Journal of Microbiology and Biotechnology

  • 제16권11호
  • /
  • Pages.1661-1677
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  • 2006
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  • 1017-7825(pISSN)
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  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지

Rhizosphere Communication: Quorum Sensing by the Rhizobia

  • He, Xuesong (Department of Biology, Indiana University) ;
  • Fuqua, Clay (Department of Oral Biology, University of California Los Angeles)
  • 발행 : 2006.11.30
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초록

Rhizobium and related genera are soil bacteria with great metabolic plasticity. These microorganisms survive in many different environments and are capable of eliciting the formation of nitrogen-fixing nodules on legumes. The successful establishment of symbiosis is precisely regulated and requires a series of signal exchanges between the two partners. Quorum sensing (QS) is a prevalent form of population density-dependent gene regulation. Recently, increasing evidence indicates that rhizobial quorum sensing provides a pervasive regulatory network, which plays a more generalized role in the physiological activity of free-living rhizobia, as well as during symbiosis. Several rhizobia utilize multiple, overlapping quorum sensing systems to regulate diverse properties, including conjugal transfer and copy number control of plasmids, exopolysaccharide biosynthesis, rhizosphere-related functions, and cell growth. Genomic and proteomic analyses have begun to reveal the wide range of functions under quorum-sensing control.

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참고문헌

  1. Albus, A. M., E. C. Pesci, L. J. Runyen-Janecky, S. E. H. West, and B. H. Iglewski. 1997. Vfr controls quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179: 3928-3935 https://doi.org/10.1128/jb.179.12.3928-3935.1997
  2. Alt-Morbe, J., J. L. Stryker, C. Fuqua, P.-L. Li, S. K. Farrand, and S. C. Winans. 1996. The conjugal transfer system of Agrobacterium tumefaciens octopine-type Ti plasmids is closely related to the transfer system of an IncP plasmid and distantly related to Ti plasmid vir genes. J. Bacteriol. 178: 4248-4257 https://doi.org/10.1128/jb.178.14.4248-4257.1996
  3. Andersson, R. A., A. R. B. Eriksson, R. Heikinheimo, A. Mae, M. Pirhonen, V. Koiv, H. Hyytiainen, A. Tuikkala, and E. T. Palva. 2000. Quorum sensing in the plant pathogen Erwinia carotovora subsp carotovora: The role of expR (Ecc). Mol. Plant Microbe Interac. 13: 384-393 https://doi.org/10.1094/MPMI.2000.13.4.384
  4. Arcondeguy, T., I. Huez, J. Fourment, and D. Kahn. 1996. Symbiotic nitrogen fixation does not require adenylylation of glutamine synthetase I in Rhizobium meliloti. FEMS Microbiol. Lett. 145: 33-40 https://doi.org/10.1111/j.1574-6968.1996.tb08553.x
  5. Banfalvi, Z., E. Kondorosi, and A. Kondorosi. 1985. Rhizobium meliloti carries two megaplasmids. Plasmid 13: 129-138 https://doi.org/10.1016/0147-619X(85)90065-4
  6. Barloy-Hubler, F., D. Capela, J. Batut, and F. Galibert. 2000. High-resolution physical map of the pSymb megaplasmid and comparison of the three replicons of Sinorhizobium meliloti strain 1021. Curr. Microbiol. 41: 109-113 https://doi.org/10.1007/s002840010103
  7. Bassler, B. L., M. Wright, R. E. Showalter, and M. R. Silverman. 1993. Intercellular signalling in Vibrio harveyi: Sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9: 773-786 https://doi.org/10.1111/j.1365-2958.1993.tb01737.x
  8. Beynon, J. I., J. E. Beringer, and A. W. B. Johnston. 1980. Plasmids and host range in Rhizobium leguminosarum and Rhizobium phaseoli. J. Gen. Microbiol. 120: 421-429
  9. Bollinger, N., D. J. Hassett, B. H. Iglewski, J. W. Costerton, and T. R. McDermott. 2001. Gene expression in Pseudomonas aeruginosa: Evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J. Bacteriol. 183: 1990-1996 https://doi.org/10.1128/JB.183.6.1990-1996.2001
