.A. & Young, N. (1996) Requirements for gene with homology to ABC transporter systems for attachment and virulence of Agrobacterium tumefaciens. J. Bacteriol. 178, 5302-5308.
  • Mayerhofer, R., Koncz-Kalman, Z., Nawrath, C., Bakkeren, G., Crameri, A., Angelis, K., Redei, G.P., Schell, J., Hohn, B. & Koncz, C. (1991) T-DNA integration: A mode of illegitimate recombination in plants. EMBO J. 10, 697-704.
  • Mysore, K.S., Nam, J. & Gelvin, S.B. (2000) An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. Proc. Natl. Acad. Sci. U.S.A. 97, 948-953.
  • Nakielny, S. & Dreyfuss, G. (1999) Transport of proteins and RNAs in and out of the nucleus. Cell 99, 677-690.
  • Offringa, R., de Groot, M.J., Haagsman, H.J., Does, M.P., van den Elzen, P.J. & Hooykaas, P.J. (1990) Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium mediated transformation. EMBO J. 9, 3077-3084.
  • Pansegrau, W., Schoumacher, F., Hohn, B. & 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 U.S.A. 90, 11538-11542.
  • Parke, D., Ornston, L.N. & Nester, E.W. (1987) Chemotaxis to plant phenolic inducers of virulence genes is constitutively expressed in the absence of the pTi plasmid in Agrobacterium tumefaciens. J. Bacteriol. 169, 5336-5338.
  • Paszkowski, J., Baur, M., Bogucki, A. & Potrykus, I. (1988) Gene targeting in plants. EMBO J. 7, 4021-4026.
  • Petit, A. & Tempé, J. (1985) The function of T-DNA in nature; in Molecular Form and Function of the Plant Genome (van Vloten-Doting, L., Groot, G. & Hall, T., eds.) pp. 625-636, Plenum Press, New York.
  • Petit, A., David, C., Dahl, G.A., Ellis, J.G. & Guyon, P. (1983) Further extension of the opine concept: Plasmids in Agrobacterium rhizogenes cooperate for opine degradation. Mol. Gen. Genet. 190, 204-214.
  • Reuhs, B.L., Kim, J.S. & Matthysse, A.G. (1997) Attachment of Agrobacterium tumefaciens to carrot cells and Arabidopsis wound sites is correlated with the presence of a cell-associated, acidic polysaccharide. J. Bacteriol. 179, 5372-5379.
  • Rossi, L., Hohn, B. & 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.
  • Rossi, L., Hohn, B. & Tinland, B. (1996) Integration of complete T-DNA units is dependent on the activity of VirE2 protein of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. U.S.A. 93, 126-130.
  • Rossi, L., Tinland, B. & Hohn, B. (1998) Role of virulence proteins of Agrobacterium in the plant; in The Rhizobiaceae (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 302-330, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Scheiffele, P., Pansegrau, W. & Lanka, E. (1995) Initiation of Agrobacterium tumefaciens T-DNA processing: Purified proteins VirD1 and VirD2 catalyze site- and strand-specific cleavage of superhelical T-border DNA in vitro. J. Biol. Chem. 270, 1269-1276.
  • Schrindler, U., Sans, N. & Schröder, J. (1989) Ornithine cyclodeaminase from octopine Ti plasmid. J. Bacteriol. 171, 847-854.
  • Schröder, J., Von Lintig, J. & Zanker, H. (1990) Octopine (occ) and nopaline (noc) catabolic regions in Ti plasmids of Agrobacterium tumefaciens; in Advances in Molecular Genetics of the Plant-Microbe Interactions (Henneke, H. & Verma, D.P.S., eds.) vol. 1, pp. 28-31, Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Shaw, C.H., Ashby, A.M., Brown, A., Royal, C., Loake, G.J. & Shaw, C. (1988) virA and virG are Ti-plasmid functions required for chemotaxis of Agrobacterium tumefaciens towards acetosyringone. Mol. Microbiol. 2, 413-417.
  • Sheng, J. & Citovsky, V. (1996) Agrobacterium- plant cell DNA transport: Have virulence proteins, will travel. Plant Cell 8, 1699-1710.
  • Stachel, S.E., Messens, E., Van Montagu, M. & 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
  • Stachel, S.E., Timmerman, B. & 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.
