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Chapter 18 : Cell-Cell Signaling within Crown Gall Tumors

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Cell-Cell Signaling within Crown Gall Tumors, Page 1 of 2

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Abstract:

It has been 100 years since was demonstrated to cause crown gall tumors at plant wound sites. This chapter first presents background information relevant to quorum sensing in and then focuses on our current knowledge of the molecular biology of the TraR-TraI system. Regulation of TraR activity is complex and occurs at the levels of transcription, protein folding, resistance to proteolysis, and the formation of quaternary complexes with other TraR subunits or with two different antiactivators of TraR. Control of expression by opines therefore has evolved independently in these two types of Ti plasmids. The genes of the operon and operon are not similar, except for . LysR and AccR are also dissimilar, as OccR is a LysR-type transcriptional activator that binds to promoter DNA both in the presence and absence of the inducing signal. Overproduction of TraR can fully overcome inhibition, suggesting that TraM acts by making stoichiometric contacts with TraR. Direct interactions were confirmed by yeast two-hybrid assays and by far Western immunoblots. The author recently used gene arrays to profile the TraR transcriptome and found that all induced genes were Ti plasmid-encoded. These genes include the and genes, which are involved in conjugal transfer; the genes, which are required for vegetative replication and plasmid partitioning into daughter cells; and .

Citation: Winans S. 2008. Cell-Cell Signaling within Crown Gall Tumors, p 291-306. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch18

Key Concept Ranking

Genetic Elements
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Transcription Start Site
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Bacterial Proteins
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Nuclear Magnetic Resonance Spectroscopy
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Type IV Secretion Systems
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Figures

Image of FIGURE 1
FIGURE 1

A model of the quorum-sensing system in octopine-type Ti plasmids. TraR is expressed in response to the tumor-released nutrient octopine, whereas the TraR antiactivator TrlR is expressed in response to mannopine, which is also released from tumors. Apo-TraR is rapidly degraded by proteases but is rescued from proteolysis by binding OOHL, the quorum-sensing signal that is produced by TraI. TraR-OOHL dimers activate transcription of and the , and operons. TraR-OOHL complexes can be inactivated through direct interactions with TraM or TrlR. OOHL can be destroyed by the BlcC protein (formerly AttM).

Citation: Winans S. 2008. Cell-Cell Signaling within Crown Gall Tumors, p 291-306. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch18
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Image of FIGURE 2
FIGURE 2

A comparison of regulation via opines on different types of Ti plasmids. On octopine-type Ti plasmids, is activated by OccR in response to octopine. The TraR antiactivator TrlR is expressed in response to mannopine, probably via inactivation of the MocR repressor. On nopaline-type Ti plasmids, is expressed when AccR repression is relieved by agrocinopines A and B. Regulation of on the chrysopine-type plasmid is similar, except the inducing opines are agrocinopines C and D. There are two copies of on pAtK84b, one thought to be activated by NocR in response to nopaline, while the other is activated in response to agrocinopines A and B via derepression of AccR.

Citation: Winans S. 2008. Cell-Cell Signaling within Crown Gall Tumors, p 291-306. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch18
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Image of FIGURE 3
FIGURE 3

(A) Induction of the regulon using full-genome microarrays. Black circles indicate genes located on the circular or linear chromosome or on the cryptic Ti plasmid pAtC58, while gray circles indicate genes located on the octopine-type Ti plasmid pTiR10. The axis shows the range of expression in the absence of TraR, while the axis shows the range of expression when TraR is overproduced, which suffices to induce the entire regulon ( ). Note that virtually all Ti plasmid genes are expressed more strongly in the presence than in the absence of TraR, as TraR activates the operon, increasing Ti plasmid copy number. (B) Induction of the regulon using Ti plasmid microarrays. Open symbols represent non-Ti plasmid genes, while filled symbols represent Ti plasmid genes. The axis represents the range of gene expression in the absence of acetosyringone (AS), while the axis represents the range of expression in the presence of 100 μM AS. Note that all Ti plasmid genes are slightly induced by AS, as AS acts through VirG to activate the operon, increasing the Ti plasmid copy number.

