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The Ti Plasmids

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  • Authors: Jay E. Gordon1, Peter J. Christie2
  • Editors: Marcelo E. Tolmasky3, Juan Carlos Alonso4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology and Molecular Genetics, University of Texas Medical School at Houston, Houston, TX 77005; 2: Department of Microbiology and Molecular Genetics, University of Texas Medical School at Houston, Houston, TX 77005; 3: California State University, Fullerton, CA; 4: Centro Nacional de Biotecnología, Cantoblanco, Madrid, Spain
  • Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0010-2013
  • Received 31 January 2014 Accepted 03 February 2014 Published 21 November 2014
  • Peter J. Christie, Peter.J.Christie@uth.tmc.edu
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  • Abstract:

    is a plant pathogen with the capacity to deliver a segment of oncogenic DNA carried on a large plasmid called the tumor-inducing or Ti plasmid to susceptible plant cells. belongs to the class , whose members include other plant pathogens (), plant and insect symbionts ( spp. and spp., respectively), human pathogens ( spp., spp., spp.), and nonpathogens (). Many species of carry large plasmids ranging in size from ∼100 kb to nearly 2 Mb. These large replicons typically code for functions essential for cell physiology, pathogenesis, or symbiosis. Most of these elements rely on a conserved gene cassette termed for replication and partitioning, and maintenance at only one or a few copies per cell ( 1 ). The subject of this review is the ∼200-kb Ti plasmids carried by infectious strains of . We will summarize the features of this plasmid as a representative of the family of megaplasmids. We will also describe novel features of this plasmid that enable cells to incite tumor formation in plants, sense and respond to an array of plant host and bacterial signal molecules, and maintain and disseminate the plasmid among populations of agrobacteria. At the end of this review, we will describe how this natural genetic engineer has been adapted to spawn an entire industry of plant biotechnology and review its potential for use in future therapeutic applications of plant and nonplant species.

  • Citation: Gordon J, Christie P. 2014. The Ti Plasmids. Microbiol Spectrum 2(6):PLAS-0010-2013. doi:10.1128/microbiolspec.PLAS-0010-2013.

Key Concept Ranking

Type IV Secretion Systems
0.40731755
Type VI Secretion System
0.40652686
0.40731755

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116. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V. 2001. Genetic transformation of HeLa cells by Agrobacterium.Proc Natl Acad Sci USA 98:1871–1876. [PubMed][CrossRef]
117. Christie PJ. 2007. Agrobacterium and plant cell transformation. p 29–43. In Schaechter M (ed), Desk Encyclopedia of Microbiology, 2nd ed. Academic Press, San Diego, CA.
118. Laverde-Gomez JA, Sarkar MK, Christie PJ. 2012. Regulation of bacterial type IV secretion systems. p 335–362. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC.
119. Baxter JC, Funnell BE. 2014. Plasmid partition mechanisms. Microbiol Spectrum 2(5). doi:10.1128/microbiolspec.PLAS-0023-2014. [CrossRef]
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/content/journal/microbiolspec/10.1128/microbiolspec.PLAS-0010-2013
2014-11-21
2017-05-25

Abstract:

is a plant pathogen with the capacity to deliver a segment of oncogenic DNA carried on a large plasmid called the tumor-inducing or Ti plasmid to susceptible plant cells. belongs to the class , whose members include other plant pathogens (), plant and insect symbionts ( spp. and spp., respectively), human pathogens ( spp., spp., spp.), and nonpathogens (). Many species of carry large plasmids ranging in size from ∼100 kb to nearly 2 Mb. These large replicons typically code for functions essential for cell physiology, pathogenesis, or symbiosis. Most of these elements rely on a conserved gene cassette termed for replication and partitioning, and maintenance at only one or a few copies per cell ( 1 ). The subject of this review is the ∼200-kb Ti plasmids carried by infectious strains of . We will summarize the features of this plasmid as a representative of the family of megaplasmids. We will also describe novel features of this plasmid that enable cells to incite tumor formation in plants, sense and respond to an array of plant host and bacterial signal molecules, and maintain and disseminate the plasmid among populations of agrobacteria. At the end of this review, we will describe how this natural genetic engineer has been adapted to spawn an entire industry of plant biotechnology and review its potential for use in future therapeutic applications of plant and nonplant species.

