N-acyl-homoserine lactone-mediated quorum sensing blockage, a novel strategy for attenuating pathogenicity of Gram-negative bacterial plant pathogens

European Journal of Plant Pathology

Volumn 111, Issue 4, 2005, Pages 327-339

  Cui, X ^a   Harling, R ^a  

^a SCOTTISH AGRICULTURAL COLLEGE   (United Kingdom)

Author keywords

Acyl homoserine lactone; Autoinducer; Autoinducer receptor protein; Global repressor genes; LuxI LuxR homologues; Pathogenicity; Phytodefense; Quorum sensing; Virulence factor

Indexed keywords

BACTERIAL DISEASE; PATHOGENICITY; PLANT DEFENSE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 19944377210     PISSN: 09291873     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10658-004-4891-0     Document Type: Article

References (109)

1. C Aguilar I Bertani V Venturi 2003 Quorum sensing system and stationary-phase sigma factor of the onion pathogen Burkholderia cepacia Genomovar I type strain, ATCC 25416 Applied and Environmental Microbiology 69 1739 1747
2. NJ Bainton BW Bycroft SR Chhabra P Stead L Gledhill PJ Hill CED Rees MK Winson GPC Salmond GSAB Stewart P Williams 1992a A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia Gene 116 87 91
3. NJ Bainton P Stead SR Chhabra BW Bycroft GPC Salmond GSAB Steward P Williams 1992 N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora Biochemical Journal 288 997 1004
4. F Barras F van Gijsegem AK Chatterjee 1994 Extracellular enzymes and pathogenesis of soft-rot Erwinia Annual Review of Phytopathology 32 201 234
5. WD Bauer M Teplitski 2001 Can plants manipulate bacterial quorum sensing? Australian Journal of Plant Physiology 28 913 921
6. S Beckvon Bodman SK Farrand 1995 Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer Journal of Bacteriology 177 5000 5008
7. P Branny JP Pearson E Pesci TL Kohler BH Iglewski C van Delden 2001 Inhibition of quorum sensing by a Pseudomonas aeruginosa dks homologue Journal of Bacteriology 183 1531 1539
8. EJ Braun 1982 Ultrastructural investigation of resistant and susceptible maize inbreds infected with Erwinia stewartii Phytopathology 72 159 166
9. W Burkholder 1950 Sour skin, a bacterial rot of onion bulbs Phytopathology 40 115 118
10. C Cha P Gao YC Chen PD Shaw SK Farrand 1998 Production of acyl-homoserine lactone quorum sensing signals by Gram-negative plant-associated bacteria Molecular Plant-Microbe Interactions 11 1119 1129
11. PF Chan NJ Bainton MM Daykin MK Winson SR Chhabra GSAB Stewart GPC Salmond BW Bycroft P Williams 1995 Small molecule mediated autoinduction of antibiotic biosynthesis in the plant pathogen Erwinia carotovora Biochemical Society Transactions 23 S127
12. SR Chhabra P Stead NJ Bainton GPC Salmond GSAB Stewart P Williams BW Bycroft 1993 Autoregulation of carbapenem biosynthesis in Erwinia carotovora ATCC 39048 by analogues of N-3-(oxohexanoyl)-L-homoserine lactone Journal of Antibiotics 46 441 454
13. PJ Christie 1997 Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria Journal of Bacteriology 179 3085 3094
14. SA Chugani M Whiteley KM Lee D D'Argenio C Manoil EP Greenberg 2001 QscR, a modulator of quorum sensing signal synthesis and virulence in P. aeruginosa Proceedings of National Academy of Sciences of the United States of America 98 2752 2757
15. SJ Clough KE Lee MA Schell TP Denny 1997 A two-component system in Ralstonia (Pseudomonas) solanacearum modulates production of PhcA-regulated virulence factors in response to 3-hydroxypalmitic acid methyl ester Journal of Bacteriology 179 3639 3648
16. A Collmer NT Keen 1986 The role of pectic enzymes in plant pathogenesis Annual Review of Phytopathology 24 383 409
17. M Cooper SM Batchelor JI Prosser 1995 Is cell density-signalling applicable to biofilms? J Wimpenny W Nichols D Stickler H Lappin-Scott The Life and Death of a Biofilm. BioLine Cardiff, UK 93 96
18. X Cui 2004 Regulation of biosurfactant production by quorum sensing in Pseudomonas fluorescens 5064, the cause of broccoli head rot disease University of Edinburgh Edinburgh, UK PhD Thesis
19. X Cui R Harling P Mutch D Darling 2005 Identification of N-3-hydroxyoctanoyl-homoserine lactone production in Pseudomonas fluorescens 5064, pathogenic to broccoli, and controlling biosurfactant production by quorum sensing European Journal of Plant Pathology 111 297 308
