Chapter 8 : Bacterial Biofilms on Plants: Relevance and Phenotypic Aspects

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Numerous bacteria and fungi are able to colonize and form biofilms on plant surfaces. Microbes colonizing aerial surfaces, such as flowers, stems, and leaves (phyllosphere), are generally referred to as epiphytes. Bacterial colonizers of the root surface (rhizosphere) are generally referred to as rhizobacteria. This chapter specifically focuses on the mechanisms involved in bacterial biofilm formation on plant roots, including pathogenic and beneficial interactions. Scanning electron microscopy (SEM) is a powerful tool to visualize at the single-cell level the process of colonization and microcolonies in the rhizosphere and on sprouts showing the presence of many differently shaped bacteria. The genetic background of plants should also be taken into account to gain a better understanding about how bacteria function in the rhizosphere. Quorum-sensing genes have been identified in several plant-associated bacteria regulating a large variety of different phenotypes involved in pathogenicity and plant beneficial effects. Hyphae of soil-born pathogenic fungi attach to the root and usually colonize the root surface before penetrating and infecting the root. Biofilm formation on fungal hyphae implicates the possibility of interactions at the molecular level between the fungus and the bacterium. Bacterium-fungus interactions are found widespread through nature, associated with plants and animals, where these microorganisms compete with each other, attack each other, and form consortia.

Citation: Bloemberg G, Lugtenberg B. 2004. Bacterial Biofilms on Plants: Relevance and Phenotypic Aspects, p 141-159. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch8
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1. Aldon, D.,, B. Brito,, C. Boucher,, and S. Genin. 2000. A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. EMBO J. 19: 2304 2314.
2. Allaway, D.,, N. A. Schofield,, M. E. Leonard,, L. Gilardoni,, T. M. Finan,, and P. S. Poole. 2001. Use of differential fluorescence induction and optical trapping to isolate environmentally induced genes. Environ. Microbiol. 3: 397 406.
3. Andersen, J. B.,, A. Heydorn,, M. Hentzer,, L. Eberl,, O. Geisenberg,, B. B. Christensen,, S. Molin,, and M. Givskov. 2001. Gfp-Based Nacyl homoserine-lactone sensor systems for detection of bacterial communities. Appl. Environ. Microbiol. 67: 575 585.
4. Andersen, J. B.,, C. Sternberg,, L. K. Poulsen,, S. P. Bjorn,, M. Givskov,, and S. Molin. 1999. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl. Environ. Microbiol. 64: 2240 2246.
5. Bentley, S. D.,, K. F. Chater,, A. M. Cerdeno-Tarraga,, G. L. Challis,, N. R. Thomson,, K. D. James,, D. E. Harris,, M. H. Quail,, H. Kieser,, D. Harper,, A. Bateman,, S. Brown,, G. Chandra,, S. W. Chen,, M. Collins,, A. Cronin,, A. Fraser,, A. Goble,, J. Hidalgo,, T. Hornsby,, S. Howarth,, C. H. Huang,, T. Kieser,, L. Larke,, L. Murphy,, K. Oliver,, S. O’Neil,, E. Rabbinowitsch,, M. A. Rajandream,, K. Rutherford,, S. Rutter,, K. Seeger,, D. Saunders,, S. Sharp,, R. Squares,, S. Squares,, K. Taylor,, T. Warren,, A. Wietzorrek,, J. Woodward,, B. G. Barrell,, J. Parkhill,, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141 147.
6. Bhattacharyya, A.,, S. Stilwagen,, N. Ivanova,, M. D’Souza,, A. Bernal,, A. Lykidis,, V. Kapatral,, I. Andersen,, N. Larsen,, T. Los,, G. Reznik,, E. Selkov, Jr.,, T. L. Walunas,, H. Feil,, W. S. Feil,, H. Purcell,, J. L. Lassez,, T. L. Hawkins,, R. Haselkorn,, R. Overbeek,, P. F. Predki,, and N. C. Kyrpides. 2002. Wholegenome comparative analysis of three phytopathogenic Xylella fastidiosa strains. Proc. Natl. Acad. Sci. USA 99: 12403 12408.
