Intercellular and intracellular signalling systems that globally control the expression of virulence genes in plant pathogenic bacteria

Molecular Plant Pathology

Volumn 14, Issue 3, 2013, Pages 308-322

  Ham, Jong Hyun ^a  

^a LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GAMMA BUTYROLACTONE DERIVATIVE;

ALPHAPROTEOBACTERIA; BETAPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENETICS; METABOLISM; PATHOGENICITY; PHYSIOLOGY; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION; VIRULENCE;

ACYL-BUTYROLACTONES; ALPHAPROTEOBACTERIA; BACTERIAL PROTEINS; BETAPROTEOBACTERIA; GAMMAPROTEOBACTERIA; QUORUM SENSING; SIGNAL TRANSDUCTION; VIRULENCE;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; GAMMAPROTEOBACTERIA; NEGIBACTERIA; XANTHOMONAS; XANTHOMONAS ORYZAE; XANTHOMONAS ORYZAE PV. ORYZAE; XYLELLA FASTIDIOSA;

EID: 84874706142     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12005     Document Type: Review

References (138)

1. Aguilar, C., Bertani, I. and Venturi, V. (2003a) Quorum-sensing system and stationary-phase sigma factor (RpoS) of the onion pathogen Burkholderia cepacia genomovar I type strain, ATCC 25416. Appl. Environ. Microbiol. 69, 1739-1747.
2. Aguilar, C., Friscina, A., Devescovi, G., Kojic, M. and Venturi, V. (2003b) Identification of quorum-sensing-regulated genes of Burkholderia cepacia. J. Bacteriol. 185, 6456-6462.
3. Almeida, R.P., Killiny, N., Newman, K.L., Chatterjee, S., Ionescu, M. and Lindow, S. (2012) Contribution of rpfB to cell-cell signal synthesis, virulence, and vector transmission of Xylella fastidiosa. Mol. Plant-Microbe Interact. 25, 453-462.
4. Amikam, D. and Benziman, M. (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J. Bacteriol. 171, 6649-6655.
5. Andersson, R.A., Eriksson, A.R., Heikinheimo, R., Mae, A., Pirhonen, M., Koiv, V., Hyytiainen, H., Tuikkala, A. and Palva, E.T. (2000) Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expREcc. Mol. Plant- Microbe Interact. 13, 384-393.
6. Andrade, M.O., Alegria, M.C., Guzzo, C.R., Docena, C., Rosa, M.C., Ramos, C.H. and Farah, C.S. (2006) The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol. Microbiol. 62, 537-551.
7. Antunes, L.C., Ferreira, R.B., Buckner, M.M. and Finlay, B.B. (2010) Quorum sensing in bacterial virulence. Microbiology, 156, 2271-2282.
8. Barber, C.E., Tang, J.L., Feng, J.X., Pan, M.Q., Wilson, T.J., Slater, H., Dow, J.M., Williams, P. and Daniels, M.J. (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol. Microbiol. 24, 555-566.
9. Bassler, B.L. and Losick, R. (2006) Bacterially speaking. Cell, 125, 237-246.
10. Bassler, B.L., Wright, M. and Silverman, M.R. (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13, 273-286.
11. Bent, A.F. and Mackey, D. (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436.
12. Bi, H., Christensen, Q.H., Feng, Y., Wang, H. and Cronan, J.E. (2012) The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional homologue having both dehydratase and thioesterase activities. Mol. Microbiol. 83, 840-855.
13. von Bodman, S.B., Majerczak, D.R. and Coplin, D.L. (1998) A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA, 95, 7687-7692.
14. Burdette, D.L., Monroe, K.M., Sotelo-Troha, K., Iwig, J.S., Eckert, B., Hyodo, M., Hayakawa, Y. and Vance, R. (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature, 478, 515-518.