  10. Brom, S., A. Garcia-de los Santos, L. Cervantes, R. Palacios, and D. Romero. 2000. In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons. Plasmid 44: 34-43 https://doi.org/10.1006/plas.2000.1469
  11. Callahan, S. M. and P. V. Dunlap. 2000. LuxR- and acyl-homoserine-lactone-controlled non-lux genes define a quorum-sensing regulon in Vibrio fischeri. J. Bacteriol. 182: 2811-2822 https://doi.org/10.1128/JB.182.10.2811-2822.2000
  12. Carbonell, X., J. L. Corchero, R. Cubarsi, P. Vila, and A. Villaverde. 2002. Control of Escherichia coli growth rate through cell density. Microbiol. Res. 157: 257-265 https://doi.org/10.1078/0944-5013-00167
  13. Cheetham, B. F. and M. E. Katz. 1995. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol. Microbiol. 18: 201-208 https://doi.org/10.1111/j.1365-2958.1995.mmi_18020201.x
  14. Chen, G., J. Malenkos, M.-R. Cha, C. Fuqua, and L. Chen. 2004. Quorum-sensing anti-activator TraM forms a dimer that dissociates to inhibit TraR. Mol. Microbiol. 52: 1641-1651 https://doi.org/10.1111/j.1365-2958.2004.04110.x
  15. Chen, H., M. Batley, J. Redmond, and B. G. Rolfe. 1985. Alteration of the effective nodulation properties of a fast-growing broad host range Rhizobium due to changes in exopolysaccharide synthesis. J. Plant Physiol. 120: 331-349 https://doi.org/10.1016/S0176-1617(85)80132-2
  16. Chen, H., M. Teplitski, J. B. Robinson, B. G. Rolfe, and W. D. Bauer. 2003. Proteomic analysis of wild-type Sinorhizobium meliloti responses to N-acyl homoserine lactone quorum-sensing signals and the transition to stationary phase. J. Bacteriol. 185: 5029-5036 https://doi.org/10.1128/JB.185.17.5029-5036.2003
  17. Cheng, H.-P. and G. C. Walker. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180: 5183-5191
  18. Crossman, L. C. 2005. Plasmid replicons of Rhizobium. Biochem. Soc. Trans. 33: 157-158 https://doi.org/10.1042/BST0330157
  19. Cubo, M. T., A. Economou, G. Murphy, A. W. B. Johnston, and J. A. Downie. 1992. Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J. Bacteriol. 174: 4026-4035 https://doi.org/10.1128/jb.174.12.4026-4035.1992
  20. D'Haeze, W. and M. Holsters. 2002. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12: 79R-105R https://doi.org/10.1093/glycob/12.6.79R
  21. Daniels, R., D. E. De Vos, J. Desair, G. Raedschelders, E. Luyten, V. Rosemeyer, C. Verreth, E. Schoeters, J. Vanderleyden, and J. Michiels. 2002. Quorum-sensing in Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J. Biol. Chem. 277: 462-468 https://doi.org/10.1074/jbc.M106655200
  22. Danino, V. E., A. Wilkinson, A. Edwards, and J. A. Downie. 2003. Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol. Microbiol. 50: 511-525 https://doi.org/10.1046/j.1365-2958.2003.03699.x
  23. Denison, R. F. and E. T. Kiers. 2004. Lifestyle alternatives for rhizobia: Mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol. Lett. 237: 187-193 https://doi.org/10.1111/j.1574-6968.2004.tb09695.x
  24. Dessaux, Y., A. Petit, S. K. Farrand, and P. J. Murphy. 1998. Opines and opine-like molecules involved in plant-Rhizobiaceae interactions, pp. 173-197. In H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas (eds.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Press, Boston
  25. Dibb, N. J., J. A. Downie, and N. J. Brewin. 1984. Identification of a rhizosphere protein encoded by the symbiotic plasmid of Rhizobium leguminosarum. J. Bacteriol. 158: 621-627
  26. Diggle, S. P., K. Winzer, A. Lazdunski, P. Williams, and M. Camara. 2002. Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J. Bacteriol. 184: 2576-2586 https://doi.org/10.1128/JB.184.10.2576-2586.2002
  27. Djordjevic, M. A., J. W. Redmond, M. Batley, and B. G. Rolfe. 1987. Clovers secrete specific phenolic compounds which either stimulate or repress nod gene expression in Rhizobium trifolii. EMBO J. 6: 1173-1178
  28. Downie, J. A. and S. A. Walker. 1999. Plant responses to nodulation factors. Curr. Opin. Plant Biol. 2: 483-489 https://doi.org/10.1016/S1369-5266(99)00018-7