7. Biancotto, V.,, S. Andreotti,, R. Balestrini,, P. Bonfante,, and S. Perotto. 2001. Extracellular polysaccharides are involved in the attachment of Azospirillum brasilense and Rhizobium leguminosarum to arbuscular mycorrhizal structures. Eur. J. Histochem. 45: 39 49.
8. Bianciotto, V.,, E. Lumini,, L. Lanfranco,, D. Minerdi,, P. Bonfante,, and S. Perotto. 2000 Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl. Environ. Microbiol. 66: 4503 4509.
9. Bloemberg, G. V.,, G. A. O’Toole,, B. J. J. Lugtenberg,, and R. Kolter. 1997. Green fluorescent protein as a marker for Pseudomonas spp. Appl. Environ. Microbiol. 63: 4543 4551.
10. Bloemberg, G. V.,, A. H. M. Wijfjes,, G. E. M. Lamers,, N. Stuurman,, and B. J. J. Lugtenberg. 2000. Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere; new perspectives for studying microbial communities. Mol. Plant-Microbe Interact. 13: 1170 1176.
11. Bolwerk, A.,, A. L. Lagopodi,, A. H. M. Wijfjes,, G. E. M. Lamers,, T. F. C. Chin-A-Woeng,, B. J. J. Lugtenberg,, and G. V. Bloemberg. 2003. Interactions in the tomato rhizosphere of two Pseudomonas biocontrol strains with the phytopathogenic fungus Fusarium oxysporum f. sp. radicislycopersici. Mol. Plant-Microbe Interact. 16: 983 993.
12. Buell, C. R.,, V. Joardar,, M. Lindeberg,, J. Selengut,, I. T. Paulsen,, M. L. Gwinn,, R. J. Dodson,, R. T. Doboy,, A. S. Durkin,, J. F. Kolodnay,, R. Madupu,, S. Daugherty,, L. Brinkac,, M. J. Beanan,, D. H. Haft,, W. C. Nelson,, T. Davidsen,, N. Zafar,, L. Zhou,, J. Liu,, Q. Yuan,, H. Khouri,, N. Fedorova,, B. Tran,, D. Russell,, K. Berry,, T. Utterback,, S. E. Van Aken,, T. V. Feldblyum,, M. D’Ascenzo,, W. L. Deng,, A. R. Ramos,, J. R. Alfano,, S. Cartinhour,, A. K. Chatterjee,, T. P. Delamey,, S. G. Lazarowitz,, G. B. Martin,, D. J. Schneider,, X. Tang,, C. L. Bender,, O. White,, C. M. Fraser,, and A. Collmer. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100: 10181 10186.
13. Camacho-Carjaval, M. M. 2001. Molecular characterization of the roles of type 4 pili, NDH-1 and PyrR in rhizosphere colonization of Pseudomonas fluorescens WCS365. Ph.D. dissertation. Leiden University, Leiden, The Netherlands.
14. Carlier, A.,, S. Uroz,, B. Smadja,, R. Fray,, X. Latour,, Y. Dessaux,, and D. Faure. 2003. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding N-acyl homoserine lactonase activity. Appl. Environ. Microbiol. 69: 4989 4993.
15. Cha, C.,, P. Chao,, Y. C. Chen,, P. D. Shaw,, and S. K. Farrand. 1998. Production of acylhomoserine lactone quorum sensing signals in gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11: 1119 1129.
16. Chin-A-Woeng, T. F. C.,, G. V. Bloemberg,, I. Mulders,, L. Dekkers,, and B. J. J. Lugtenberg. 2000. Root colonization is essential for root biocontrol of tomato foot and root rot by the phenazine-1-carboxamide producing bacterium Pseudomonas chlororaphis PCL1391. Mol. Plant-Microbe Interact. 13: 1340 1345.