15. Burr, T., Barnard, A.M., Corbett, M.J., Pemberton, C.L., Simpson, N.J. and Salmond, G.P. (2006) Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol. Microbiol. 59, 113-125.
16. Cao, J.G. and Meighen, E.A. (1989) Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J. Biol. Chem. 264, 21 670-21 676.
17. Carlier, A., Chevrot, R., Dessaux, Y. and Faure, D. (2004) The assimilation of gammabutyrolactone in Agrobacterium tumefaciens C58 interferes with the accumulation of the N-acyl-homoserine lactone signal. Mol. Plant-Microbe Interact. 17, 951-957.
18. Chai, Y., Zhu, J. and Winans, S.C. (2001) TrlR, a defective TraR-like protein of Agrobacterium tumefaciens, blocks TraR function in vitro by forming inactive TrlR:TraR dimers. Mol. Microbiol. 40, 414-421.
19. Chai, Y., Tsai, C.S., Cho, H. and Winans, S.C. (2007) Reconstitution of the biochemical activities of the AttJ repressor and the AttK, AttL, and AttM catabolic enzymes of Agrobacterium tumefaciens. J. Bacteriol. 189, 3674-3679.
20. Chatterjee, S. and Sonti, R.V. (2002) rpfF mutants of Xanthomonas oryzae pv. oryzae are deficient for virulence and growth under low iron conditions. Mol. Plant-Microbe Interact. 15, 463-471.
21. Chatterjee, S., Newman, K.L. and Lindow, S.E. (2008a) Cell-to-cell signaling in Xylella fastidiosa suppresses movement and xylem vessel colonization in grape. Mol. Plant-Microbe Interact. 21, 1309-1315.
22. Chatterjee, S., Wistrom, C. and Lindow, S.E. (2008b) A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proc. Natl. Acad. Sci. USA, 105, 2670-2675.
23. Chen, R., Barphagha, I.K., Karki, H.S. and Ham, J.H. (2012) Dissection of quorumsensing genes in Burkholderia glumae reveals non-canonical regulation and the new regulatory gene tofM for toxoflavin production. PLoS ONE. In press.
24. Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B.L. and Hughson, F.M. (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature, 415, 545-549.
25. Cheng, Z., He, Y.W., Lim, S.C., Qamra, R., Walsh, M.A., Zhang, L.H. and Song, H. (2010) Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure, 18, 1199-1209.
26. Chin, K.H., Lee, Y.C., Tu, Z.L., Chen, C.H., Tseng, Y.H., Yang, J.M., Ryan, R.P., McCarthy, Y., Dow, J.M., Wang, A.H. and Chou, S.H. (2010) The cAMP receptorlike protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J. Mol. Biol. 396, 646-662.
27. Colnaghi Simionato, A.V., da Silva, D.S., Lambais, M.R. and Carrilho, E. (2007) Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EIMS. J. Mass Spectrom. 42, 490-496.
28. Corrigan, R.M., Abbott, J.C., Burhenne, H., Kaever, V. and Grundling, A. (2011) c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog. 7, e1002217.
29. Cotter, P.A. and Stibitz, S. (2007) c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10, 17-23.
30. Coulthurst, S.J., Lilley, K.S. and Salmond, G.P. (2006) Genetic and proteomic analysis of the role of luxS in the enteric phytopathogen, Erwinia carotovora. Mol. Plant Pathol. 7, 31-45.
31. Cui, Y., Chatterjee, A., Hasegawa, H., Dixit, V., Leigh, N. and Chatterjee, A.K. (2005) ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J. Bacteriol. 187, 4792-4803.
32. Cui, Y., Chatterjee, A., Hasegawa, H. and Chatterjee, A.K. (2006) Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals. J. Bacteriol. 188, 4715-4726.
33. Deng, Y., Boon, C., Eberl, L. and Zhang, L.H. (2009) Differential modulation of Burkholderia cenocepacia virulence and energy metabolism by the quorum-sensing signal BDSF and its synthase. J. Bacteriol. 191, 7270-7278.