  29. Economou, A., F. K. L. Hawkins, J. A. Downie, and A. W. B. Johnston. 1989. Transcription of rhiA, a gene on a Rhizobium leguminosarum bv. viciae Sym plasmid, requires rhiR and is repressed by flavonoids that induce nod genes. Mol. Microbiol. 3: 87-93 https://doi.org/10.1111/j.1365-2958.1989.tb00107.x
  30. 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: 382-386 https://doi.org/10.1128/JB.183.1.382-386.2001
  31. Engebrecht, J., K. H. Nealson, and M. Silverman. 1983. Bacterial bioluminescence: Isolation and genetic analysis of the functions from Vibrio fischeri. Cell 32: 773-781 https://doi.org/10.1016/0092-8674(83)90063-6
  32. Engebrecht, J. and M. Silverman. 1984. Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA 81: 4154-4158
  33. Finan, T. M., A. M. Hirsch, J. A. Leigh, E. Johansen, G. A. Kuldan, S. Deegan, G. C. Walker, and E. R. Singer. 1985. Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40: 869-877 https://doi.org/10.1016/0092-8674(85)90346-0
  34. Fisher, R. F., T. T. Egelhoff, J. T. Mulligan, and S. R. Long. 1988. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev. 2: 282-293 https://doi.org/10.1101/gad.2.3.282
  35. Fisher, R. F. and S. R. Long. 1993. Interactions of NodD at the nod Box: NodD binds to two distinct sites on the same face of the helix and induces a bend in the DNA. J. Mol. Biol. 233: 336-348 https://doi.org/10.1006/jmbi.1993.1515
  36. Franssen, H. J., I. Vijn, W. C. Yang, and T. Bisseling. 1992. Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol. Biol. 19: 89-107 https://doi.org/10.1007/BF00015608
  37. Freiberg, C., R. Fellay, A. Balroch, W. J. Broughton, A. Rosenthal, and X. Perret. 1997. Molecular basis of symbiosis between Rhizobium and legumes. Nature 387: 394-401 https://doi.org/10.1038/387394a0
  38. 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: 1367-1373 https://doi.org/10.1128/jb.177.5.1367-1373.1995
  39. Fuqua, C. and A. Eberhard. 1999. Signal generation in autoinduction systems: Synthesis of acylated homoserine lactones by LuxI-type proteins, pp. 211-230. In G. M. Dunny and S. C. Winans (eds.), Cell-Cell Signaling in Bacteria. ASM Press, Washington, D.C
  40. Fuqua, C. and E. P. Greenberg. 2002. Listening in on bacteria: Acylhomoserine lactone signalling. Nature Rev. Mol. Cell Biol. 3: 685-695 https://doi.org/10.1038/nrm907
  41. 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: 435-440 https://doi.org/10.1128/jb.178.2.435-440.1996
  42. Fuqua, C. and S. C. Winans. 1996. Localization of the OccR-activated and TraR-activated promoters that express two ABC-type permeases and the traR gene of the Ti plasmid pTiR10. Mol. Microbiol. 20: 1199-1210 https://doi.org/10.1111/j.1365-2958.1996.tb02640.x
  43. 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: 2796-2806 https://doi.org/10.1128/jb.176.10.2796-2806.1994
  44. Fuqua, W. C., S. C. Winans, and E. P. Greenberg. 1994. Quorum sensing in bacteria: The LuxR/LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269-275 https://doi.org/10.1128/jb.176.2.269-275.1994
  45. Gage, D. J. 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68: 280-300 https://doi.org/10.1128/MMBR.68.2.280-300.2004
  46. Galibert, F., T. M. Finan, S. R. Long, A. Puhler, P. Abola, F. Ampe, F. Barloy-Hubler, M. J. Barnett, A. Becker, P. Boistard, G. Bothe, M. Boutry, L. Bowser, J. Buhrmester, E. Cadieu, D. Capela, P. Chain, A. Cowie, R. W. Davis, S. Dreano, N. A. Federspiel, R. F. Fisher, S. Gloux, T. Godrie, A. Goffeau, B. Golding, J. Gouzy, M. Gurjal, I. Hernandez-Lucas, A. Hong, L. Huizar, R. W. Hyman, T. Jones, D. Kahn, M. L. Kahn, S. Kalman, D. H. Keating, E. Kiss, C. Komp, V. Lelaure, D. Masuy, C. Palm, M. C. Peck, T. M. Pohl, D. Portetelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thebault, M. Vandenbol, F. J. Vorholter, S. Weidner, D. H. Wells, K. Wong, K. C. Yeh, and J. Batut. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293: 668-672 https://doi.org/10.1126/science.1060966