17. Chin-A-Woeng, T. F. C.,, G. V. Bloemberg,, A. J. van der Bij,, K. M. G. M. vander Drift,, J. Schripsema,, B. Kroon,, R. J. Scheffer,, C. Keel,, P. A. H. M. Bakker,, H.-V. Tichy,, F. J. de Bruijn,, J. E. Thomas-Oates,, and B. J. J. Lugtenberg. 1998. Biocontrol by phenazine-1-carboxamide producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f.sp. radicis-lycopersici. Mol. Plant-Microbe Interact. 11: 1069 1077.
18. Chin-A-Woeng, T. F. C.,, W. de Priester,, A. J. van der Bij,, and B. J. J. Lugtenberg. 1997. Description of the colonization of a gnotobiotic tomato rhizosphere by Pseudomonas fluorescens biocontrol strain WCS365, using scanning electron microscopy. Mol. Plant-Microbe Interact. 10: 79 86.
19. Chin-A-Woeng, T. F. C.,, D. van den Broek,, G. de Voer,, K. M. G. M. van der Drift,, J. E. Thomas-Oates,, B. J. J. Lugtenberg,, and G. V. Bloemberg. 2001. Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted in the medium. Mol. Plant-Microbe Interact. 14: 969 979.
20. Ching-Hong, Y.,, J. A. Menge,, and D. A. Cooksey. 1994. Mutations affecting hyphal colonisation and pyoverdine production in pseudomonads antagonistic toward Phytophtora parasitica. Appl. Environ. Microbiol. 60: 473 481.
21. Davey, M. E.,, N. C. Caiazza,, and G. A. O’Toole. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185: 1027 1036.
22. Davies, D. G.,, M. R. Parsek,, J. P. Pearson,, B. H. Iglewski,, J. W. Costerton,, and E. P. Greenberg. 1998. The involvement of cell-tocell signals in the development of a bacterial biofilm. Science 280: 295 298.
23. Dekkers, L. C.,, I. H. Mulders,, C. C. Phoelich,, T. F. C. Chin-A-Woeng,, A. H. M. Wijfjes,, and B. J. J. Lugtenberg. 2000. The sss colonization gene of the tomato- Fusarium oxysporum f.sp. radicis lycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild-type Pseudomonas spp. bacteria. Mol. Plant-Microbe Interact. 13: 1177 1183.
24. de Weert, S.,, H. Vermeiren,, I. H. Mulders,, I. Kuiper,, N. Hendrickx,, G. V. Bloemberg,, J. Vanderleyden,, R. De Mot,, and B. J. J. Lugtenberg. 2002. Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 15: 1173 1180.
25. D’Haeze, W.,, and M. Holsters. 2002. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12: 79 105.
26. Dong, Y. H.,, A. R. Gusti,, Q. Zhang,, J. L. Xu,, and L. H. Zhang. 2002. Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68: 1754 1759.
27. Dong, Y. H.,, L. H. Wang,, J. L. Xu,, H. B. Zhang,, X. F. Zhang,, and L. H. Zhang. 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813 817.
28. Dong, Y. H.,, J. L. Xu,, X. Z. Li,, and L. H. Zhang. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97: 3526 3531.
29. Dorr, J.,, T. Hurek,, and B. Reinhold-Hurek. 1998. Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol. Microbiol. 30: 7 17.
30. Duffy, B.,, and G. Defago. 1997. Zinc improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology 87: 1250 1257.
31. Duffy, B.,, A. Schouten,, and J. M. Raaijmakers. 2003. Pathogen self-defense: mechanism to counteract microbial antagonism. Annu. Rev. Phytopathol. 41: 501 538.