34. Deng, Y., Wu, J., Tao, F. and Zhang, L.H. (2011) Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem. Rev. 111, 160-173.
35. Devescovi, G., Bigirimana, J., Degrassi, G., Cabrio, L., LiPuma, J.J., Kim, J., Hwang, I. and Venturi, V. (2007) Involvement of a quorum-sensing-regulated lipase secreted by a clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl. Environ. Microbiol. 73, 4950-4958.
36. Diggle, S.P., Lumjiaktase, P., Dipilato, F., Winzer, K., Kunakorn, M., Barrett, D.A., Chhabra, S.R., Camara, M. and Williams, P. (2006) Functional genetic analysis reveals a 2-alkyl-4-quinolone signaling system in the human pathogen Burkholderia pseudomallei and related bacteria. Chem. Biol. 13, 701-710.
37. Duerkop, B.A., Ulrich, R.L. and Greenberg, E.P. (2007) Octanoyl-homoserine lactone is the cognate signal for Burkholderia mallei BmaR1-BmaI1 quorum sensing. J. Bacteriol. 189, 5034-5040.
38. Duerkop, B.A., Varga, J., Chandler, J.R., Peterson, S.B., Herman, J.P., Churchill, M.E., Parsek, M.R., Nierman, W.C. and Greenberg, E.P. (2009) Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J. Bacteriol. 191, 3909-3918.
39. Eberl, L. (2006) Quorum sensing in the genus Burkholderia. Int. J. Med. Microbiol. 296, 103-110.
40. French, C.T., Lao, P., Loraine, A.E., Matthews, B.T., Yu, H. and Dybvig, K. (2008) Large-scale transposon mutagenesis of Mycoplasma pulmonis. Mol. Microbiol. 69, 67-76.
41. Fuqua, C. and Winans, S.C. (1996) Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J. Bacteriol. 178, 435-440.
42. Fuqua, C., Burbea, M. and Winans, S.C. (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.
43. Fuqua, W.C. and Winans, S.C. (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.
44. Fuqua, W.C., Winans, S.C. and Greenberg, E.P. (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176, 269-275.
45. Gao, Y., Song, J., Hu, B., Zhang, L., Liu, Q. and Liu, F. (2009) The luxS gene is involved in AI-2 production, pathogenicity, and some phenotypes in Erwinia amylovora. Curr. Microbiol. 58, 1-10.
46. Glass, J.I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M.R., Maruf, M., Hutchison, C.A., Smith, H.O. and Venter, J.C. (2006) Essential genes of a minimal bacterium. Proc. Natl. Acad. Sci. USA, 103, 425-430.
47. Gomelsky, M. (2011) cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol. Microbiol. 79, 562-565.
48. Goo, E., Kang, Y., Kim, H. and Hwang, I. (2010) Proteomic analysis of quorum sensing-dependent proteins in Burkholderia glumae. J. Proteome Res. 9, 3184-3199.
49. Han, S.W., Lee, S.W. and Ronald, P.C. (2011a) Secretion, modification, and regulation of Ax21. Curr. Opin. Microbiol. 14, 62-67.
50. Han, S.W., Sriariyanun, M., Lee, S.W., Sharma, M., Bahar, O., Bower, Z. and Ronald, P.C. (2011b) Small protein-mediated quorum sensing in a Gram-negative bacterium. PLoS ONE, 6, e29192.
51. He, Y.W. and Zhang, L.H. (2008) Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol. Rev. 32, 842-857.
52. He, Y.W., Wang, C., Zhou, L., Song, H., Dow, J.M. and Zhang, L.H. (2006) Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J. Biol. Chem. 281, 33 414-33 421.
53. He, Y.W., Ng, A.Y., Xu, M., Lin, K., Wang, L.H., Dong, Y.H. and Zhang, L.H. (2007) Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol. Microbiol. 64, 281-292.