  47. Gao, M., H. Chen, A. Eberhard, M. R. Gronquist, J. B. Robinson, B. G. Rolfe, and W. D. Bauer. 2005. sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J. Bacteriol. 187: 7931-7944 https://doi.org/10.1128/JB.187.23.7931-7944.2005
  48. Gelvin, S. B. 2003. Agrobacterium-mediated plant transformation: The biology behind the 'gene-jockeying' tool. Microbiol. Mol. Biol. Rev. 67: 16-37 https://doi.org/10.1128/MMBR.67.1.16-37.2003
  49. Glazebrook, J. and G. C. Walker. 1989. A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell 56: 661-672 https://doi.org/10.1016/0092-8674(89)90588-6
  50. Gonzalez, J. E. and M. M. Marketon. 2003. Quorum sensing in nitrogen-fixing rhizobia. Microbiol. Mol. Biol. Rev. 67: 574-592 https://doi.org/10.1128/MMBR.67.4.574-592.2003
  51. Gonzalez, J. E., G. M. York, and G. C. Walker. 1996. Rhizobium meliloti exopolysaccharides: Synthesis and symbiotic function. Gene 179: 141-146 https://doi.org/10.1016/S0378-1119(96)00322-8
  52. 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: 2323-2328 https://doi.org/10.1126/science.1066803
  53. Gottfert, M., S. Rothlisberger, C. Kundig, C. Beck, R. Marty, and H. Hennecke. 2001. Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J. Bacteriol. 183: 1405-1412 https://doi.org/10.1128/JB.183.4.1405-1412.2001
  54. Gould, T. A., H. P. Schweizer, and M. E. Churchill. 2004. Structure of the Pseudomonas aeruginosa acyl-homoserine lactone synthase LasI. Mol. Microbiol. 53: 1135-1146 https://doi.org/10.1111/j.1365-2958.2004.04211.x
  55. Gray, K. M., J. P. Pearson, J. A. Downie, B. E. A. Boboye, and E. P. Greenberg. 1996. Cell-to-cell signalling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: Autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372-376 https://doi.org/10.1128/jb.178.2.372-376.1996
  56. Gussin, G. N., C. W. Ronson, and F. M. Ausubel. 1986. Regulation of nitrogen fixation genes. Annu. Rev. Genet. 20: 567-591 https://doi.org/10.1146/annurev.ge.20.120186.003031
  57. Hanzelka, B. L., M. R. Parsek, D. L. Val, P. V. Dunlap, J. E. Cronan Jr., and E. P. Greenberg. 1999. Acylhomoserine lactone synthase activity of the Vibrio fischeri AinS protein. J. Bacteriol. 181: 5766-5770
  58. 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: 809-822 https://doi.org/10.1128/JB.185.3.809-822.2003
  59. Hentzer, M., H. Wu, J. B. Andersen, K. Riedel, T. B. Rasmussen, N. Bagge, N. Kumar, M. A. Schembri, Z. Song, P. Kristoffersen, M. Manefield, J. W. Costerton, S. Molin, L. Eberl, P. Steinberg, S. Kjelleberg, N. Hoiby, and M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22: 3803-3815 https://doi.org/10.1093/emboj/cdg366
  60. Hirsch, A. M., M. R. Lum, and J. A. Downie. 2001. What makes the rhizobia-legume symbiosis so special? Plant Physiol. 127: 1484-1492 https://doi.org/10.1104/pp.010866
  61. Hirsch, P. R. 1979. Plasmid-determined bacteriocin production by Rhizobium leguminosarum. J. Gen. Microbiol. 113: 219-228 https://doi.org/10.1099/00221287-113-2-219
  62. Hoang, H. H., A. Becker, and J. E. Gonzalez. 2004. The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J. Bacteriol. 186: 5460-5472 https://doi.org/10.1128/JB.186.16.5460-5472.2004
  63. 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: 449-458 https://doi.org/10.1128/jb.177.2.449-458.1995
  64. 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: 4639-4643
  65. Kaneko, T., Y. Nakamura, S. Sato, E. Asamizu, T. Kato, S. Sasamoto, A. Watanabe, K. Idesawa, A. Ishikawa, K. Kawashima, T. Kimura, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, Y. Mochizuki, S. Nakayama, N. Nakazaki, S. Shimpo, M. Sugimoto, C. Takeuchi, M. Yamada, and S. Tabata. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7: 331-338 https://doi.org/10.1093/dnares/7.6.331
  66. Kaplan, H. B. and E. P. Greenberg. 1985. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J. Bacteriol. 163: 1210-1214