  • Swart, S., Smit, G., Lugtenberg, B.J.J. & Kije, J.W. (1993) Restoration of attachment, virulence and nodulation of Agrobacterium tumefaciens chvB mutants by rhicadhesin. J. Bacteriol. 175, 597-605.
  • Tinland, B. (1996) The integration of T-DNA into plant genomes. Trends Plant Sci. 1, 178-184.
  • Tinland, B. & Hohn, B. (1995) Recombination between prokaryotic and eukaryotic DNA: Integration of Agrobacterium tumefaciens T-DNA into the plant genome. Genet. Eng. (NY) 17, 209-229.
  • Tinland, B., Fournier, P., Heckel, T. & Otten, L. (1992) Expression of a chimeric heat-shock-inducible Agrobacterium 6b oncogene in Nicotiana rustica. Plant Mol. Biol. 18, 921-930.
  • Tinland, B., Schoumacher, F., Gloeckler, V., Bravo- Angel, A.M. & 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.
  • Toro, N., Data, A., Carmi, O.A., Young, C., Prusti, R.K. & Nester, E.W. (1989) The Agrobacterium tumefaciens virC1 gene product binds to overdrive, a T-DNA transfer enhancer. J. Bacteriol. 171, 6845-6849.
  • Uttaro, A.D., Cangelosi, G.A., Geremia, R.A., Nester, E.W. & Ugalde, R.A. (1990) Biochemical characterization of avirulent exoC mutants of Agrobacterium tumefaciens. J. Bacteriol. 172, 1640-1646.
  • Von Lintig, J., Kreusch, D. & Schröder, J. (1994) Opine regulated promoters and LysR-type regulators in the nopaline (noc) and octopine (occ) catabolic regions of Ti plasmid of Agrobacterium tumefaciens. J. Bacteriol. 176, 495- 503.
  • Winans, S.C., Allenza, P., Stachel, S.E., McBride, K.E. & Nester, E.W. (1987) Characterization of the virE operon of the Agrobacterium tumefaciens Ti plasmid pTiA6. Nucleic Acids Res. 15, 825-837.
  • Yanofsky, M.F., Porter, S.G., Young, C., Albright, L.M., Gordon, M.P. & Nester, E.W. (1986) The virD operon from Agrobacterium tumefaciens encodes a site-specific endonuclease. Cell 47, 471-477.
  • Zanker, H., Von Lintig, J. & Schröder, J. (1992) Opine transport genes in the octopine (occ) and nopaline (noc) catabolic regions in Ti plasmids of Agrobacterium tumefaciens. J. Bacteriol. 174, 841-849.
  • Zhu, J., Oger, P.M., Schrammeijer, B., Hooykaas, P.J.J., Farrand, S.K. & Winans, S.C. (2000) The bases of crown gall tumorigenesis. J. Bacteriol. 182, 3885-3895.
  • Ziemienowicz, A., Görlich, D., Lanka, E., Hohn, B. & Rossi, L. (1999) Import of DNA into mammalian nuclei by proteins originating from a plant pathogenic bacterium. Proc. Natl. Acad. Sci. U.S.A. 96, 3729-3733.
  • Ziemienowicz, A., Tinland, B., Bryant, J., Gloeckler, V. & Hohn, B. (2000) Plant enzymes but not Agrobacterium VirD2 mediate T-DNA ligation in vitro. Mol. Cell. Biol. 20, 6317- 6322.
  • Ziemienowicz, A., Merkle, T., Schoumacher, F. Hohn, B. & Rossi, L. (2001) Import of Agrobacterium T-DNA into plant nuclei: Two distinct functions of VirD2 and VirE2 proteins. Plant Cell 13, 369-383.
  • Zorreguieta, A., Geremia, R.A., Cavaignac, S., Cangelosi, G.A., Nester, E.W. & Ugalde, R.A. (1988) Identification of the product of an Agrobacterium tumefaciens chromosomal virulence gene. Mol. Plant-Microbe Interact. 1, 121-127.
  • Zupan, J.R. & Zambryski, P. (1997) The Agrobacterium DNA transfer complex. Crit. Rev. Plant Sci. 16, 279-295.
  • Zupan, J.R., Citovsky, V. & Zambryski, P. (1996) Agrobacterium VirE2 protein mediates nuclear uptake of single-stranded DNA in plant cells. Proc. Natl. Acad. Sci. U.S.A. 93, 2392- 2397.
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