Plant phenolic acids affect the virulence of Pectobacterium aroidearum and P.carotovorum ssp. brasiliense via quorum sensing regulation

Molecular Plant Pathology

Volumn 17, Issue 4, 2016, Pages 487-500

  Joshi, Janak Raj ^a,b   Burdman, Saul ^a   Lipsky, Alexander ^b   Yariv, Shaked ^b   Yedidia, Iris ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

Bacterial virulence; Cinnamic acid; Pectobacterium; Quorum sensing; Salicylic acid

Indexed keywords

CINNAMIC ACID; CINNAMIC ACID DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE; HYDROXYBENZOIC ACID DERIVATIVE; MESSENGER RNA; PHENOLIC ACID; SALICYLIC ACID;

ANALOGS AND DERIVATIVES; BACTERIAL GENE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY; PECTOBACTERIUM; QUORUM SENSING; VIRULENCE;

4-BUTYROLACTONE; CINNAMATES; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HYDROXYBENZOATES; PECTOBACTERIUM; QUORUM SENSING; RNA, MESSENGER; SALICYLIC ACID; VIRULENCE;

EID: 84940915739     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12295     Document Type: Article

References (89)

1. Antunes, L.C., Ferreira, R.B., Buckner, M.M. and Finlay, B.B. (2010) Quorum sensing in bacterial virulence. Microbiology, 156, 2271-2282.
2. Bandara, M.B., Zhu, H., Sankaridurg, P.R. and Willcox, M.D. (2006) Salicylic acid reduces the production of several potential virulence factors of Pseudomonas aeruginosa associated with microbial keratitis. Invest. Ophthalmol. Vis. Sci. 47, 4453-4460.
3. Barnard, A.L. and Salmond, G.C. (2007) Quorum sensing in Erwinia species. Annal. Bioanal. Chem. 387, 415-423.
4. Barnard, A.M., Bowden, S.D., Burr, T., Coulthurst, S.J., Monson, R.E. and Salmond, G.P. (2007) Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos. Trans. R. Soc. London, B: Biol. Sci. 362, 1165-1183.
5. Bodini, S.F., Manfredini, S., Epp, M., Valentini, S. and Santori, F. (2009) Quorum sensing inhibition activity of garlic extract and p-coumaric acid. Lett. Appl. Microbiol. 49, 551-555.
6. Broberg, M., Lee, G.W., Nykyri, J., Lee, Y.H., Pirhonen, M. and Palva, E.T. (2014) The global response regulator ExpA controls virulence gene expression through RsmA-mediated and RsmA-independent pathways in Pectobacterium wasabiae SCC3193. Appl. Environ. Microbiol. 80, 1972-1984.
7. Burr, T., Barnard, A.M.L., Corbett, M.J., Pemberton, C.L., Simpson, N.J.L. and Salmond, G.P.C. (2006) Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol. Microbiol. 59, 113-125.
8. Chang, C.-Y., Krishnan, T., Wang, H., Chen, Y., Yin, W.-F., Chong, Y.-M., Tan, L.Y., Chong, T.M. and Chan, K.-G. (2014) Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone synthase as druggable target. Sci. Rep. 4, 1-8.
9. Charkowski, A., Blanco, C., Condemine, G., Expert, D., Franza, T., Hayes, C., Hugouvieux-Cotte-Pattat, N., Solanilla, E.L., Low, D., Moleleki, L., Pirhonrn, M., Pitman, A., Perna, N., Reverchon, S., Palenzuela, P.R., Francisco, M.S., Toth, I., Tsuyumu, S., Waals, J.D., Wolf, J.V.D., Gijsegem, F.V., Yang, C.-H. and Yedidia, I. (2012) The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu. Rev. Phytopathol. 50, 425-449.
10. Chatterjee, A., Cui, Y., Liu, Y., Dumenyo, C.K. and Chatterjee, A.K. (1995) Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl. Environ. Microbiol. 61, 1959-1967.
11. Chatterjee, A., Cui, Y., Hasegawa, H., Leigh, N., Dixit, V. and Chatterjee, A.K. (2005) Comparative analysis of two classes of quorum-sensing signaling systems that control production of extracellular proteins and secondary metabolites in Erwinia carotovora subspecies. J. Bacteriol. 187, 8026-8038.