  67. Khan, S. R., D. V. Mavrodi, G. J. Jog, H. Suga, L. S. Thomashow, and S. K. Farrand. 2005. Activation of the phz operon of Pseudomonas fluorescens 2-79 requires the LuxR homolog PhzR, N-(3-OH-hexanoyl)-$_L$-homoserine lactone produced by the LuxI homolog PhzI, and a cis-acting phz box. J. Bacteriol. 187: 6517-6527 https://doi.org/10.1128/JB.187.18.6517-6527.2005
  68. Kiratisin, P., K. D. Tucker, and L. Passador. 2002. LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J. Bacteriol. 184: 4912-4919 https://doi.org/10.1128/JB.184.17.4912-4919.2002
  69. Kovach, M. E., M. D. Shaffer, and K. M. Peterson. 1996. A putative integrase gene defines the distal end of a large cluster of ToxR-regulated colonization genes in Vibrio cholerae. Microbiology 142: 2165-2174 https://doi.org/10.1099/13500872-142-8-2165
  70. Kwon, S. W., J. Y. Park, J. K. Kim, J. W. Kang, Y. H. Cho, C. K. Lim, M. A. Parker, and G. B. Lee. 2005. Phylogenetic analysis of the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the basis of 16S rRNA gene and internally transcribed spacer region sequences. Int. J. Sys. Evol. Microbiol. 55: 263-270 https://doi.org/10.1099/ijs.0.63097-0
  71. Lanka, E. and B. M. Wilkins. 1995. DNA processing reactions in bacterial conjugation. Annu. Rev. Biochem. 64: 141-169 https://doi.org/10.1146/annurev.bi.64.070195.001041
  72. Latifi, A., M. Foglino, K. Tanaka, P. Williams, and A. Lazdunski. 1996. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21: 1137-1146 https://doi.org/10.1046/j.1365-2958.1996.00063.x
  73. Laue, B. E., Y. Jiang, S. R. Chhabra, S. Jacob, G. S. A. B. Stewart, A. Hardman, J. A. Downie, F. O'Gara, and P. Williams. 2000. The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecanoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146: 2469-2480 https://doi.org/10.1099/00221287-146-10-2469
  74. Leigh, J. A. and D. L. Coplin. 1992. Exopolysaccharides in plant-bacterial interactions. Annu. Rev. Microbiol. 46: 307-346 https://doi.org/10.1146/annurev.mi.46.100192.001515
  75. Leigh, J. A. and C. C. Lee. 1988. Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules. J. Bacteriol. 170: 3327-3332 https://doi.org/10.1128/jb.170.8.3327-3332.1988
  76. Li, P.-L. and S. K. Farrand. 2000. The replicator of the nopaline-type Ti plasmid pTiC58 is a member of the repABC family and is influenced by the TraR-dependent quorum-sensing regulatory system. J. Bacteriol. 182: 179-188 https://doi.org/10.1128/JB.182.1.179-188.2000
  77. Lithgow, J. K., A. Wilkinson, A. Hardman, B. Rodelas, F. Wisniewski-Dye, P. Williams, and J. A. Downie. 2000. The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol. Microbiol. 37: 81-97 https://doi.org/10.1046/j.1365-2958.2000.01960.x
  78. Loh, J., R. W. Carlson, W. S. York, and G. Stacey. 2002. Bradyoxetin, a unique chemical signal involved in symbiotic gene regulation. Proc. Natl. Acad. Sci. USA 99: 14446-14451
  79. Loh, J., D. P. Lohar, B. Andersen, and G. Stacey. 2002. A two-component regulator mediates population-density-dependent expression of the Bradyrhizobium japonicum nodulation genes. J. Bacteriol. 184: 1759-1766 https://doi.org/10.1128/JB.184.6.1759-1766.2002
  80. Marketon, M. M., S. A. Glenn, A. Eberhard, and J. E. Gonzalez. 2003. Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J. Bacteriol. 185: 325-331 https://doi.org/10.1128/JB.185.1.325-331.2003
  81. Marketon, M. M. and J. E. Gonzalez. 2002. Identification of two quorum-sensing systems in Sinorhizobium meliloti. J. Bacteriol. 184: 3466-3475 https://doi.org/10.1128/JB.184.13.3466-3475.2002
  82. Marketon, M. M., M. R. Gronquist, A. Eberhard, and J. E. Gonzalez. 2002. Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J. Bacteriol. 184: 5686-5695 https://doi.org/10.1128/JB.184.20.5686-5695.2002
  83. Mercado-Blanco, J. and N. Toro. 1996. Plasmids in rhizobia: The role of non-symbiotic plasmids. Mol. Plant-Microbe Interact. 9: 535-545 https://doi.org/10.1094/MPMI-9-0535
  84. Miller, R. W., D. G. McRae, A. Al-Jobore, and W. B. Berndt. 1988. Respiration supported nitrogenase activity of isolated Rhizobium meliloti bacteroids. J. Cell. Biochem. 38: 35-49 https://doi.org/10.1002/jcb.240380105