54. He, Y.W., Boon, C., Zhou, L. and Zhang, L.H. (2009) Co-regulation of Xanthomonas campestris virulence by quorum sensing and a novel two-component regulatory system RavS/RavR. Mol. Microbiol. 71, 1464-1476.
55. He, Y.W., Wu, J., Cha, J.S. and Zhang, L.H. (2010) Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol. 10, 187.
56. Huber, B., Feldmann, F., Kothe, M., Vandamme, P., Wopperer, J., Riedel, K. and Eberl, L. (2004) Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect. Immun. 72, 7220-7230.
57. Hwang, I., Li, P.L., Zhang, L., Piper, K.R., Cook, D.M., Tate, M.E. and Farrand, S.K. (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.
58. Hwang, I., Cook, D.M. and Farrand, S.K. (1995) A new regulatory element modulates homoserine lactone-mediated autoinduction of Ti plasmid conjugal transfer. J. Bacteriol. 177, 449-458.
59. Hwang, I., Smyth, A.J., Luo, Z.Q. and Farrand, S.K. (1999) Modulating quorum sensing by antiactivation: TraM interacts with TraR to inhibit activation of Ti plasmid conjugal transfer genes. Mol. Microbiol. 34, 282-294.
60. Jones, S., Yu, B., Baiton, N.J., Birdsall, M., Bycoft, B.W., Chhabra, S.R., Cox, A.J.R., Reeves, P.J., Stephens, S.,Winson, M.K., Salmond, G.P.C., Stewart, G.S.A.B. and Williams, P. (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12, 2477-2482.
61. Kim, J., Kim, J.G., Kang, Y., Jang, J.Y., Jog, G.J., Lim, J.Y., Kim, S., Suga, H., Nagamatsu, T. and Hwang, I. (2004) Quorum sensing and the LysR-type transcriptional activator ToxR regulate toxoflavin biosynthesis and transport in Burkholderia glumae. Mol. Microbiol. 54, 921-934.
62. Kim, J., Kang, Y., Choi, O., Jeong, Y., Jeong, J.E., Lim, J.Y., Kim, M., Moon, J.S., Suga, H. and Hwang, I. (2007) Regulation of polar flagellum genes is mediated by quorum sensing and FlhDC in Burkholderia glumae. Mol. Microbiol. 64, 165-179.
63. Kim, J., Oh, J., Choi, O., Kang, Y., Kim, H., Goo, E., Ma, J., Nagamatsu, T., Moon, J.S. and Hwang, I. (2009) Biochemical evidence for ToxR and ToxJ binding to the tox operons of Burkholderia glumae and mutational analysis of ToxR. J. Bacteriol. 191, 4870-4878.
64. Koutsoudis, M.D., Tsaltas, D., Minogue, T.D. and von Bodman, S.B. (2006) Quorumsensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc. Natl. Acad. Sci. USA, 103, 5983-5988.
65. Leduc, J.L. and Roberts, G.P. (2009) Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J. Bacteriol. 191, 7121-7122.
66. Lee, S.W., Han, S.W., Sririyanum, M., Park, C.J., Seo, Y.S. and Ronald, P.C. (2009) A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science, 326, 850-853.
67. Li, T.N., Chin, K.H., Fung, K.M., Yang, M.T., Wang, A.H. and Chou, S.H. (2011) A novel tetrameric PilZ domain structure from xanthomonads. PLoS ONE, 6, e22036.
68. Liu, H., Coulthurst, S.J., Pritchard, L., Hedley, P.E., Ravensdale, M., Humphris, S., Burr, T., Takle, G., Brurgerg, M.-B., Birch, P.R.J., Salmond, G.P.C. and Toth, I.K. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogenic Pectobacterium atrosepticum. PLoS Pathog. 4, e1000093.
69. Lowery, C.A., Dickerson, T.J. and Janda, K.D. (2008) Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chem. Soc. Rev. 37, 1337-1346.