12. Chow, S., Gu, K., Jiang, L. and Nassour, A. (2011) Salicylic acid affects swimming, twitching and swarming motility in Pseudomonas aeruginosa, resulting in decreased biofilm formation. J. Exp. Microbiol. Immunol. 15, 22-29.
13. Crépin, A., Barbey, C., Beury-Cirou, A., Hélias, V., Taupin, L., Reverchon, S., Nasser, W., Faure, D., Dufour, A., Orange, N., Feuilloley, M., Heurlier, K., Burini, J.-F. and Latour, X. (2012) Quorum sensing signaling molecules produced by reference and emerging soft-rot bacteria (Dickeya and Pectobacterium spp. PLoS ONE, 7, e35176.
14. 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.
15. Czajkowski, R., van der Wolf, J., Krolicka, A., Ozymko, Z., Narajczyk, M., Kaczynska, N. and Lojkowska, E. (2015) Salicylic acid can reduce infection symptoms caused by Dickeya solani in tissue culture grown potato (Solanum tuberosum L.) plants. Eur. J. Plant Pathol. 141, 545-558.
16. Daglia, M. (2012) Polyphenols as antimicrobial agents. Curr. Opin. Biotechnol. 23, 174-181.
17. Davidsson, P.R.R., Kariola, T., Niemi, O. and Palva, T. (2013) Pathogenicity of and plant immunity to soft rot pectobacteria. Front. Plant Sci. 4, 191.
18. Deep, A., Chaudhary, U. and Gupta, V. (2011) Quorum sensing and bacterial pathogenicity: from molecules to disease. J. Lab. Physicians, 3, 4-11.
19. Defoirdt, T., Brackman, G. and Coenye, T. (2013) Quorum sensing inhibitors: how strong is the evidence? Trends Microbiol. 21, 619-624.
20. Dong, Y.-H., Wang, L.-H., Xu, J.-L., Zhang, H.-B., Zhang, X.-F. and Zhang, L.-H. (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 411, 813-817.
21. Engebrecht, J. and Silverman, M. (1984) Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA, 81, 4154-4158.
22. Faure, D. and Dessaux, Y. (2007) Quorum sensing as a target for developing control strategies for the plant pathogen Pectobacterium. Eur. J. Plant Pathol. 119, 353-365.
23. Fuqua, C., Parsek, M.R. and Greenberg, E.P. (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35, 439-468.
24. 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.
25. Galloway, W.R., Hodgkinson, J.T., Bowden, S., Welch, M. and Spring, D.R. (2012) Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol. 20, 449-458.
26. Helman, Y. and Chernin, L. (2015) Silencing the mob: disrupting quorum sensing as a means to fight plant disease. Mol. Plant Pathol. 16, 316-329.
27. Hema, R., Vemanna, R.S., Sreeramulu, S., Reddy, C.P., Senthil-Kumar, M. and Udayakumar, M. (2014) Stable expression of mtlD gene imparts multiple stress tolerance in finger millet. PLoS ONE, 9, e99110.
28. Hentzer, M., Wu, H., Andersen, J.B., Riedel, K., Rasmussen, T.B., Bagge, N., Kumar, N., Schembri, M.A., Song, Z., Kistoffersen, P., Manefield, M., Costerton, J.W., Molin, S., Eberl, L., Steinberg, P., Kjellebreg, S., Hoiby, N. and Givskov, M. (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22, 3803-3815.
29. Hommais, F., Oger-Desfeux, C., Van Gijsegem, F., Castang, S., Ligori, S., Expert, D., Nasser, W. and Reverchon, S. (2008) PecS is a global regulator of the symptomatic phase in the phytopathogenic bacterium Erwinia chrysanthemi 3937. J. Bacteriol. 190, 7508-7522.
30. Jafra, S., Jalink, H., Van Der Schoor, R. and Van Der Wolf, J.M. (2006) Pectobacterium carotovorum subsp. carotovorum strains show diversity in production of and response to N-acyl homoserine lactones. J. Phytopathol. 154, 729-739.
31. Jang, Y.-S., Sohn, S.-I. and Wang, M.-H. (2006) The hrpN gene of Erwinia amylovora stimulates tobacco growth and enhances resistance to Botrytis cinerea. Planta, 223, 449-456.
32. Jones, S., Yu, B., Bainton, N.J., Birdsall, M., Bycroft, B.W., Chhabra, S.R., Cox, A.J., Golby, P., Reeves, P.J. and Stephens, S. (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12, 2477-2482.