  85. Milton, D. L., V. J. Chalker, D. Kirke, A. Hardman, M. Camara, and P. Williams. 2001. The LuxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-hydroxyhexanoyl)homoserine lactone and N-hexanoylhomoserine lactone. J. Bacteriol. 183: 3537-3547 https://doi.org/10.1128/JB.183.12.3537-3547.2001
  86. Minogue, T. D., M. Wehland-von Trebra, F. Bernhard, and S. Beck von Bodman. 2002. The autoregulatory role of EsaR, a quorum sensing regulator in Pantoea stewartii subsp. stewartii: Evidence for a repressor function. Mol. Microbiol. 44: 1625-1635 https://doi.org/10.1046/j.1365-2958.2002.02987.x
  87. 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: 1655-1658 https://doi.org/10.1126/science.272.5268.1655
  88. Morrison, N. A., C. Y. Hau, M. J. Trinick, J. Shine, and B. G. Rolfe. 1983. Heat curing of a Sym plasmid in a fast-growing Rhizobium sp. that is able to nodulate legumes and the nonlegume Parasponia sp. J. Bacteriol. 153: 527-531
  89. Morrison, N. A., Y. H. Cen, H. C. Chen, J. Plazinski, R. Ridge, and B. G. Rolfe. 1984. Mobilization of a Sym plasmid from a fast-growing cowpea Rhizobium strain. J. Bacteriol. 160: 483-487
  90. Murphy, P. J., N. Heycke, Z. Banfalvi, M. E. Tate, F. de Bruijn, A. Kondorosi, J. Tempe, and J. Schell. 1987. Genes for the catabolism and synthesis of an opine-like compound in Rhizobium meliloti are closely linked and on the Sym plasmid. Proc. Natl. Acad. Sci. USA 84: 493-497
  91. Oresnik, I. J., S.-L. Liu, C. K. Yost, and M. F. Hynes. 2000. Megaplasmid pRme2011a of Sinorhizobium meliloti is not required for viability. J. Bacteriol. 182: 3582-3586 https://doi.org/10.1128/JB.182.12.3582-3586.2000
  92. 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: 1059-1073 https://doi.org/10.1046/j.1365-2958.2003.03488.x
  93. Parsek, M. R. and E. P. Greenberg. 2000. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: A signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. USA 97: 8789-8793
  94. Pellock, B. J., H.-P. Cheng, and G. C. Walker. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182: 4310-4318 https://doi.org/10.1128/JB.182.15.4310-4318.2000
  95. Pellock, B. J., M. Teplitski, R. P. Boinay, W. D. Bauer, and G. C. Walker. 2002. A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 184: 5067-5076 https://doi.org/10.1128/JB.184.18.5067-5076.2002
  96. Perret, X., C. Staehelin, and W. J. Broughton. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64: 180-201 https://doi.org/10.1128/MMBR.64.1.180-201.2000
  97. Phillips, D. A. and Y. Kapulnik. 1995. Plant isoflavonoids, pathogens and symbionts. Trends Microbiol. 3: 58-64 https://doi.org/10.1016/S0966-842X(00)88876-9
  98. 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: 448-450 https://doi.org/10.1038/362448a0
  99. 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: 1077-1089 https://doi.org/10.1046/j.1365-2958.1999.01422.x
  100. Piper, K. R. and S. K. Farrand. 2000. Quorum sensing but not autoinduction of Ti plasmid conjugal transfer requires control by the opine regulon and the antiactivator TraM. J. Bacteriol. 182: 1080-1088 https://doi.org/10.1128/JB.182.4.1080-1088.2000
  101. Pongsilp, N., E. Triplett, and M. Sadowsky. 2005. Detection of homoserine lactone-like quorum sensing molecules in Bradyrhizobium strains. Curr. Microbiol. 51: 250-254 https://doi.org/10.1007/s00284-005-4550-5
  102. Preisig, O., D. Anthamatten, and H. Hennecke. 1993. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. USA 90: 3309-3313
  103. Ramirez-Romero, M. A., N. Soberon, A. Perez-Oseguera, J. Tellez-Sosa, and M. A. Cevallos. 2000. Structural elements required for replication and incompatibility of the Rhizobium etli symbiotic plasmid. J. Bacteriol. 182: 3117-3124 https://doi.org/10.1128/JB.182.11.3117-3124.2000
  104. Reverchon, S., M. L. Bouillant, G. Salmond, and W. Nasser. 1998. Integration of the quorum-sensing system in the regulatory networks controlling virulence factor synthesis in Erwinia chrysanthemi. Mol. Microbiol. 29: 1407-1418 https://doi.org/10.1046/j.1365-2958.1998.01023.x