32. Elasri, M.,, S. Delorme,, P. Lemanceau,, G. Stewart,, B. Laue,, E. Glickmann,, P. M. Oger,, and Y. Dessaux. 2001. Acyl-homoserine lactone production is more common among plantassociated Pseudomonas spp. than among soilborne Pseudomonas spp. Appl. Environ. Microbiol. 67: 1198 1209.
33. Espinosa-Urgel, M.,, A. Salido,, and J. L. Ramos. 2000. Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 182: 2363 2369.
34. Fett, W. F.,, and P. H. Cooke. 2003. Scanning electron microscopy of native biofilms on mung bean sprouts. Can. J. Microbiol. 49: 45 50.
35. Flavier, A. B.,, L. M. Ganova-Raeva,, M. A. Schell,, and T. P. 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. J. Bacteriol. 179: 7089 7097.
36. Fray, R. G.,, J. P. Throup,, M. Daykin,, A. Wallace,, P. Williams,, G. S. Stewart,, and D. Grierson. 1999. Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nat. Biotechnol. 17: 1017 1020.
37. Fuqua, C.,, and E. P. Greenberg. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3: 685 695.
38. Gaballa, A.,, P. D. Abeysinghe,, G. Urich,, S. Matthijs,, H. De Greve,, P. Cornelis,, and N. Koedam. 1997. Trehalose induces antagonism towards Pythium debaryanum in Pseudomonas fluorescens ATCC 17400. Appl. Environ. Microbiol. 63: 4340 4345.
39. Gage, D. J. 2002. Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J. Bacteriol. 184: 7042 7046.
40. Gage, D. J.,, T. Bobo,, and S. R. Long. 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa ( Medicago sativa). J. Bacteriol. 178: 7159 7166.
41. Galibert, F.,, T. M. Finan,, S. R. Long,, A. Puhler,, P. Abola,, F. Ampe,, F. Barloy- Hubler,, M. J. Barnett,, A. Bocker,, P. Boistard,, G. Bothe,, M. Boutry,, L. Bowser,, J. Buhmester,, 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. Portelle,, B. Purnelle,, U. Ramspergor,, R. Surzycki,, P. Thebault,, M. Vandenbol,, P. 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.
42. Goodner, B.,, G. Hinkle,, S. Gattung,, N. Miller,, M. Blanchard,, B. Qurollo,, B. S. Goldman,, Y. Cas,, 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.
43. Gray, K. M.,, J. P. Pearson,, J. A. Downie,, B. E. Boboye,, and E. P. Greenberg. 1996. Cell-tocell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372 376.
44. Greenberg, J. T.,, and B. A. Vinatzer. 2003. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6: 20 28.
45. Guttman, D. S.,, B. A. Vinatzer,, S. F. Sarkar,, M. V. Ranall,, G. Kettler,, and J. T. Greenberg. 2002. A functional screen for the Type II (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722 1726.
46. Heeb, S.,, and D. Haas. 2001. Regulatory roles of the GacS/GacA two-component system in plantassociated and other gram-negative bacteria. Mol. Plant-Microbe Interact. 14: 1351 1363.
47. Heeb, S.,, Y. Itoh,, T. Nishijyo,, U. Schnider,, C. Keel,, J. Wade,, U. Walsh,, F. O’Gara,, and D. Haas. 2000. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in Gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 13: 232 237.
48. Hentzer, M.,, K. Riedel,, T. B. Rasmussen,, A. Heydorn,, J. B. Andersen,, M. R. Parsek,, S. A. Rice,, L. Eberl,, S. Molin,, N. Hoiby,, S. Kjelleberg,, and M. Givskov. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148: 87 102.
49. 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.
50. Höfte, M.,, Q. Dong,, S. Kourambas,, V. Krishnapillai,, D. Sherratt,, and M. Mergeay. 1994. The sss gene product, which affects pyoverdin production in Pseudomonas aeruginosa 7NSK2, is a sitespecific recombinase. Mol. Microbiol. 14: 1011 1020.