33. Joshi, J.R., Burdman, S., Lipsky, A. and Yedidia, I. (2015) Effects of plant antimicrobial phenolic compounds on virulence of the genus Pectobacterium. Res. Microbiol. 166, 535-545. doi: 10.1016/j.resmic.2015.04.004.
34. Kalia, V.C. (2013) Quorum sensing inhibitors: an overview. Biotechnol. Adv. 31, 224-245.
35. de Kievit, T.R. and Iglewski, B.H. (2000) Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68, 4839-4849.
36. Kõiv, V., Andresen, L., Broberg, M., Frolova, J., Somervuo, P., Auvinen, P., Pirhonen, M., Tenson, T. and Mae, A. (2013) Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae. PLoS ONE, 8, e54248.
37. Krishnan, T., Yin, W.F. and Chan, K.G. (2012) Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa PAO1 by Ayurveda spice clove (Syzygium aromaticum) bud extract. Sensors, 12, 4016-4030.
38. Laasik, E., Andresen, L. and Mäe, A. (2006) Type II quorum sensing regulates virulence in Erwinia carotovora ssp. carotovora. FEMS Microbiol. Lett. 258, 227-234.
39. Lagonenko, L., Lagonenko, A. and Evtushenkov, A. (2013) Impact of salicylic acid on biofilm formation by plant pathogenic bacteria. J. Biol. Earth Sci. 3, B176-B181.
40. Lee, D.H., Lim, J.A., Lee, J., Roh, E., Jung, K., Choi, M., Oh, C., Ryu, S., Yun, J. and Heu, S. (2013) Characterization of genes required for the pathogenicity of Pectobacterium carotovorum subsp. carotovorum Pcc21 in Chinese cabbage. Microbiology, 159, 1487-1496.
41. Li, Y., Peng, Q., Selimi, D., Wang, Q., Charkowski, A.O., Chen, X. and Yang, C.-H. (2009) The plant phenolic compound p-coumaric acid represses gene expression in the Dickeya dadantii type III secretion system. Appl. Environ. Microbiol. 75, 1223-1228.
42. Li, Y., Hutchins, W., Wu, X., Liang, C., Zhang, C., Yuan, X., Khokhani, D., Chen, X., Che, Y., Wang, Q. and Yang, C.-H. (2015) Derivative of plant phenolic compound inhibits the type III secretion system of Dickeya dadantii via HrpX/HrpY two-component signal transduction and Rsm systems. Mol. Plant Pathol. 16, 150-163.
43. Liu, H., Coulthurst, S.J., Pritchard, L., Hedley, P.E., Ravensdale, M., Humphris, S., Burr, T., Takle, G., Brurberg, M.-B., Brich, 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 pathogen Pectobacterium atrosepticum. PLoS Path. 4, e1000093.
44. Ma, B., Hibbing, M.E., Kim, H.-S., Reedy, R.M., Yedidia, I., Breuer, J., Breuer, J., Glasner, J.D., Perna, N.T., Kelman, A. and Charkowski, A.O. (2007) Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology, 97, 1150-1163.
45. Mandal, S.M., Chakraborty, D. and Dey, S. (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal. Behav. 5, 359-368.
46. Manefield, M., Harris, L., Rice, S.A., de Nys, R. and Kjelleberg, S. (2000) Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl. Environ. Microbiol. 66, 2079-2084.
47. Manefield, M., Welch, M., Givskov, M., Salmond, G.P. and Kjelleberg, S. (2001) Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiol. Lett. 205, 131-138.
48. Marchler-Bauer, A., Zheng, C., Chitsaz, F., Derbyshire, M.K., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., Hurwitz, D.I., Lanczcki, C.J., Lu, F., Marchler, G.H., Song, J.S., Thanki, N., Yamashita, R.A., Zhang, D. and Bryant, S.H. (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acid Res. 41, 348-352.
49. Matern, U. and Kneusel, R. (1988) Phenolic compounds in plant disease resistance. Phytoparasitica, 16, 153-170.
50. McClean, K.H., Winson, M.K., Fish, L., Taylor, A., Chhabra, S.R., Camara, M., Daykin, M., Lamb, J.H., Swift, S., Bycroft, B.W., Stewart, G.S. and Williams, P. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology, 143, 3703-3711.