  105. Rhodius, V. A. and S. J. W. Busby. 1998. Positive activation of gene expression. Curr. Opin. Microbiol. 1: 152-159 https://doi.org/10.1016/S1369-5274(98)80005-2
  106. Rodelas, B., J. K. Lithgow, F. Wisniewski-Dye, A. Hardman, A. Wilkinson, A. Economou, P. Williams, and J. A. Downie. 1999. Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 181: 3816-3823
  107. Rosemeyer, V., J. Michiels, C. Verreth, and J. Vanderleyden. 1998. luxI- and luxR-homologous genes of Rhizobium etli CNPAF512 contribute to synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J. Bacteriol. 180: 815-821
  108. Schaefer, A. L., D. L. Val, B. L. Hanzelka, J. E. Cronan Jr., and E. P. Greenberg. 1996. Generation of cell-to-cell signals in quorum sensing: Acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA 93: 9505-9509
  109. Schripsema, J., K. E. E. de Rudder, T. B. van Vliet, P. P. Lankhorst, E. de Vroom, J. W. Kijne, and A. A. N. van Brussel. 1996. Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-$_L$-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J. Bacteriol. 178: 366-371 https://doi.org/10.1128/jb.178.2.366-371.1996
  110. Schuster, M., C. P. Lostroh, T. Ogi, and E. P. Greenberg. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: A transcriptome analysis. J. Bacteriol. 185: 2066-2079 https://doi.org/10.1128/JB.185.7.2066-2079.2003
  111. Schuster, M., M. L. Urbanowski, and E. P. Greenberg. 2004. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc. Natl. Acad. Sci. USA 101: 15833-15839
  112. Shapiro, J. 1988. Bacteria as multicellular organisms. Sci. Am. 265: 82-89 https://doi.org/10.1038/scientificamerican1091-82
  113. Shapiro, J. A. 1998. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52: 81-104 https://doi.org/10.1146/annurev.micro.52.1.81
  114. Spaink, H. P., A. Kondorosi, and P. J. J. Hooykaas. 1998. The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Boston
  115. Stevens, A. M., N. Fujita, A. Ishihama, and E. P. Greenberg. 1999. Involvement of the RNA polymerase alpha-subunit C-terminal domain in LuxR-dependent activation of the Vibrio fischeri luminescence genes. J. Bacteriol. 181: 4704-4707
  116. Stevens, A. M. and E. P. Greenberg. 1999. Transcriptional activation by LuxR, pp. 231-242. In G. M. Dunny and S. C. Winans (eds.), Cell-Cell Signaling in Bacteria. ASM Press, Washington, D.C
  117. Sullivan, J. T., H. N. Patrick, W. L. Lowther, D. B. Scott, and C. W. Ronson. 1995. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc. Natl. Acad. Sci. USA 92: 8985-8989
  118. Sullivan, J. T. and C. W. Ronson. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci. USA 95: 5145-5149
  119. Swiderska, A., A. K. Berndtson, M.-R. Cha, L. Li, G. M. J. I. Beaudoin, 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: 49449-49458 https://doi.org/10.1074/jbc.M107881200
  120. Thomas, C. M. 2000. Paradigms of plasmid organization. Mol. Microbiol. 37: 485-491 https://doi.org/10.1046/j.1365-2958.2000.02006.x
  121. Truchet, G., P. Roche, P. Lerouge, J. Vasse, S. Camut, F. de Billy, J.-C. Prome, and J. Denarie. 1991. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670-673 https://doi.org/10.1038/351670a0
  122. Tun-Garrido, C., P. Bustos, V. Gonzalez, and S. Brom. 2003. Conjugative transfer of p42a from Rhizobium etli CFN42, which is required for mobilization of the symbiotic plasmid, is regulated by quorum sensing. J. Bacteriol. 185: 1681-1692 https://doi.org/10.1128/JB.185.5.1681-1692.2003
  123. Tyerman, S. D., L. F. Whitehead, and D. A. Day. 1995. A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature 378: 629-632 https://doi.org/10.1038/378629a0
  124. Udvardi, M. K., G. D. Price, P. M. Gresshoff, and D. A. Day. 1988. A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett. 231: 36-40 https://doi.org/10.1016/0014-5793(88)80697-5
  125. van Delden, C., R. Comte, and A. M. Bally. 2001. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J. Bacteriol. 183: 5376-5384 https://doi.org/10.1128/JB.183.18.5376-5384.2001