20. YY Cui A Chatterjee Y Liu K Dumenyo AK Chatterjee 1995 Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-l-homoserine lactone, and pathogenicity in soft-rotting Erwiniaspp Journal of Bacteriology 177 5108 5115
21. R Daniels DE De Vos J Desair G Raedschelders E Luyten V Rosemeyer C Verreth E Schoeters J Vanderleyden J Michiels 2002 The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation Journal of Biological Chemistry 277 462 468
22. TR de Kievit PC Seed L Passador J Nezezon BH Iglewski 1999 RsaL, a novel repressor of virulence gene expression in Pseudomonas aeruginosa Journal of Bacteriology 181 2175 2184
23. TR de Kievit BH Iglewski 2000 Bacterial quorum sensing in pathogenic relationships Infection and Immunity 68 4839 4849
24. R de Nys A Wright GM Konig O Sticher 1993 New halogenated furanones from the marine alga Delisea pulchra Tetrahedron 49 11213 11220
25. PJ Dolph DR Majerczak DL Coplin 1988 Characterization of a gene cluster for exopolysaccharide biosynthesis and virulence in Erwinia stewartii Journal of Bacteriology 170 865 871
26. YH Dong JL Xu XZ Li LH Zhang 2000 AiiA, an enzyme that inactivates the acyl-homoserine lactone quorum sensing signal and attenuates the virulence of Erwinia carotovora Proceedings of National Academy of Sciences of the United States of America 97 3526 3531
27. YH Dong LH Wang JL Xu HB Zhang XF Zhang LH Zhang 2001 Quenching quorum sensing dependent bacterial infection by an N-acylhomoserine lactonase Nature 411 813 817
28. YH Dong AR Gusti Q Zhang JL Xu LH Zhang 2002 Identification of quorum quenching N-acyl-homoserine lactonases from Bacillus species Applied and Environmental Microbiology 68 1754 1759
29. YH Dong XF Zhang JL Xu LH Zhang 2004 Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference Applied and Environmental Microbiology 70 954 960
30. CK Dumenyo A Mukherjee W Chum AK Chatterjee 1998 Genetic and physiological evidence for the production of N-acyl homoserine lactones by Pseudomonas syringae pv. syringae and other fluorescent plant pathogenic Pseudomonasspecies European Journal of Plant Pathology 104 569 582
31. GM Dunny SC Winans 1997 Cell-cell signaling in bacteria ASM press Washington DC, USA
32. A Eberhard AL Burlingame GL Kenyon KH Nealson NJ Oppenheimer 1981 Structural identification of autoinducer of Photobacterium fischeri luciferase Biochemistry 20 2444 2449
33. A Eberhard CA Widrig P McBath JB Schineller 1986 Analogs of the autoinducer of bioluminescence in Vibrio fischeri Archives of Microbiology 146 35 40
34. AK EI-Sayed J Hothersall CM Thomas 2001 Quorum sensing-dependent regulation of biosynthesis of the polyketide antibiotic mupirocin in Pseudomonas fluorescens NCIMB 10586 Microbiology 147 2127 2139
35. M Elasri S Delorme P Lemanceau G Stewart B Laue E Glickmann PM Oger Y Dessaux 2001 Acyl-homoserine lactone production is more common among plant-associated Pseudomonasspp. than among soilborne Pseudomonas spp Applied and Environmental Microbiology 67 1198 1209
36. J Engebrecht K Nealson M Silverman 1983 Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri Cell 32 773 781
37. RG Finch DI Pritchard BW Bycroft P Williams GSAB Stewart 1998 Quorum sensing - a novel target for anti-infective therapy Journal of Antimicrobial Agents and Chemotherapy 42 569 571
38. S Flagan Weng-Ki Ching JR Leadbetter 2003 Arthrobacter strain VAI-A utilizes acyl-homoserine lactone inactivation products and stimulates quorum signal biodegradation by Variovorax paradoxus Applied and Environmental Microbiology 69 909 916
39. AB Flavier LM Ganova-Raeva MA Schell TP Denny 1997 Hierarchical autoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester Journal of Bacteriology 179 7089 7097
40. RG Fray JP Throup M Daykin A Wallace P Williams GSAB Stewart D Grierson 1999 Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria Nature Biotechnology l 17 1017 1020
41. RG Fray 2002 Altering plant-microbe interaction through artificially manipulating bacterial quorum sensing Annals of Botany 89 245 253
42. WC Fuqua SC Winans EP Greenberg 1994 Quorum sensing in bacteria; the LuxR-LuxI family of cell density responsive transcriptional regulators Journal of Bacteriology 176 269 275