51. Middleton, B., Rodgers, H.C., Cámara, M., Knox, A.J., Williams, P. and Hardman, A. (2002) Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol. Lett. 207, 1-7.
52. Mirzoeva, O.K., Grishanin, R.N. and Calder, P.C. (1997) Antimicrobial action of propolis and some of its components: the effects on growth, membrane potential and motility of bacteria. Microbiol. Res. 152, 239-246.
53. Mole, B.M., Baltrus, D.A., Dangl, J.L. and Grant, S.R. (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol. 15, 363-371.
54. Molina, L., Constantinescu, F., Michel, L., Reimmann, C., Duffy, B. and Défago, G. (2003) Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol. Ecol. 45, 71-81.
55. Molina, L., Rezzonico, F., Defago, G. and Duffy, B. (2005) Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J. Bacteriol. 187, 3206-3213.
56. Mukherjee, A., Cui, Y., Liu, Y., Dumenyo, C.K. and Chatterjee, A.K. (1996) Global regulation in Erwinia species by Erwinia carotovora rsmA, a homologue of Escherichia coli csrA: repression of secondary metabolites, pathogenicity and hypersensitive reaction. Microbiology, 142, 427-434.
57. Murray, E.J., Crowley, R.C., Truman, A., Clarke, S.R., Cottam, J.A., Jadhav, G.P., Steele, V.R., O'Shea, P., Lindholm, C., Cockayne, A., Chhabra, S.R., Chan, W.C. and Williams, P. (2014) Targeting Staphylococcus aureus quorum sensing with nonpeptidic small molecule inhibitors. J. Med. Chem. 57, 2813-2819.
58. Nabhan, S., De Boer, S.H., Maiss, E. and Wydra, K. (2012) Taxonomic relatedness between Pectobacterium carotovorum subsp. carotovorum, Pectobacterium carotovorum subsp. odoriferum and Pectobacterium carotovorum subsp. brasiliense subsp. nov. J. Appl. Microbiol. 113, 904-913.
59. Nabhan, S., De Boer, S.H., Maiss, E. and Wydra, K. (2013) Pectobacterium aroidearum sp. nov., a soft rot pathogen with preference for monocotyledonous plants. Int. J. Syst. Evol. Microbiol. 63, 2520-2525.
60. Nasser, W., Bouillant, M.L., Salmond, G. and Reverchon, S. (1998) Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N-acyl-homoserine lactone signal molecules. Mol. Microbiol. 29, 1391-1405.
61. Nealson, K.H., Platt, T. and Hastings, J.W. (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104, 313-322.
62. O'Loughlin, C.T., Miller, L.C., Siryaporn, A., Drescher, K., Semmelhack, M.F. and Bassler, B.L. (2013) A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc. Natl. Acad. Sci. USA, 110, 17981-17986.
63. Onkendi, E. and Moleleki, L. (2014) Characterization of Pectobacterium carotovorum subsp. carotovorum and brasiliense from diseased potatoes in Kenya. Eur. J. Plant Pathol. 139, 557-566.
64. Park, T.-H., Choi, B.-S., Choi, A.-Y., Choi, I.-Y., Heu, S. and Park, B.-S. (2012) Genome sequence of Pectobacterium carotovorum subsp. carotovorum strain PCC21, a pathogen causing soft rot in Chinese cabbage. J. Bacteriol. 194, 6345-6346.
65. 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.
66. Pollumaa, L., Alamae, T. and Mae, A. (2012) Quorum sensing and expression of virulence in pectobacteria. Sensors, 12, 3327-3349.
67. Praillet, T., Nasser, W., Robert-Baudouy, J. and Reverchon, S. (1996) Purification and functional characterization of PecS, a regulator of virulence-factor synthesis in Erwinia chrysanthemi. Mol. Microbiol. 20, 391-402.
68. Prithiviraj, B., Bais, H.P., Weir, T., Suresh, B., Najarro, E.H., Dayakar, B.V., Schweizer, H.P. and Vivanco, J.M. (2005) Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect. Immun. 73, 5319-5328.
69. Reverchon, S., Nasser, W. and Robert-Baudouy, J. (1994) pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi. Mol. Microbiol. 11, 1127-1139.