Citation: Winans S. 2008. Cell-Cell Signaling within Crown Gall Tumors, p 291-306. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch18
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Image of FIGURE 4
FIGURE 4

Interactions between TraR and other regulators. (A) TraR and VirG both regulate the operon and therefore influence the Ti plasmid copy number. TraROOHL complexes bind to boxes II and III ( and ) to activate promoters P1, P2, and P3, as well as the divergent promoter P. P~VirG bind to a box () to activate promoter P4. Of these, P4 is active in the absence of either protein, causing a basal level of gene expression sufficient for low-level Ti plasmid replication. (B) RepA and RepB form a complex that binds to an operator directly downstream of promoter P4 and also binds to a site between and (not shown). Binding represses all four promoters of the operon. RepC is negatively regulated at the transcript elongation or translational level by a small antisense RNA encoded by the gene. (C) The divergent and operons are activated by TraR-OOHL complexes bound to the box I (). Both promoters are also repressed by the TraA protein bound to the origin of conjugal transfer (). TraA also processes one DNA strand at in a step that is essential for conjugation. TraC and TraD assist TraA in repression, in DNA processing, and in conjugation but are not essential for any of these events.

Citation: Winans S. 2008. Cell-Cell Signaling within Crown Gall Tumors, p 291-306. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch18
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References

