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Agrobacterium tumefaciens and A. rhizogenes use different proteins to transport bacterial DNA into the plant cell nucleus
Article first published online: 6 APR 2009
DOI: 10.1111/j.1751-7915.2009.00104.x
© 2009 The Author. Journal compilation © 2009 Society for Applied Microbiology and Blackwell Publishing Ltd
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Microbial Biotechnology
Special Issue: Special Issue: Life of microbes that interact with plants
Volume 2, Issue 4, pages 416–427, July 2009
Total views since August 2010: 94
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How to Cite
Ream, W. (2009), Agrobacterium tumefaciens and A. rhizogenes use different proteins to transport bacterial DNA into the plant cell nucleus. Microbial Biotechnology, 2: 416–427. doi: 10.1111/j.1751-7915.2009.00104.x
Publication History
- Issue published online: 15 JUN 2009
- Article first published online: 6 APR 2009
- Received 26 November 2008; accepted 5 March 2009.
- Abstract
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References
- , and (1997) The translocating RecBCD enzyme stimulates recombination by directing RecA protein on to ssDNA in a chi-regulated manner. Cell 90: 77–86.
- , , and (2001) Non-homologous end-joining proteins are required for Agrobacterium T-DNA integration. EMBO J 20: 6550–6558.
- , and (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc Natl Acad Sci USA 94: 10723–10728.
- , , , , , and (2008) IMPa-4, an Arabidopsis importin alpha isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell 20: 2661–2680.
- , , and (1995) Inhibition of VirB-mediated transfer of diverse substrates from Agrobacterium tumefaciens by the IncQ plasmid RSF1010. J Bacteriol 177: 4890–4899.
- , , and (1982) Overlapping genes at the DNA primase locus of the large plasmid ColI. Nucleic Acids Res 10: 85–869.
- , and (2004) Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304: 1170–1173.
- (1997) Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J Bacteriol 179: 3085–3094.
- , , , and (1988) The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J Bacteriol 170: 2659–2667.
- , , and (1999) The RecBC enzyme loads RecA protein onto ssDNA asymmetrically and independently of chi, resulting in constitutive recombination activation. Genes Dev 13: 901–911.
- , , and (1988) Single-stranded DNA binding protein encoded by the virE locus of Agrobacterium tumefaciens. Science 240: 501–504.
- , , and (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.
- , , , and (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256: 1802–1805.
- , , and (1994) Nuclear import of Agrobacterium VirD2 and VirE2 proteins in maize and tobacco. Proc Natl Acad Sci USA 91: 3210–3214.
- , , , , , , et al. (2004) Protein interactions involved in nuclear import of the Agrobacterium VirE2 protein in vivo and in vitro. J Biol Chem 279: 29528–29533.
- , and (1984) Analysis of the R16 primase gene. Plasmid 12: 206–210.
- (1988) Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein. Proc Natl Acad Sci USA 85: 2909–2913.
- , , , , , , et al. (1999) VirE1 is a specific molecular chaperone for the exported single-stranded-DNA-binding protein VirE2 in Agrobacterium. Mol Microbiol 31: 1795–1807.
- , and (1997) Functional domains of Agrobacterium tumefaciens single-stranded DNA-binding protein VirE2. J Bacteriol 179: 1165–1173.
- , and (2003) The VirE2 protein of Agrobacterium tumefaciens: the Yin and Yang of T-DNA transfer. FEMS Microbiology Letters 223: 1–6.
- , , , , and (2001) An Agrobacterium VirE2 channel for transferred-DNA transport into plant cells. Proc Natl Acad Sci USA 98: 485–490.
- , and (1981) Nucleotide sequence from the genetic left end of bacteriophage T7 DNA to the beginning of gene 4. J Mol Biol 148: 303–330.
- , , , , , , et al. (2008) Crystal structure of the Agrobacterium virulence complex VirE1-VirE2 reveals a flexible protein that can accomodate different partners. Proc Natl Acad Sci USA 105: 11170–11175.
- , , , and (1987) Characterization of Agrobacterium tumefaciens virulence proteins induced by the plant factor acetosyringone. J Mol Biol 197: 635–645.
- , , and (1996) The tra region of the nopaline-type Ti plasmid is a chimera with elements related to the transfer systems of RSF1010, RP4, and F. J Bacteriol 178: 4233–4247.