43. WG Fuqua SG Winans EP Greenberg 1996 Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum sensing transcriptional regulators Annual Review of Microbiology 50 721 751
44. MJ Gambello S Kaye BH Iglewski 1993 LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene and an enhancer of exotoxin A expression Infection and Immunity 61 1180 1184
45. M Gao M Teplitski JB Robinson WD Bauer 2003 Production of substances by Medicago truncatula that affect bacterial quorum sensing Molecular Plant-Microbe Interactions 16 827 834
46. M Givskov R de Nys M Manefield L Gram R Maximilien L Eberl S Molin PD Steinberg S Kjelleberg 1996 Eukaryotic interference with homoserine lactone mediated prokaryotic signaling Journal of Bacteriology 178 6618 6622
47. A Glessner RS Smith BH Iglewski JB Robinson 1999 Roles of the Pseudomonas aeruginosa las and rhl quorum sensing systems in control of twitching motility Journal of Bacteriology 181 1623 1629
48. EP Greenberg JW Hastings S Ulitzur 1979 Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria Archives of Microbiology 120 87 91
49. EP Greenberg 2000 Acyl-homoserine lactone quorum sensing in bacteria Journal of Microbiology 38 117 121
50. BL Hanzelka EP Greenberg 1995 Evidence that the N-terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducer-binding domain Journal of Bacteriology 177 815 817
51. BL Hanzelka EP Greenberg 1996 Quorum sensing in Vibrio fischeri: evidence that S-adenosylmethionine is the amino acid substrate for autoinducer synthesis Journal of Bacteriology 178 5291 5294
52. AC Hayward 1995 Pseudomonas solanacearum US Singh RP Singh K Kohmoto Pathogenesis and Host Specificity in Plant Diseases: Histopathological, Biochemical, Genetic and Molecular Bases. Elsevier Science Inc. Tarrytown, NY, USA 139 151 Vol I, Prokaryotes
53. PD Hildebrand 1989 Surfactant-like characteristics and identity of bacteria associated with broccoli head rot in Atlantic Canada Canadian Journal of Plant Pathology 11 205 224
54. JC Hinton JM Sidebotham LJ Hyman MC Perombelon GP Salmond 1989 Isolation and characterization of transposon-induced mutants of Erwinia carotovora subsp. atroseptica exhibiting reduced virulence Molecular and General Genetics 217 141 148
55. TT Hoang HP Schweizer 1999 Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis Journal of Bacteriology 181 5489 5497
56. MTG Holden SR Chhabra R de Nys P Stead NJ Bainton PJ Hill M Manefield N Kumar M Labatte D England S Rice M Givskov GPC Salmond GSAB Stewart BW Bycroft S Kjelleberg P Williams 1999 Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria Molecular Microbiology 33 1254 1266
57. IY Hwang PL Li LH Zhang KR Piper DM Cook ME Tate SK Farrand 1994 TraI, a LuxI homologue is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer Proceedings of National Academy of Sciences of the United States of America 91 4639 4643
58. Y Jiang M Camara SR Chhabra KR Hardie BW Bycroft A Lazdunski GPC Salmond GSAB Stewart P Williams 1998 In vitro biosynthesis of the Pseudomonas aeruginosa quorum sensing signal molecule, N-butanoyl-L-homoserine lactone Molecular Microbiology 28 193 203
59. S Jones B Yu NJ Bainton M Birdsall BW Bycroft SR Chhabra AJR Cox P Golby PJ Reeves S Stephens MK Winson GPC Salmond GSAB Stewart P Williams 1993 The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa EMBO Journal 12 2477 2482
60. S Kjelleberg P Steinberg M Givskov L Gram M Manefield R de Nys 1997 Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquatic Microbiology and Ecology 13 85 93
61. JR Leadbetter EP Greenberg 2000 Metabolism of acyl-homoserine lactone quorum sensing signals by Variovorax paradoxus Journal of Bacteriology 182 6921 6926
62. SJ Lee SY Park JJ Lee DY Yum BT Koo JK Lee 2002 Genes encoding the N-acyl homoserine lactone degrading enzyme are widespread in many subspecies of Bacillus thuringiensis Applied and Environmental Microbiology 68 3919 3924
63. JA Leigh DL Coplin 1992 Exopolysaccharides in plant-bacterial interactions Annual Review of Microbiology 46 307 346
64. S Lewenza B Conway EP Greenberg PA Sokol 1999 Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI Journal of Bacteriology 181 748 756
65. YH Lin JL Xu J Hu LH Wang SL Ong JR Leadbetter LH Zhang 2003 Acyl-homoserine lactone acylase from Ralstonia str. XJ12B represents a novel and potent class of quorum quenching enzymes Molecular Microbiology 47 849 860