70. Luo, Y. and Helmann, J.D. (2012) Analysis of the role of Bacillus subtilis sigma(M) in beta-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol. Microbiol. 83, 623-639.
71. Malott, R.J., O'Grady, E.P., Toller, J., Inhulsen, S., Eberl, L. and Sokol, P.A. (2009) A Burkholderia cenocepacia orphan LuxR homolog is involved in quorum-sensing regulation. J. Bacteriol. 191, 2447-2460.
72. Marden, J.N., Dong, Q., Roychowdhury, S., Berleman, J.E. and Bauer, C.E. (2011) Cyclic GMP controls Rhodospirillum centenum cyst development. Mol. Microbiol. 79, 600-615.
73. Mattiuzzo, M., Bertani, I., Ferluga, S., Cabrio, L., Bigirimana, J., Guarnaccia, C., Pongor, S., Maraite, H. and Venturi, V. (2011) The plant pathogen Pseudomonas fuscovaginae contains two conserved quorum sensing systems involved in virulence and negatively regulated by RsaL and the novel regulator RsaM. Environ. Microbiol. 13, 145-162.
74. McCarthy, Y., Ryan, R.P., O'Donovan, K., He, Y.Q., Jiang, B.L., Feng, J.X., Tang, J.L. and Dow, J.M. (2008) The role of PilZ domain proteins in the virulence of Xanthomonas campestris pv. campestris. Mol. Plant Pathol. 9, 819-824.
75. McCarthy, Y., Dow, J.M. and Ryan, R.P. (2011) The Ax21 protein is a cell-cell signal that regulates virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J. Bacteriol. 193, 6375-6378.
76. McGowan, S.J., Barnard, A.M., Bosgelmez, G., Sebaihia, M., Simpson, N.J., Thomson, N.R., Todd, D.E., Welch, M., Whitehead, N.A. and Salmond, G.P. (2005) Carbapenem antibiotic biosynthesis in Erwinia carotovora is regulated by physiological and genetic factors modulating the quorum sensing-dependent control pathway. Mol. Microbiol. 55, 526-545.
77. Miller, M.B., Skorupski, K., Lenz, D.H., Taylor, R.K. and Bassler, B.L. (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell, 110, 303-314.
78. Miller, S.T., Xavier, K.B., Campagna, S.R., Taga, M.E., Semmelhack, M.F., Bassler, B.L. and Hughson, F.M. (2004) Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol. Cell, 15, 677-687.
79. Mills, E., Pultz, I.S., Kulasekara, H.D. and Miller, S.I. (2011) The bacterial second messenger c-di-GMP: mechanisms of signalling. Cell. Microbiol. 13, 1122-1129.
80. Minogue, T.D., Carlier, A.L., Koutsoudis, M.D. and von Bodman, S.B. (2005) The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. stewartii is a function of EsaR-mediated repression of the rcsA gene. Mol. Microbiol. 56, 189-203.
81. More, M.I., Finger, L.D., Stryker, J.L., Fuqua, C., Eberhard, A. and Winans, S.C. (1996) Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science, 272, 1655-1658.
82. Morohoshi, T., Nakamura, Y., Yamazaki, G., Ishida, A., Kato, N. and Ikeda, T. (2007) The plant pathogen Pantoea ananatis produces N-acylhomoserine lactone and causes center rot disease of onion by quorum sensing. J. Bacteriol. 189, 8333-8338.
83. Nasser,W., Robert-Baudouy, J. and Reverchon, S. (1997) Antagonistic effect of CRP and KdgR in the transcription control of the Erwinia chrysanthemi pectinolysis genes. Mol. Microbiol. 26, 1071-1082.
84. Newman, K.L., Almeida, R.P., Purcell, A.H. and Lindow, S.E. (2004) Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc. Natl. Acad. Sci. USA, 101, 1737-1742.
85. Oger, P., Kim, K.S., Sackett, R.L., Piper, K.R. and Farrand, S.K. (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, 277-288.