- , , , , , , et al. (2007) Plant transformation by Agrobacterium tumefaciens: modulation of single-stranded DNA-VirE2 complex assembly by VirE1. J Biol Chem 282: 3458–3464.
- , , and (1998) Regena (Rga), a Drosophila homolog of the global negative transcriptional regulator CDC36 (NOT2) from yeast, modifies gene expression and suppresses position effect variegation. Genetics 148: 317–329.
- , and (1980) Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J Bacteriol 144: 732–743.
- (1998) Agrobacterium VirE2 proteins can form a complex with T strands in the plant cytoplasm. J Bacteriol 180: 4300–4302.
- (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51: 223–256.
- (2003) Agrobacterium-mediated plant transformation: the biology behind the ‘gene jockeying’ tool. Microbiol Mol Biol Rev 67: 16–37.
- , , and (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.
- , , , , , and (2008) VirE2: a unique ssDNA-compacting molecular machine. PLoS Biol 6: e44. doi:10.1371/journal.pbio.0060044.
- , , and (1996) Transport of DNA into the nuclei of Xenopus oocytes by a modified VirE2 protein of Agrobacterium. The Plant Cell 8: 363–373.
- , , , and (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.
- , , and (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.
- , , and (2004) Agrobacterium rhizogenes GALLS protein substitutes for Agrobacterium tumefaciens single-stranded DNA-binding protein VirE2. J Bacteriol 186: 3065–3077.
- , , , , , , and (2006) Agrobacterium rhizogenes GALLS protein contains domains for ATP binding, nuclear localization, and type IV secretion. J Bacteriol 188: 8222–8230.
- , , , , and (2009) Agrobacterium rhizogenes GALLS gene encodes two secreted proteins required for gene transfer to plants. J Bacteriol 191: 355–364.
- (1988) A new superfamily of replicative proteins. Nature 333: 22–23.
- , , , and (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.
- , , , and (2002) Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc Natl Acad Sci USA 99: 15327–15332.
- , , , , , and (1997) Targeted disruption in Arabidopsis. Nature 389: 802–803.
- , , , , and (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58: 401–465.
- , , and (1999) pSa causes oncogenic suppression of Agrobacterium by inhibiting VirE2 protein export. J Bacteriol 181: 186–196.
- , , , and (2005) Exploring cargo transport mechanics in the type IV secretion systems. Trends Microbiol 13: 295–298.
- , and (1974) Intragenic regulation of the synthesis of phiX174 gene A proteins. Nature 249: 345–348.
- , , , , , , et al. (1991) T-DNA integration: a mode of illegitimate recombination in plants. EMBO J 10: 697–704.
- , , , , , , and (2001) The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rhizobiaceae. J Mol Biol 307: 771–784.
- , and (2003) RecFOR proteins load RecA protein onto gapped DNA to acceleate DNA strand exchange: a universal step of recombinational repair. Mol Cell 11: 1337–1347.
- , , , , , , and (1998) Role of the Agrobacterium tumefaciens VirD2 protein in T-DNA transfer and integration. Mol Plant Microbe Interact 11: 668–683.
- , , , and (1996) Early transcription of Agrobacterium T-DNA genes in tobacco and maize. Plant Cell 8: 873–886.
- , , , , , and (1990) Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacteium mediated transformation. EMBO J 9: 3077–3084.
- , , , , and (1991) Localization and orientation of the VirD4 protein of Agrobacterium tumefaciens in the cell membrane. Molecular and General. Genetics 228: 24–32.
- , , , , , and (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.
- , and (1985) T-DNA border sequences required for crown gall tumorigenesis. Proc Natl Acad Sci USA 82: 5112–5116.
- (1991) Helical interactions in a homologous pairing and strand exchange driven by RecA protein. J Biol Chem 266: 5355–5358.
- (1998) Import of Agrobacterium tumefaciens virulence proteins and transferred DNA into plant cell nuclei. In Subcellular Biochemistry, Vol. 29. Biswas, B.B., and Das, H.K. (eds). New York, USA: Plenum Press, pp. 365–384.
- , , , , and (1998) Interaction of the DNA modifying proteins VirD1 and VirD2 of Agrobacterium tumefaciens: analysis by subcellular localization in mammalian cells. Proc Natl Acad Sci USA 95: 9105–9110.