51. Hogan, D. A.,, and R. Kolter. 2002. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229 2232.
52. Izallalen, M.,, R. C. Levesque,, X. Perret,, W. J. Broughton,, and H. Antoun. 2002. Broad-hostrange mobilizable suicide vectors for promoter trapping in gram-negative bacteria. BioTechniques 33: 1038 1043.
53. Kaneko, T.,, Y. Nakamura,, S. Sato,, E. Asamizu,, T. Kato,, S. Sasamoto,, A. Watanabe,, K. Idesawa,, A. Ishikawa,, K. Kawashiña,, 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.
54. Kaneko, T.,, Y. Nakamura,, S. Sato,, K. Minamisawa,, T. Uchiumi,, S. Sasamoto,, A. Watanabe,, K. Idesawa,, M. Iriguchi,, K. Kawashima,, M. Kohara,, M. Matsumoto,, S. Shimpo,, H. Tsuruoka,, T. Wada,, M. Yamada,, and S. Tabata. 2002. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9: 189 197.
55. Klausen, M.,, A. Heydorn,, P. Ragas,, L. Lambertsen,, A. Aaes-Jorgensen,, S. Molin,, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48: 1511 1524.
56. Kuiper I.,, G. V. Bloemberg,, S. Noreen,, J. E. Thomas-Oates,, and B. J. J. Lugtenberg. 2001. Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol. Plant-Microbe Interact. 14: 1096 1104.
57. Kuiper, I.,, L. Kravchenkov,, G. V. Bloemberg,, and B. J. J. Lugtenberg. 2002. Pseudomonas putida strain PCL1444, selected for efficient root colonization and naphthalene degradation, effectively utilizes root exudates components Mol. Plant-Microbe Interact. 15: 734 741.
58. Kuiper, I.,, E. L. Lagendijk,, R. Pickford,, J. Derrick,, G. E. M. Lamers,, J. E. Thomas-Oates,, B. J. J. Lugtenberg,, and G. V. Bloemberg. 2004. Characterization of two Pseudomonas putida lipopeptide biosurfactants, Putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol. Microbiol. 51: 97 113.
59. Kunst, F.,, N. Ogasawara,, I. Moszer,, A. M. Albertini,, G. Alloni,, V. Azevedo,, M. G. Bertero,, P. Bessieres,, A. Bolotin,, S. Borchert,, R. Borris,, L. Boursier,, A. Brans,, M. Braun,, S. C. Brignell,, S. Bron,, S. Brouillet,, C. V. Bruschi,, B. Caldwell,, V. Capuano,, N. M. Carter,, S. K. Choi,, J. J. Codani,, I. F. Connerton,, A. Danchin, et al. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249 256.
60. Lagopodi, A. L.,, A. F. J. Ram,, G. E. M. Lamers,, P. J. Punt,, C. A. M. J. J. van den Hondel,, B. J. J. Lugtenberg,, and G. V. Bloemberg. 2002. Confocal laser scanning mircoscopical analysis of tomato root colonization and infection by Fusarium oxysporum f.sp. radicis-lycopersici using the green fluorescent protein as a marker. Mol. Plant-Microbe Interact. 15: 172 179.
61. Laue, B. E.,, Y. Jiang,, S. R. Chhabra,, S. Jacob,, G. S. 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- cistetradecenoyl) homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146: 2469 2480.
62. Lee, S. J.,, S. Y. Park,, J. J. Lee,, D. Y. Yum,, B. T. Koo,, and J. K. Lee. 2002. Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl. Environ. Microbiol. 68: 3919 3924.
63. Lee, S. W.,, and D. A. Cooksey. 2000. Genes expressed in Pseudomonas putida during colonization of a plant-pathogenic fungus. Appl. Environ. Microbiol. 66: 2764 2772.