/content/book/10.1128/9781555815578.ch18
1. Beck von Bodman, S.,, G. T. Hayman,, and S. K. Farrand. 1992. Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. Proc. Natl. Acad. Sci. USA 89:643647.
2. Binns, A. N.,, and P. Costantino. 1998. The Agrobacterium oncogenes, p. 251–266. In H. P. Spaink,, A. Kondorosi,, and P. J. Hooykaas (ed.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
3. Busby, S.,, and R. H. Ebright. 1999. Transcription activation by catabolite activator protein (CAP). J. Mol. Biol. 293:199213.
4. Carlier, A. L.,, and S. B. von Bodman. 2006. The rcsA promoter of Pantoea stewartii subsp. stewartii features a low-level constitutive promoter and an EsaR quorum-sensing-regulated promoter. J. Bacteriol. 188:45814584.
5. Chai, Y.,, and S. C. Winans. 2005. RepB protein of an Agrobacterium tumefaciens Ti plasmid binds to two adjacent sites between repA and repB for plasmid partitioning and autorepression. Mol. Microbiol. 58:11141129.
6. Chai, Y.,, and S. C. Winans. 2004. Site-directed mutagenesis of a LuxR-type quorum-sensing transcription factor: alteration of autoinducer specificity. Mol. Microbiol. 51:765776.
7. Chai, Y.,, and S. C. Winans. 2005. A small anti-sense RNA downregulates expression of an essential replicase protein of an Agrobacterium tumefaciens Ti plasmid. Mol. Microbiol. 56:15741585.
8. Chai, Y.,, J. Zhu,, and S. C. Winans. 2001. TrlR, a defective TraR-like protein of Agrobacterium tumefaciens, blocks TraR function in vitro by forming inactive TrlR:TraR dimers. Mol. Microbiol. 40:414421.
9. Chen, G.,, J. W. Malenkos,, M. R. Cha,, C. Fuqua,, and L. Chen. 2004. Quorum-sensing antiactivator TraM forms a dimer that dissociates to inhibit TraR. Mol. Microbiol. 52:16411651.
10. Reference deleted.
11. Cho, H.,, and S. C. Winans. 2007. TraA, TraC, and TraD autorepress two divergent quorum-regulated promoters near the transfer origin of the Ti plasmid of Agrobacterium tumefaciens. Mol. Microbiol. 63:17691782.
12. Cho, H.,, and S. C. Winans. 2005. VirA and VirG activate the Ti plasmid repABC operon, elevating plasmid copy number in response to wound-released chemical signals. Proc. Natl. Acad. Sci. USA 102:1484314848.
13. Ducros, V. M.,, R. J. Lewis,, C. S. Verma,, E. J. Dodson,, G. Leonard,, J. P. Turkenburg,, G. N. Murshudov,, A. J. Wilkinson,, and J. A. Brannigan. 2001. Crystal structure of GerE, the ultimate transcriptional regulator of spore formation in Bacillus subtilis. J. Mol. Biol. 306:759771.
14. Dyson, H. J.,, and P. E. Wright. 2002. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 12:5460.
15. Egland, K. A.,, and E. P. Greenberg. 2001. Quorum sensing in Vibrio fischeri: analysis of the LuxR DNA binding region by alanine-scanning mutagenesis. J. Bacteriol. 183:382386.
16. Ellis, J. G.,, A. Kerr,, A. Petit,, and J. Tempe. 1982. Conjugal transfer of nopaline and agropine Ti-plasmids—the role of agrocinopines. Mol. Gen. Genet. 186:269273.
17. Escobar, M. A.,, and A. M. Dandekar. 2003. Agrobacterium tumefaciens as an agent of disease. Trends Plant. Sci. 8:380386.
18. Fuqua, C.,, M. Burbea,, and S. C. Winans. 1995. Activity of the Agrobacterium Ti plasmid conjugal transfer regulator TraR is inhibited by the product of the traM gene. J. Bacteriol. 177:13671373.
19. Fuqua, C.,, and E. P. Greenberg. 2002. Listening in on bacteria: acylhomoserine lactone signalling. Nat. Rev. Mol. Cell. Biol. 3:685695.
20. Fuqua, C.,, and S. C. Winans. 1996. Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J. Bacteriol. 178:435440.
21. Fuqua, C.,, and S. C. Winans. 1996. Localization of OccR-activated and TraR-activated promoters that express two ABC-type permeases and the traR gene of Ti plasmid pTiR10. Mol. Microbiol. 20:11991210.
22. Fuqua, W. C.,, and S. C. Winans. 1994. A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J. Bacteriol. 176:27962806.
23. Gelvin, S. B. 2003. Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying”tool. Microbiol. Mol. Biol. Rev. 67:1637.
24. Genetello, C.,, N. Van Larebeke,, M. Holsters,, A. De Picker,, M. Van Montagu,, and J. Schell. 1977. Ti plasmids of Agrobacterium as conjugative plasmids. Nature 265:561563.
25. Goodner, B.,, G. Hinkle,, S. Gattung,, N. Miller,, M. Blanchard,, B. Qurollo,, B. S. Goldman,, Y. Cao,, M. Askenazi,, C. Halling,, L. Mullin,, K. Houmiel,, J. Gordon,, M. Vaudin,, O. Iartchouk,, A. Epp,, F. Liu,, C. Wollam,, M. Allinger,, D. Doughty,, C. Scott,, C. Lappas,, B. Markelz,, C. Flanagan,, C. Crowell,, J. Gurson,, C. Lomo,, C. Sear,, G. Strub,, C. Cielo,, and S. Slater. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:23232328.
26. He, X.,, W. Chang,, D. L. Pierce,, L. O. Seib,, J. Wagner,, and C. Fuqua. 2003. Quorum sensing in Rhizobium sp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate. J. Bacteriol. 185:809822.
27. Reference deleted.
28. Hwang, I.,, D. M. Cook,, and S. K. Farrand. 1995. A new regulatory element modulates homoserine lactone-mediated autoinduction of Ti plasmid conjugal transfer. J. Bacteriol. 177:449458.