66. A Mae M Montesano V Koiv ET Palva 2001 Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to bacterial phytopathogen Erwinia carotovora Molecular Plant-Microbe Interactions 13 637 648
67. M Manefield L Harris SA Rice R de Nys S Kjelleberg 2000 Inhibition of luminescence and virulence in the black tiger prawn pathogen Vibrio harveyi by intercellular signal antagonists Applied and Environmental Microbiology 66 2079 2084
68. M Manefield M Welch M Givskov GPC Salmond S Kjelleberg 2001 Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora FEMS Microbiology Letters 205 131 138
69. M Manefield TB Rasmussen M Henzter JB Andersen P Steinberg S Kjelleberg M Givskov 2002 Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover Microbiology 148 1119 1127
70. U Mathesius S Mulders M Gao M Teplitski G Caetano-Anolles BG Rolfe WD Bauer 2003 Extensive and specific responses of a eukaryote to bacterial quorum sensing signals Proceedings of National Academy of Sciences of the United States of America 100 1444 1449
71. T Matsuyama K Kaneda Y Nakagawa K Isa H Hara-Hotta I Yano 1992 A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and -independent spreading growth of Serratia macrescens Journal of Bacteriology 174 1769 1776
72. D McKenney KE Brown DG Allison 1995 Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication Journal of Bacteriology 177 6989 6992
73. L McMurry RE Petrucci Jr SB Levy 1980 Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli Proceedings of National Academy of Sciences of the United States of America 77 3974 3977
74. MI More LD Finger JL Stryker G Fuqua A Eberhard SC Winans 1996 Enzymatic synthesis of a quorum sensing autoinducer through the use of defined substrates Science 272 1655 1658
75. UA Ochsner J Reiser 1995 Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa Proceedings of National Academy of Sciences of the United States of America 92 6424 6428
76. MR Parsek DL Val BL Hanzelka JE Gronan EP Greenberg 1999 Acylhomoserine-lactone quorum sensing signal generation Proceedings of National Academy of Sciences of the United States of America 96 4360 4365
77. L Passador JM Cook MJ Gambello L Rust HB Iglewski 1993 Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication Science 260 1127 1130
78. JP Pearson KM Gray L Passador KD Tucker A Eberhard BH Iglewski EP Greenberg 1994 Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes Proceedings of National Academy of Sciences of the United States of America 91 197 201
79. JP Pearson L Passador BH Iglewski EP Greenberg 1995 A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa Proceedings of National Academy of Sciences of the United States of America 92 1490 1494
80. JP Pearson C van Delden BH Iglewski 1999 Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell to cell signals Journal of Bacteriology 181 1203 1210
81. EC Pesci BH Iglewski 1999 Quorum sensing in Pseudomonas aeruginosa GM Dunny SC Winans Cell-cell signaling in bacteria. American Society of Microbiology Press Washington, DC, USA 147 155
82. LS Pierson III LS Thomashow 1992 Cloning and heterologous expression of the phenazine biosynthetic locus of Pseudomonas aureofaciens 30-84 Molecular Plant-Microbe Interactions 5 330 339
83. KS Piper Bodman Beck von S Farrand 1993 Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction Nature 362 448 450
84. M Pirhonen H Saarilahti MB Karlsson ET Palva 1991 Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis Molecular Plant-Microbe Interactions 4 276 283
85. M Pirhonen D Flego R Heikinheimo ET Palva 1993 A small diffusible molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora EMBO Journal 12 2467 2476
86. A Puskas EP Greenberg S Kaplan AL Schaefer 1997 A quorum sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides Journal of Bacteriology 179 7530 7537
87. LG Rahme EJ Stevens SF Wolfort J Shao RG Tompkins FM Ausubel 1995 Common virulence factors for bacterial pathogenicity in plants and animals Science 268 1899 1902
88. TB Rasmussen M Manefield JB Andersen L Eberl U Anthoni C Christophersen P Steinberg S Kjelleberg M. Givskov 2000 How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciensMG1 Microbiology 146 3237 3244