70. Rutherford, S.T. and Bassler, B.L. (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2, 1-25.
71. Schauder, S., Shokat, K., Surette, M.G. and Bassler, B.L. (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41, 463-476.
72. Smadja, B., Latour, X., Faure, D., Chevalier, S., Dessaux, Y. and Orange, N. (2004) Involvement of N-acylhomoserine lactones throughout plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum). Mol. Plant-Microbe Interact. 17, 1269-1278.
73. Smith, D., Wang, J.H., Swatton, J.E., Davenport, P., Price, B., Mikkelsen, H., Stickland, H., Nishikawa, K., Gardiol, V., Spring, D.R. and Welch, M. (2006) Variations on a theme: diverse N-acyl homoserine lactone-mediated quorum sensing mechanisms in gram-negative bacteria. Prog. Surf. Sci. 89, 167-211.
74. Sova, M. (2012) Antioxidant and antimicrobial activities of cinnamic acid derivatives. Mini Rev. Med. Chem. 12, 749-767.
75. Taga, M.E., Semmelhack, J.L. and Bassler, B.L. (2001) The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Mol. Microbiol. 42, 777-793.
76. Takle, G.W., Toth, I.K. and Brurberg, M.B. (2007) Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum. BMC Plant Biol. 7, 50.
77. Toth, I.K. and Birch, P.R.J. (2005) Rotting softly and stealthily. Curr. Opin. Plant Biol. 8, 424-429.
78. Toth, I.K., Bell, K.S., Holeva, M.C. and Birch, P.R.J. (2003) Soft rot Erwiniae: from genes to genomes. Mol. Plant Pathol. 4, 17-30.
79. Toth, I.K., van der Wolf, J.M., Saddler, G., Lojkowska, E., Hélias, V., Pirhonen, M., Tsror (Lahkim), L. and Elphinstone, J.G. (2011) Dickeya species: an emerging problem for potato production in Europe. Plant Pathol. 60, 385-399.
80. Wagner, V.E., Bushnell, D., Passador, L., Brooks, A.I. and Iglewski, B.H. (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185, 2080-2095.
81. Waters, C.M. and Bassler, B.L. (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346.
82. Wei, Z.M. and Beer, S.V. (1995) hrpL activates Erwinia amylovora hrp gene transcription and is a member of the ECF subfamily of sigma factors. J. Bacteriol. 177, 6201-6210.
83. Winson, M.K., Swift, S., Fish, L., Throup, J.P., Jørgensen, F., Chhabra, S.R., Bycroft, B.W., Williams, P. and Stewart, G.S.A.B. (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163, 185-192.
84. Winzer, K., Falconer, C., Garber, N.C., Diggle, S.P., Camara, M. and Williams, P. (2000) The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182, 6401-6411.
85. Yang, L., Rybtke, M.T., Jakobsen, T.H., Hentzer, M., Bjarnsholt, T., Givskov, M. and Tolker-Nielsen, T. (2009) Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrob. Agents Chemother. 53, 2432-2443.
86. Yang, S., Peng, Q., San Francisco, M., Wang, Y., Zeng, Q. and Yang, C.H. (2008) Type III secretion system genes of Dickeya dadantii 3937 are induced by plant phenolic acids. PLoS ONE, 3, e2973.
87. Yishay, M., Burdman, S., Valverde, A., Luzzatto, T., Ophir, R. and Yedidia, I. (2008) Differential pathogenicity and genetic diversity among Pectobacterium carotovorum ssp. carotovorum isolates from monocot and dicot hosts support early genomic divergence within this taxon. Environ. Microbiol. 10, 2746-2759.
88. Yuan, Z.C., Edlind, M.P., Liu, P., Saenkham, P., Banta, L.M., Wise, A.A., Ronzone, E., Binns, A.N., Kerr, K. and Nester, E.U. (2007) The plant signal salicylic acid shuts down expression of the vir regulon and activates quormone-quenching genes in Agrobacterium. Proc. Natl. Acad. Sci. USA, 104, 11790-11795.
89. Zhang, Y., Xu, S., Ding, P., Wang, D., Cheng, Y.T., He, J., Gao, M., Xu, F., Li, Y., Zhu, Z., Li, X. and Zhang, Y. (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. USA, 107, 18220-18225.