64. Leveau, J. H.,, and S. E. Lindow. 2002b. Bioreporters in microbial ecology. Curr. Opin. Microbiol. 5: 259 265.
65. Leveau, J. H.,, and S. E. Lindow. 2001. Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc. Natl. Acad. Sci. USA 98: 3446 3453.
66. Lin, Y. H.,, J. L. Xu,, J. Hu,, Wang,, S. L. Ong,, J. R. Leadbetter,, and L. H. Zhang. 2003. Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol. Microbiol. 47: 849 860.
67. Lindow, S. E.,, and J. H. J. Leveau. 2002. Phyllosphere microbiology. Curr. Opin. Biotechnol. 13: 238 243.
68. Liu, H.,, Y. Kang,, S. Genin,, M. A. Schell,, and T. P. Denny. 2001. Twitching motility of Ralstonia solanacearum requires a type IV pilus system. Microbiology 147: 3215 3229.
69. Loh, J.,, E. A. Pierson,, L. S. Pierson III,, G. Stacey,, and A. Chatterjee. 2002. Quorum sensing in plant-associated bacteria. Curr. Opin. Plant Biol. 5: 285 290.
70. Lübeck, P. S.,, M. Hansen,, and J. Sørensen. 2000. Simultaneous detection of the establishment of seed-inoculated Pseudomonas fluorescens strain Dr54 and native soil. bacteria on sugar beet root surfaces using fluorescense antibody and in situ hybridization techniques. FEMS Microbiol. Ecol. 33: 11 19.
71. Lugtenberg, B. J. J.,, T. F. C. Chin-A-Woeng,, and G. V. Bloemberg. 2002. Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81: 373 383.
72. Lugtenberg, B. J. J.,, L. Dekkers,, and G. V. Bloemberg. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39: 461 490.
73. Lugtenberg, B. J. J.,, L. V. Kravchenko,, and M. Simons. 1999. Tomato seed and root exudates sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ. Microbiol. 1: 439 446.
74. Mae, A.,, M. Montesano,, V. Koiv,, and E. T. Palva. 2001. Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. Mol. Plant-Microbe Interact. 14: 1035 1042.
75. Manefield, M.,, M. Welch,, M. Givskov,, G. P. Salmond,, and 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 Microbiol. Lett. 205: 131 138.
76. Marie, C.,, W. J. Deakin,, V. Viprey,, J. Kopcinska,, W. Golinowski,, H. B. Krishnan,, X. Perret,, and W. J. Broughton. 2003. Characterization of Nops, nodulation outer proteins, secreted via the type III secretion system of NGR234. Mol. Plant-Microbe Interact. 16: 743 751.
77. Mathesius, U.,, S. Mulders,, M. Gao,, M. Teplitski,, G. Caetano-Anolles,, B. G. Rolfe,, and W. D. Bauer. 2003. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. USA 0: 1444 1449.
78. Matthysse, A. G.,, and S. McMahan. 1998. Root colonization by Agrobacterium tumefaciens is reduced in cel, attB, attD, and attR mutants. Appl. Environ. Microbiol. 64: 2341 2345.
79. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56: 289 314.
80. Miller, M. B.,, and B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165 199.
81. Nelson, K. E.,, C. Weinel,, I. T. Paulsen,, R. J. Dodson,, H. Hilbert,, V. A. Martins dos Santos,, D. E. Fouts,, S. R. Gil,, M. Pop,, M. Holmes,, L. Brinkac,, M. Beanan,, R. T. DeBoy,, S. Daugherty,, J. Kolodnay,, R. Madupu,, W. Nelson,, O. White,, J. Peterson,, H. Khouri,, I. Hance,, P. Chris Lee,, E. Holtzapple,, D. Scanlan,, K. Tran,, A. Moazzez,, T. Utterback,, M. Rizzo,, K. Lee,, D. Kosack,, D. Moestl,, H. Wedler,, J. Lauber,, D. Stjepandic,, J. Hoheisel,, M. Straetz,, S. Heim,, C. Kiewitz,, J. A. Eisen,, K. N. Timmis,, A. Dusterhoft,, B. Tummler,, and C. M. Fraser. 2002. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4: 799 808.