86. Oppenheimer-Shaanan, Y., Wexselblatt, E., Katzhendler, J., Yavin, E. and Ben- Yehuda, S. (2011) c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep. 12, 594-601.
87. Pereira, C.S., Thompson, J.A. and Xavier, K.B. (2012) AI-2-mediated signaling in bacteria. FEMS Microbiol. Rev. doi: 10.1111/j.1574-6976.2012.00345.x. [Epub ahead of print].
88. Perez-Mendoza, D., Coulthurst, S.J., Humphris, S., Campbell, E., Welch, M., Toth, I.K. and Salmond, G.P. (2011a) A multi-repeat adhesin of the phytopathogen, Pectobacterium atrosepticum, is secreted by a Type I pathway and is subject to complex regulation involving a non-canonical diguanylate cyclase. Mol. Microbiol. 82, 719-733.
89. Perez-Mendoza, D., Coulthurst, S.J., Sanjuan, J. and Salmond, G.P. (2011b) N-Acetylglucosamine-dependent biofilm formation in Pectobacterium atrosepticum is cryptic and activated by elevated c-di-GMP levels. Microbiology, 157, 3340-3348.
90. Pirhonen, M., Flego, D., Heikinheimo, R. and Palva, E.T. (1993) A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J. 12, 2467-2476.
91. Quinones, B., Pujol, C.J. and Lindow, S.E. (2004) Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae. Mol. Plant-Microbe Interact. 17, 521-531.
92. Quinones, B., Dulla, G. and Lindow, S.E. (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol. Plant- Microbe Interact. 18, 682-693.
93. Rai, R., Ranjan, M., Pradhan, B.B. and Chatterjee, S. (2012) Atypical regulation of virulence-associated functions by a diffusible signal factor in Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 25, 789-801.
94. Reverchon, S., Expert, D., Robert-Baudouy, J. and Nasser,W. (1997) The cyclic AMP receptor protein is the main activator of pectinolysis genes in Erwinia chrysanthemi. J. Bacteriol. 179, 3500-3508.
95. Reverchon, S., Bouillant, M.L., Salmond,G. and Nasser,W. (1998) Integration of the quorum-sensing system in the regulatory networks controlling virulence factor synthesis in Erwinia chrysanthemi. Mol. Microbiol. 29, 1407-1418.
96. Rezzonico, F. and Duffy, B. (2007) The role of luxS in the fire blight pathogen Erwinia amylovora is limited to metabolism and does not involve quorum sensing. Mol. Plant-Microbe Interact. 20, 1284-1297.
97. Rezzonico, F. and Duffy, B. (2008) Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol. 8, 154.
98. Rocha-Estrada, J., Aceves-Diez, A.E., Guarneros, G. and Torre, M. (2010) The RNPP family of quorum-sensing proteins in Gram-positive bacteria. Appl. Microbiol. Biotechnol. 87, 913-923.
99. Romling, U. (2012) Cyclic di-GMP, an established secondary messenger still speeding up. Environ. Microbiol. 14, 1817-1829.
100. Ronald, P.C. (2011) Small protein-mediated quorum sensing in a gram-negative bacterium: novel targets for control of infectious disease. Discov. Med. 12, 461-470.
101. Roy, V., Adams, B.L. and Bentley, W.E. (2011) Developing next generation antimicrobials by intercepting AI-2 mediated quorum sensing. Enzyme Microb. Technol. 49, 113-123.
102. Ryan, R.P. and Dow, J.M. (2010) Intermolecular interactions between HD-GYP and GGDEF domain proteins mediate virulence-related signal transduction in Xanthomonas campestris. Virulence, 1, 404-408.
103. Ryan, R.P., Fouhy, Y., Lucey, J.F., Crossman, L.C., Spiro, S., He, Y.W., Zhang, L.H., Heeb, S., Camara, M., Williams, P. and Dow, J.M. (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. USA, 103, 6712-6717.