29. Hwang, I.,, P. L. Li,, L. Zhang,, K. R. Piper,, D. M. Cook,, M. E. Tate,, and S. K. Farrand. 1994. TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. Proc. Natl. Acad. Sci. USA 91:46394643.
30. Hwang, I.,, A. J. Smyth,, Z. Q. Luo,, and S. K. Farrand. 1999. Modulating quorum sensing by antiactivation:TraM interacts with TraR to inhibit activation of Ti plasmid conjugal transfer genes. Mol. Microbiol. 34:282294.
31. Johnson, T. M.,, and A. Das. 1998. Organization and regulation of expression of the Agrobacterium virulence genes, p. 265–279. In H. P. Spaink,, A. Kondorosi,, and P. J. Hooykaas (ed.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
32. Jones, S.,, P. van Heyningen,, H. M. Berman,, and J. M. Thornton. 1999. Protein-DNA interactions: a structural analysis. J. Mol. Biol. 287:877896.
33. Kado, C. I. 1994. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis. Mol. Microbiol. 12:1722.
34. Kerr, A. 1971. Acquisition of virulence by nonpathogenic isolates of Agrobacterium radiobacter. Physiol. Plant Pathol. 1:241246.
35. Kerr, A. 1969. Transfer of virulence between isolates of Agrobacterium. Nature 223:11751176.
36. Kerr, A.,, P. Manigault,, and J. Tempe. 1977. Transfer of virulence in vivo and in vitro in Agrobacterium. Nature 265:560561.
37. Lessl, M.,, D. Balzer,, W. Pansegrau,, and E. Lanka. 1992. Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J. Biol. Chem. 267:2047120480.
38. Lessl, M.,, and E. Lanka. 1994. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77:321324.
39. Lewis, M. 2005. The lac repressor. C. R. Biol. 328:521548.
40. Luo, Z. Q.,, Y. Qin,, and S. K. Farrand. 2000. The antiactivator TraM interferes with the autoinducer-dependent binding of TraR to DNA by interacting with the C-terminal region of the quorum-sensing activator. J. Biol. Chem. 275:77137722.
41. Luo, Z. Q.,, A. J. Smyth,, P. Gao,, Y. Qin,, and S. K. Farrand. 2003. Mutational analysis of TraR. Correlating function with molecular structure of a quorum-sensing transcriptional activator. J. Biol. Chem. 278:1317313182.
42. Maris, A. E.,, M. R. Sawaya,, M. Kaczor-Grzeskowiak,, M. R. Jarvis,, S. M. Bearson,, M. L. Kopka,, I. Schroder,, R. P. Gunsalus,, and R. E. Dickerson. 2002. Dimerization allows DNA target site recognition by the NarL response regulator. Nat. Struct. Biol. 9:771778.
43. More, M. I.,, L. D. Finger,, J. L. Stryker,, C. Fuqua,, A. Eberhard,, and S. C. Winans. 1996. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:16551658.
44. Nelson, H. C. 1995. Structure and function of DNA-binding proteins. Curr. Opin. Genet. Dev. 5:180189.
45. Niu, W.,, Y. Kim,, G. Tau,, T. Heyduk,, and R. H. Ebright. 1996. Transcription activation at class II CAP-dependent promoters: two interactions between CAP and RNA polymerase. Cell 87:11231134.
46. Oger, P.,, and S. K. Farrand. 2001. Co-evolution of the agrocinopine opines and the agrocinopine-mediated control of TraR, the quorum-sensing activator of the Ti plasmid conjugation system. Mol. Microbiol. 41:11731185.
47. Oger, P.,, and S. K. Farrand. 2002. Two opines control conjugal transfer of an Agrobacterium plasmid by regulating expression of separate copies of the quorum-sensing activator gene traR. J. Bacteriol. 184:11211131.
48. Oger, P.,, K. S. Kim,, R. L. Sackett,, K. R. Piper,, and S. K. Farrand. 1998. Octopine-type Ti plasmids code for a mannopine-inducible dominant-negative allele of traR, the quorum-sensing activator that regulates Ti plasmid conjugal transfer. Mol. Microbiol. 27:277288.
49. Pappas, K. M.,, and S. C. Winans. 2003. A LuxR-type regulator from Agrobacterium tumefaciens elevates Ti plasmid copy number by activating transcription of plasmid replication genes. Mol. Microbiol. 48:10591073.
50. Pappas, K. M.,, and S. C. Winans. 2003. The RepA and RepB autorepressors and TraR play opposing roles in the regulation of a Ti plasmid repABC operon. Mol. Microbiol. 49:441455.
51. Piper, K. R.,, S. Beck von Bodman,, and S. K. Farrand. 1993. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362:448450.
52. Piper, K. R.,, S. Beck Von Bodman,, I. Hwang,, and S. K. Farrand. 1999. Hierarchical gene regulatory systems arising from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium. Mol. Microbiol. 32:10771089.
53. Pohlman, R. F.,, H. D. Genetti,, and S. C. Winans. 1994. Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol. Microbiol. 14:655668.
54. Qin, Y.,, Z. Q. Luo,, A. J. Smyth,, P. Gao,, S. Beck von Bodman,, and S. K. Farrand. 2000. Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm. EMBO J. 19:52125221.
55. Qin, Y.,, A. J. Smyth,, S. Su,, and S. K. Farrand. 2004. Dimerization properties of TraM, the antiactivator that modulates TraR-mediated quorum-dependent expression of the Ti plasmid tra genes. Mol. Microbiol. 53:14711485.