89. AL Schaefer DL Val BL Hanzelka JE Cronan EP Greenberg 1996a Generation of cell-to-cell signals in quorum sensing: acylhomoserine lactone synthase activity of a purified V. fischeri LuxI protein Proceedings of National Academy of Sciences of the United States of America 93 9505 9509
90. AL Schaefer BL Hanzelka A Eberhard EP Greenberg 1996b Quorum sensing in Vibrio fischeri: probing autoinducer LuxR interactions with autoinducer analogs Journal of Bacteriology 178 2897 2901
91. AL Schaefer TA Taylor JT Beatty EP Greenberg 2002 Long-chain acyl-homoserine lactone quorum sensing regulation of Rhodobacter capsulatus gene transfer agent production Journal of Bacteriology 184 6515 6521
92. MA Schell 1996 To be or not to be: how Pseudomonas solanacearum decides whether or not to express virulence genes European Journal of Plant Pathology 102 459 469
93. PC Seed L Passador BH Iglewsi 1995 Activation of thePseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy Journal of Bacteriology 177 654 659
94. J Sheng V Citovsky 1996 Agrobacterium-plant cell DNA transport: have virulence proteins, will travel Plant Cell 8 1699 1710
95. S Srinivasan J Ostling T Charlton R de Nys K Takayama S Kjelleberg 1998 Extracellular signal molecules involved in the carbon starvation response of marine Vibriosp. strain S14 Journal of Bacteriology 180 201 209
96. S Swift MK Winson PF Chan NJ Bainton M Birdsall PJ Reeves CED Rees SR Chhabra PJ Hill JP Throup BW Bycroft GPC Salmond P Williams GSAB Stewart 1993 A novel strategy for the isolation of luxIhomologue: evidence for the widespread distribution of a LuxR: LuxI superfamily in enteric bacteria Molecular Microbiology 10 511 520
97. S Swift AV Karlyshev L Fish E Durant MK Winson SR Chhabra P Williams S MacIntyre GSAB Stewart 1997 Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologues AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules Journal of Bacteriology 179 5271 5281
98. S Swift P Williams GSAB Stewart 1999 N-acylhomoserine lactones and quorum sensing in the proteobacteria GM Dunny SC Winans Cell-Cell Signaling in Bacteria. American Society of Microbiology Press Washington, DC, USA 291 313
99. S Swift MJ Lynch L Fish DF Kirke JM Tomas GSAB Stewart P Williams 1999b Quorum sensing dependent regulation and blockade of exoprotease production in Aeromonas hydrophila Infection and Immunity 67 5192 5199
100. M Teplitski JB Roberson WD Bauer 2000 Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria Molecular Plant-Microbe Interactions 13 637 648
101. M Teplitski H Chen S Rajamani M Gao M Merighi RT Sayre JB Robinson BG Rolfe WD Bauer 2004 Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria Plant Physiology 134 137 146
102. S Uroz C D'Angelo-Picard A Carlier M Elasri C Sicot A Petit P Oger D Faure Y Dessaux 2003 Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria Microbiology 149 1981 1989
103. F van Bambeke Y Glupczynski P Plesiat JC Pechere PM Tulkens 2003 Antibiotic efflux pumps in prokaryotic cells: occurrence, impact on resistance and strategies for the future of antimicrobial therapy Journal of Antimicrobial Chemotherapy 51 1055 1065
104. P Williams GSAB Stewart M Camara MK Winson SR Chhabra GP Salmond BW Bycroft 1996 Signal transduction through quorum sensing in Pseudomonas aeruginosa T Nakazawa K Furukawa D Haas S Silver Pseudomonas: Molecular Biology and Biotechnology American Society of Microbiology Press Washington DC USA 195 205
105. MK Winson M Camara A Latifi M Foglino SR Chhabra M Daykin M Bally V Chapon GPC Salmond BW Bycroft A Lazdunski GSAB Stewart P Williams 1995 Multiple N-acylhomoserine lactone signal molecules regulate production of virulence determinant and secondary metabolites in Pseudomonas aeruginosa Proceedings of National Academy of Sciences of the United States of America 92 9427 9431
106. L Zhang A Kerr 1991 A diffusible compound can enhance conjugal transfer of the Ti plasmid in Agrobacterium tumefaciens Journal of Bacteriology 173 1867 1872
107. L Zhang PJ Murphy A Kerr ME Tate 1993 Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones Nature 362 446 448
108. LH Zhang 2003 Quorum quenching and proactive host defense Trends in Plant Science 8 238 244
109. J Zhu JW Beaber MI More C Fuqua A Eberhard SC Winans 1998 Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens Journal of Bacteriology 180 5398 5405