- , , , , and (2000) A genetic system for detection of protein nuclear import and export. Nat Biotechnol 18: 433–437.
- , , and (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.
- , , and (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.
- , , , , , and (1989) Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene 75: 271–288.
- , , , , and (2003) Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: evidence for transport of a novel effector protein VirE3. Nucleic Acids Res 31: 860–868.
- , , , and (1989) Cooperative binding of the VirE2 protein to single-stranded DNA. J Bacteriol 171: 2573–2580.
- , , and (2005) High-frequency gene targeting in Arabidopsis plants expressing the yeast RAD54 gene. Proc Natl Acad Sci USA 102: 12265–12269.
- , , and (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.
- , , , and (2001) The carboxy-terminus of VirE2 from Agrobacterium tumefaciens is required for its transport to host cells by the virB-encoded type IV transport system. Mol Microbiol 41: 1283–1293.
- , and (1986) The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J 5: 1445–1454.
- , and (1986) Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation. Cell 47: 155–157.
- , , and (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.
- , , and (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.
- , , and (1998) The conjugal intermediate of plasmid RSF1010 inhibits Agrobacterium tumefaciens virulence and VirB-dependent export of VirE2. J Bacteriol 180: 3933–3939.
- , , , , and (1996) VirE1 protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J Bacteriol 178: 1207–1212.
- , and (1999) The Agrobacterium tumefaciens chaperone-like protein, VirE1, interacts with VirE2 at domains required for single-stranded DNA binding and cooperative interaction. J Bacteriol 181: 6850–6855.
- , , , and (1992) The T-DNA-linked VirD2 protein contains two distinct functional nuclear localization signals. Proc Natl Acad Sci USA 89: 7442–7446.
- , and (2002) Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol 12: 121–129.
- , , , , and (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through walls. Annu Rev Microbiol 54: 187–219.
- , , and (2001) VIP1, an Arabidopsis protein that interacts with Agrobacterim VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J 20: 3596–3607.
- , , and (2002) Increasing plant susceptibility to Agrobacterium infection by overexpression of the Arabidopsis nuclear protein VIP1. Proc Natl Acad Sci USA 99: 10435–10440.
- , , and (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.
- , , , , , and (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979–982.
- , , , and (2003) Recognition of the Agrobacterium tumefaciens VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol 133: 1–11.
- , , , , , and (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci USA 102: 832–837.
- , , , and (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.
- , and (1988) VirD2 protein of Agrobacterium tumefaciens very tightly linked to the 5′ end of T-strand DNA. Science 242: 927–930.
- , and (2001) The six functions of Agrobacterium VirE2. Proc Natl Acad Sci USA 98: 385–386.
- , , and (2002) Agrobacterium VirE2 gets the VIP1 treatment in plant nuclear import. Trends Plant Sci 7: 1–3.
- , , and (1997) Recombinational DNA repair: the RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps. Cell 91: 347–356.
- , , , , and (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164: 33–44.
- , , , , and (1987) Characterization of the virE operon of the Agrobacterium Ti plasmid pTiA6. Nucleic Acids Res 15: 825–838.
- , , , , , and (1986) The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease. Cell 47: 471–477.
- , and (1988) Association of the VirD2 protein with the 5′ end of T strands in Agrobacterium tumefaciens. J Bacteriol 170: 3367–3374.
- , , , and (1994) Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc Natl Acad Sci USA 91: 2994–2998.
- , and (1999) Mutagenesis of the Agrobacterium VirE2 single-stranded DNA-binding protein identifies regions required for self-association and interaction with VirE1 and a permissive site for hybrid protein construction. J Bacteriol 181: 4342–4352.
- , , , , , and (2000) The bases of crown gall tumorigenesis. J Bacteriol 182: 3885–3895.
- , , , , and (1999) Import of DNA into mammalian nuclei by proteins originating from a plant pathogenic bacterium. Proc Natl Acad Sci USA 96: 3729–3733.
- , , , , and (2001) Import of Agrobacterium T-DNA into plant nuclei: two distinct functions of VirD2 and VirE2 proteins. Plant Cell 13: 369–384.
- , , and (1996) Agrobacterium VirE2 protein mediates nuclear uptake of single-stranded DNA in plant cells. Proc Natl Acad Sci USA 93: 2392–2397.

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