  126. Vannini, A., C. Volpari, C. Gargiola, E. Muraglia, R. Cortese, R. De Francesco, P. Nedderman, and S. Di Marco. 2002. The crystal structure of the quorum-sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 21: 1-9 https://doi.org/10.1093/emboj/21.1.1
  127. Visick, K. L. and C. Fuqua. 2005. Decoding microbial chatter: Cell-cell communication in bacteria. J. Bacteriol. 187: 5507-5519 https://doi.org/10.1128/JB.187.16.5507-5519.2005
  128. Wagner, V. E., D. Bushnell, L. Passador, A. I. Brooks, and B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: Effects of growth phase and environment. J. Bacteriol. 185: 2080-2095 https://doi.org/10.1128/JB.185.7.2080-2095.2003
  129. Wang, H., Z. Zhong, T. Cai, S. Li, and J. Zhu. 2004. Heterologous overexpression of quorum-sensing regulators to study cell-density-dependent phenotypes in a symbiotic plant bacterium Mesorhizobium huakuii. Arch. Microbiol. 182: 520-525 https://doi.org/10.1007/s00203-004-0735-8
  130. Wang, L.-X., Y. Wang, B. Pellock, and G. C. Walker. 1999. Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181: 6788-6796
  131. Waters, C. M. and B. L. Bassler. 2005. Quorum sensing: Cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319-346 https://doi.org/10.1146/annurev.cellbio.21.012704.131001
  132. Watson, W. T., T. D. Minogue, D. L. Val, S. Beck von Bodman, and M. E. A. Churchill. 2002. Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol. Cell. 9: 1-20 https://doi.org/10.1016/S1097-2765(02)00437-9
  133. 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: 1473-1486 https://doi.org/10.1111/j.1365-2958.2004.04482.x
  134. Whitehead, N. A., A. M. L. Barnard, H. Slater, N. J. L. Simpson, and G. P. C. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25: 365-404 https://doi.org/10.1111/j.1574-6976.2001.tb00583.x
  135. Wijffelman, C. A., E. Pees, A. A. N. van Brussel, and P. J. J. Hooykaas. 1983. Repression of small bacteriocin excretion in Rhizobium leguminosarum and Rhizobium trifolii by transmissible plasmids. Mol. Gen. Genet. 192: 171-176 https://doi.org/10.1007/BF00327663
  136. Wilkinson, A., V. Danino, F. Wisniewski-Dye, J. K. Lithgow, and J. A. Downie. 2002. N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J. Bacteriol. 184: 4510-4519 https://doi.org/10.1128/JB.184.16.4510-4519.2002
  137. Wisniewski-Dye, F. and J. A. Downie. 2002. Quorum-sensing in Rhizobium. Antonie Van Leeuwehoek 81: 397-407 https://doi.org/10.1023/A:1020501104051
  138. Wisniewski-Dye, F., J. Jones, S. R. Chhabra, and J. A. Downie. 2002. raiIR genes are part of a quorum-sensing network controlled by cinI and cinR in Rhizobium leguminosarum. J. Bacteriol. 184: 1597-1606 https://doi.org/10.1128/JB.184.6.1597-1606.2002
  139. Wood, D. W., J. C. Setulab, R. Kaul, D. E. Monks, J. P. Kitajima, V. K. Okura, Y. Zhou, L. Chen, G. E. Wood, N. F. J. Almeida, L. Woo, Y. Chen, I. T. Paulsen, J. A. Eisen, P. D. Karp, D. S. Dovee, P. Chapman, J. Clendenning, G. Deatherage, W. Gillet, C. Grant, T. Kutyavin, R. Levy, M.-J. Li, E. McClellund, 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. Gordon, M. V. Olson, and E. W. Nester. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323 https://doi.org/10.1126/science.1066804
  140. Workum, W. A. T., S. V. Slageren, A. A. N. van Brussel, and J. W. Kijne. 1998. Role of exopolysaccarides of Rhizobium leguminosarum bv. viciae as host plant-specific molecules required for infection thread formation during nodulation of Vicia sativa. Mol. Plant Microbe Interac. 11: 1233-1241 https://doi.org/10.1094/MPMI.1998.11.12.1233
  141. 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 autoinducer-type pheromone and DNA. Nature 417: 971-974 https://doi.org/10.1038/nature00833
  142. 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: 4832-4837
  143. Zhu, J. and S. C. Winans. 2001. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc. Natl. Acad. Sci. USA 98: 1507-1512