56. Shoemaker, B. A.,, J. J. Portman,, and P. G. Wolynes. 2000. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. USA 97:88688873.
57. Smith, E. F.,, and C. O. Townsend. 1907. A plant-tumor of bacterial origin. Science 24:671673.
58. Stachel, S. E.,, and P. C. Zambryski. 1986. virA and virG control the plant-induced activation of the T-DNA transfer process of A. tumefaciens. Cell 46:325333.
59. Swiderska, A.,, A. K. Berndtson,, M. R. Cha,, L. Li,, G. M. Beaudoin III,, J. Zhu,, and C. Fuqua. 2001. Inhibition of the Agrobacterium tumefaciens TraR quorum-sensing regulator. Interactions with the TraM anti-activator. J. Biol. Chem. 276:4944949458.
60. Reference deleted.
61. Van Larebeke, N.,, G. Engler,, M. Holsters,, S. Van den Elsacker,, I. Zaenen,, R. A. Schilperoort,, and J. Schell. 1974. Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature 252:169170.
62. Vannini, A.,, C. Volpari,, and S. Di Marco. 2004. Crystal structure of the quorum-sensing protein TraM and its interaction with the transcriptional regulator TraR. J. Biol. Chem. 279:2429124296.
63. Vannini, A.,, C. Volpari,, C. Gargioli,, E. Muraglia,, R. Cortese,, R. De Francesco,, P. Neddermann,, and S. D. Marco. 2002. The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 21:43934401.
64. von Bodman, S. B.,, J. K. Ball,, M. A. Faini,, C. M. Herrera,, T. D. Minogue,, M. L. Urbanowski,, and A. M. Stevens. 2003. The quorum sensing negative regulators EsaR and ExpR(Ecc), homologues within the LuxR family, retain the ability to function as activators of transcription. J. Bacteriol. 185:70017007.
65. Wang, L.,, J. D. Helmann,, and S. C. Winans. 1992. The A. tumefaciens transcriptional activator OccR causes a bend at a target promoter, which is partially relaxed by a plant tumor metabolite. Cell 69:659667.
66. White, C. E.,, and S. C. Winans. 2007. The quorum-sensing transcription factor TraR decodes its DNA binding site by direct contacts with DNA bases and by detection of DNA flexibility. Mol. Microbiol. 64:245256.
67. White, C. E.,, and S. C. Winans. 2005. Identification of amino acid residues of the Agrobacterium tumefaciens quorum-sensing regulator TraR that are critical for positive control of transcription. Mol. Microbiol. 55:14731486.
68. Whitehead, N. A.,, A. M. Barnard,, H. Slater,, N. J. Simpson,, and G. P. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365404.
69. Winans, S. C.,, R. A. Kerstetter,, and E. W. Nester. 1988. Transcriptional regulation of the virA and virG genes of Agrobacterium tumefaciens. J. Bacteriol. 170:40474054.
70. Reference deleted.
71. Wood, D. W.,, J. C. Setubal,, R. Kaul,, D. E. Monks,, J. P. Kitajima,, V. K. Okura,, Y. Zhou,, L. Chen,, G. E. Wood,, N. F. Almeida,, Jr., L. Woo,, Y. Chen,, I. T. Paulsen,, J. A. Eisen,, P. D. Karp,, D. Bovee,, Sr., P. Chapman,, J. Clendenning,, G. Deatherage,, W. Gillet,, C. Grant,, T. Kutyavin,, R. Levy,, M. J. Li,, E. McClelland,, A. Palmieri,, C. Raymond,, G. Rouse,, C. Saenphimmachak,, Z. Wu,, P. Romero,, D. Gordon,, S. Zhang,, H. Yoo,, Y. Tao,, P. Biddle,, M. Jung,, W. Krespan,, M. Perry,, B. Gordon-Kamm,, L. Liao,, S. Kim,, C. Hendrick,, Z. Y. Zhao,, M. Dolan,, F. Chumley,, S. V. Tingey,, J. F. Tomb,, M. P. Gordon,, M. V. Olson,, and E. W. Nester. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:23172323.
72. Yao, Y.,, M. A. Martinez-Yamout,, T. J. Dickerson,, A. P. Brogan,, P. E. Wright,, and H. J. Dyson. 2006. Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J. Mol. Biol. 355:262273.
73. Young, J. M.,, L. D. Kuykendall,, E. Martinez-Romero,, A. Kerr,, and H. Sawada. 2003. Classification and nomenclature of Agrobacterium and Rhizobium. Int. J. Syst. Evol. Microbiol. 53:16891695.
74. Zhang, L.,, P. J. Murphy,, A. Kerr,, and M. E. Tate. 1993. Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones. Nature 362:446448.
75. Zhang, R. G.,, T. Pappas,, J. L. Brace,, P. C. Miller,, T. Oulmassov,, J. M. Molyneaux,, J. C. Anderson,, J. K. Bashkin,, S. C. Winans,, and A. Joachimiak. 2002. Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971974.
76. Zhu, J.,, J. W. Beaber,, M. I. More,, C. Fuqua,, A. Eberhard,, and S. C. Winans. 1998. Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J. Bacteriol. 180:53985405.
77. Zhu, J.,, P. M. Oger,, B. Schrammeijer,, P. J. Hooykaas,, S. K. Farrand,, and S. C. Winans. 2000. The bases of crown gall tumorigenesis. J. Bacteriol. 182:38853895.
78. Zhu, J.,, and S. C. Winans. 1998. Activity of the quorum-sensing regulator TraR of Agrobacterium tumefaciens is inhibited by a truncated, dominant defective TraR-like protein. Mol. Microbiol. 27:289297.
79. Zhu, J.,, and S. C. Winans. 1999. Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc. Natl. Acad. Sci. USA 96:48324837.
80. Zhu, J.,, and S. C. Winans. 2001. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, pro-tease resistance, and dimerization. Proc. Natl. Acad. Sci. USA 98:15071512.

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