104. Ryan, R.P., McCarthy, Y., Andrade, M., Farah, C.S., Armitage, J.P. and Dow, J.M. (2010) Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc. Natl. Acad. Sci. USA, 107, 5989-5994.
105. Ryan, R.P., McCarthy, Y., Kiely, P.A., O'Connor, R., Farah, C.S., Armitage, J.P. and Dow, J.M. (2012) Dynamic complex formation between HD-GYP, GGDEF and PilZ domain proteins regulates motility in Xanthomonas campestris. Mol. Microbiol. 86, 557-567.
106. Schirmer, T. and Jenal, U. (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat. Rev. Microbiol. 7, 724-735.
107. Schmidt, S., Blom, J.F., Pernthaler, J., Berg, G., Baldwin, A., Mahenthiralingam, E. and Eberl, L. (2009) Production of the antifungal compound pyrrolnitrin is quorum sensing-regulated in members of the Burkholderia cepacia complex. Environ. Microbiol. 11, 1422-1437.
108. Seyedsayamdost, M.R., Chandler, J.R., Blodgett, J.A., Lima, P.S., Duerkop, B.A., Oinuma, K., Greenberg, E.P. and Clardy, J. (2010) Quorum-sensing-regulated bactobolin production by Burkholderia thailandensis E264. Org. Lett. 12, 716-719.
109. Shank, E.A. and Kolter, R. (2011) Extracellular signaling and multicellularity in Bacillus subtilis. Curr. Opin. Microbiol. 14, 741-747.
110. Sjoblom, S., Brader, G., Koch, G. and Palva, E.T. (2006) Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol. Microbiol. 60, 1474-1489.
111. Slater, H., Alvarez-Morales, A., Barber, C.E., Daniels, M.J. and Dow, J.M. (2000) A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol. Microbiol. 38, 986-1003.
112. Sondermann, H., Shikuma, N.J. and Yildiz, F.H. (2012) You've come a long way: c-di-GMP signaling. Curr. Opin. Microbiol. 15, 140-146.
113. Song, J.H., Ko, K.S., Lee, J.Y., Baek, J.Y., Oh, W.S., Yoon, H.S., Jeong, J.Y. and Chun, J. (2005) Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Mol. Cells, 19, 365-374.
114. Song,W.Y.,Wang, G.L., Chen, L.L., Kim, H.S., Pi, L.Y., Holsten, T., Gardner, J.,Wang, B., Zhai, W.X., Zhu, L.H., Fauquet, C. and Ronald, P. (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science, 270, 1804-1806.
115. Sun, J., Daniel, R., Wagner-Dobler, I. and Zeng, A.P. (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol. Biol. 4, 36.
116. Tang, J.L., Liu, Y.N., Barber, C.E., Dow, J.M.,Wootton, J.C. and Daniels, M.J. (1991) Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris. Mol. Gen. Genet. 226, 409-417.
117. Tang, J.L., Feng, J.X., Li, Q.Q.,Wen, H.X., Zhou, D.L.,Wilson, T.J., Dow, J.M., Ma, Q.S. and Daniels, M.J. (1996) Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv. oryzae: involvement in exopolysaccharide production and virulence to rice. Mol. Plant-Microbe Interact. 9, 664-666.
118. Tao, F., He, Y.W., Wu, D.H., Swarup, S. and Zhang, L.H. (2010) The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J. Bacteriol. 192, 1020-1029.
119. Thomson, N.R., Nasser, W., McGowan, S., Sebaihia, M. and Salmond, G.P. (1999) Erwinia carotovora has two KdgR-like proteins belonging to the IciR family of transcriptional regulators: identification and characterization of the RexZ activator and the KdgR repressor of pathogenesis. Microbiology, 145 (Pt 7), 1531-1545.