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FIGURE 1

Schematic of octopine-type Ti plasmid pTiA6 showing locations of genes coding for plasmid maintenance (), infection of plant cells ( region, T-DNA), cell survival in the tumor environment (opine catabolism), and conjugative transfer of the Ti plasmid to recipient agrobacteria ( and ). The various contributions of the gene products to T-DNA transfer are listed. T-DNA and T-DNA are delimited by -like border sequences (black boxes; RB, right border; LB, left border); OD, sequence (white boxes) enhances VirD2 relaxase nicking at the T-DNA border sequences. When delivered to plant cells and integrated into the plant nuclear genome, T-DNAs code for biosynthesis of auxins and cytokinins, resulting in the proliferation of plant tissues, and production of opines that serve as nutrients for the infecting bacterium. (This figure has been adapted from reference 117 [Christie PJ, and Plant Cell Transformation, : , 2009], copyright 2009, with permission from Elsevier.) doi:10.1128/microbiolspec.PLAS-0010-2013.f1

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0010-2013
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FIGURE 2

Regulation of the operon of octopine-type Ti plasmids. Transcription of the operon is inhibited by autorepression mediated by RepA-RepB complexes at the operator region downstream of P4 (a region of dyad symmetry is denoted by inverted arrows) and at the partitioning () site located between and . Expression of is inhibited transcriptionally and posttranscriptionally by the countertranscribed RNA RepE. Tumor-inducing (Ti) plasmids are maintained as single copies in the absence of external signals. Additional regulation of Ti plasmid replication during the cell cycle may be provided by phosphorylated CtrA and by CcrM methylation at GANTC motifs within and upstream of . Sensory perception of two exogenous signals results in elevated transcription of the cassette and increased plasmid copy number. Plant-released phenolic compounds are detected by the VirA-VirG two-component system; Phospho-VirG binds a box to activate transcription from promoter P4. TraR–3-oxo-octanoylhomoserine lactone complexes bind boxes, activating the operon through promoters P1, P2, P3, and P4. (Adapted from reference 1 with permission from Macmillan Publishers Ltd. [Pinto UM, Pappas KM, Winans SC, The ABCs of plasmid replication and segregation. 755–765, 2012, doi:10.1038/nrmicro2882], copyright 2012.) doi:10.1128/microbiolspec.PLAS-0010-2013.f2

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0010-2013
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FIGURE 3

Schematic showing steps of type IV secretion, as presented for the Ti-encoded VirB/VirD4 transfer system. Step I: the DNA transfer and replication (Dtr) proteins bind the -like right border repeat sequence (Ti plasmid, red squares flanking T-DNA) to form the relaxosome. VirD2 relaxase nicks the T strand, which is then unwound from the template strand of the pTi plasmid. Step II: ParA-like VirC1 and VirD2, and probably other factors, mediate binding of the VirD2-T-strand transfer intermediate with the VirD4 substrate receptor or type IV coupling protein (T4CP). Step III: The transfer intermediate is translocated across the cell envelope through a secretion channel composed of the VirD4 T4CP and the VirB mating pair formation (Mpf) proteins. Effector proteins, e.g., VirE2, VirE3, VirF, also dock with VirD4 and then are delivered independently of the T-DNA through the secretion channel. Independently of VirD4, the VirB proteins also assemble into a conjugative pilus, which is used to establish contact with a susceptible target cell. IM, inner membrane; P, periplasm; OM, outer membrane. doi:10.1128/microbiolspec.PLAS-0010-2013.f3

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0010-2013
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FIGURE 4

Genetic organization of the Ti plasmid-encoded and operons. The genes and some of the known functions of the encoded products are presented at the top. This T4SS is closely related in operon organization and subunit composition to a T4SS encoded by the conjugative plasmid pKM101. The Trb system is closely related in operon organization and subunit composition to a T4SS encoded by the conjugative plasmid RP4. Genes encoding protein homologs are identically color-coded. doi:10.1128/microbiolspec.PLAS-0010-2013.f4

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0010-2013
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FIGURE 5

A schematic of chemical signaling events between cells and transformed plant cells. Signals released from wounded plant cells initiate the infection process through the VirA/VirG/ChvE sensory response system, resulting in activation of the Ti plasmid-encoded genes. The Vir proteins mediate T-DNA processing, assembly of the VirB/VirD4 T4SS, and T-DNA translocation to susceptible plant cells. VirA/VirG also induce expression of the Ti plasmid genes resulting in elevated Ti plasmid copy number. Opines released from transformed plant cells activate opine catabolism functions for growth of infecting bacteria. Opines also activate synthesis of TraR which in turn induces production of the TraI homoserine lactone (AHL) synthase. TraR and AHL at a critical concentration activate the Ti plasmid replication and conjugation functions resulting in elevated Ti plasmid copy number and dissemination to neighboring agrobacterial cells. TlrR and TraM negatively regulate TraR activity, and AiiB negatively controls AHL levels. Adapted from reference 118 . doi:10.1128/microbiolspec.PLAS-0010-2013.f5

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0010-2013
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