120. Thowthampitak, J., Shaffer, B.T., Prathuangwong, S. and Loper, J.E. (2008) Role of rpfF in virulence and exoenzyme production of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean. Phytopathology, 98, 1252-1260.
121. Trimble, M.J. and McCarter, L.L. (2011) Bis-(3'-5')-cyclic dimeric GMP-linked quorum sensing controls swarming in Vibrio parahaemolyticus. Proc. Natl. Acad. Sci. USA, 108, 18 079-18 084.
122. Tsai, C.S. and Winans, S.C. (2010) LuxR-type quorum-sensing regulators that are detached from common scents. Mol. Microbiol. 77, 1072-1082.
123. Ulrich, R.L., Deshazer, D., Hines, H.B. and Jeddeloh, J.A. (2004) Quorum sensing: a transcriptional regulatory system involved in the pathogenicity of Burkholderia mallei. Infect. Immun. 72, 6589-6596.
124. Vannini, A., Volpari, C., Gargioli, C., Muraglia, E., Cortese, R., De Francesco, R., Neddermann, P. and Marco, S.D. (2002) The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 21, 4393-4401.
125. Venturi, V., Rampioni, G., Pongor, S. and Leoni, L. (2011) The virtue of temperance: built-in negative regulators of quorum sensing in Pseudomonas. Mol. Microbiol. 82, 1060-1070.
126. Wang, C., Zhang, H.B., Wang, L.H. and Zhang, L.H. (2006) Succinic semialdehyde couples stress response to quorum-sensing signal decay in Agrobacterium tumefaciens. Mol. Microbiol. 62, 45-56.
127. Wang, L.H., He, Y., Gao, Y.,Wu, J.E., Dong, Y.H., He, C.,Wang, S.X.,Weng, L.X., Xu, J.L., Tay, L., Fang, R.X. and Zhang, L.H. (2004) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 51, 903-912.
128. Witte, G., Hartung, S., Buttner, K. and Hopfner, K.P. (2008) Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol. Cell, 30, 167-178.
129. Woodward, J.J., Iavarone, A.T. and Portnoy, D.A. (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science, 328, 1703-1705.
130. Yi, X., Yamazaki, A., Biddle, E., Zeng, Q. and Yang, C.H. (2010) Genetic analysis of two phosphodiesterases reveals cyclic diguanylate regulation of virulence factors in Dickeya dadantii. Mol. Microbiol. 77, 787-800.
131. Zhang, H.B., Wang, L.H. and Zhang, L.H. (2002) Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA, 99, 4638-4643.
132. Zhang, H.B., Wang, C. and Zhang, L.H. (2004) The quormone degradation system of Agrobacterium tumefaciens is regulated by starvation signal and stress alarmone (p)ppGpp. Mol. Microbiol. 52, 1389-1401.
133. Zhang, L., Murphy, P.J., Kerr, A. and Tate, M.E. (1993) Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature, 362, 446-448.
134. Zhang, L.H. (2010) A novel C-di-GMP effector linking intracellular virulence regulon to quorum sensing and hypoxia sensing. Virulence, 1, 391-394.
135. Zhang, R.G., Pappas, K.M., Brace, J.L., Miller, P.C., Oulmassov, T., Molyneaux, J.M., Anderson, J.C., Bashkin, J.K.,Winans, S.C. and Joachimiak, A. (2002) Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature, 417, 971-974.
136. Zhao, Y., Qian, G., Yin, F., Fan, J., Zhai, Z., Liu, C., Hu, B. and Liu, F. (2011) Proteomic analysis of the regulatory function of DSF-dependent quorum sensing in Xanthomonas oryzae pv. oryzicola. Microb. Pathog. 50, 48-55.
137. Zhu, J. and Winans, S.C. (1998) Activity of the quorum-sensing regulator TraR of Agrobacterium tumefaciens is inhibited by a truncated, dominant defective TraR-like protein. Mol. Microbiol. 27, 289-297.
138. Zhu, J. and Winans, S.C. (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.