82. Notz, R.,, M. Maurhofer,, U. Schnider-Keel,, B. Duffy,, and G. Defago. 2001. Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 91: 873 881.
83. Notz, R. E.,, M. Maurhofer,, H. Dubach,, D. Haas,, and G. Defago. 2002. Fusaric acid producing strains of Fusarium oxysporum alter 2,4-diacetylphloroglucinol biosynthetic gene expression in Pseudomonas fluorescens CHA0 in vitro and in the rhizosphere of wheat. Appl. Environ. Microbiol. 68: 2229 2235.
84. O’Toole, G.,, H. B. Kaplan,, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54: 49 79.
85. O’Toole, G. A.,, and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295 304.
86. Park, S. Y.,, S. J. Lee,, T. K. Oh,, J. W. Oh,, B. T. Koo,, D. Y. Yum,, and J. K. Lee. 2003. AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149: 1541 1550.
87. Pierson, P. A.,, D. W. Wood,, J. A. Cannon,, F. M. Blachere,, and L. S. Pierson III. 1998. LSP: interpopulation signaling via N-acylhomoserine lactones among bacteria in the wheat rhizosphere. Mol. Plant-Microbe Interact. 11: 1078 1084.
88. Preston, G. M.,, N. Bertrand,, and P. B. Rainey. 2001. Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25 . Mol. Microbiol. 41: 999 1014.
89. Raaijmakers, J. M.,, M. Vlami,, and J. T. de Souza. 2002. Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek 81: 537 547.
90. Rainey, P. B. 1999. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1: 243 257.
91. Ramos, H. J.,, L. D. Roncato-Maccari,, F. M. Souza,, J. R. Soares-Ramos,, M. Hungria,, and F. O. Pedrosa. 2002. Monitoring Azospirillumwheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J. Biotechnol. 97: 243 252.
92. Ramos, C.,, L. Molbak,, and S. Molin. 2000. Bacterial activity in the rhizosphere analyzed at the single-cell level by monitoring ribosome contents and synthesis rates. Appl. Environ. Microbiol. 66: 801 809.
93. Rasmussen, T. B.,, M. Manefield,, J. B. Andersen,, L. Eberl,, U. Anthoni,, C. Christophersen,, P. Steinberg,, S. Kjelleberg,, and M. Givskov. 2000. How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 12: 3237 3244.
94. Reimmann, C.,, N. Ginet,, L. Michel,, C. Keel,, P. Michaux,, V. Krishnapillai,, M. Zala,, K. Heurlier,, K. Triandafillu,, H. Harms,, G. Defago,, and D. Haas. 2002. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148: 923 932.
95. Roine, E.,, D. M. Raineri,, M. Romantschuk,, M. Wilson,, and D. N. Nunn. 1998. Characterization of type IV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 11: 1048 1056.
96. Salanoubat, M.,, S. Genin,, F. Artiguenave,, J. Gouzy,, S. Mangenot,, M. Arlat,, A. Billault,, P. Brottier,, J. C. Camus,, L. Cattolico,, M. Chandler,, N. Choisne,, C. Claudel-Renard,, S. Cunnac,, N. Demange,, C. Gaspin,, M. Lavie,, A. Moisan,, C. Robert,, W. Saurin,, T. Schiex,, P. Siguier,, P. Thebault,, M. Whalen,, P. Wincker,, M. Levy,, J. Weissenbach,, and C. A. Boucher. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415: 497 502.
97. Schembri, M. A.,, K. Kjaergaard,, and P. Klemm. 2003. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48: 253 267.
98. Schnider-Keel, U.,, A. Seematter,, M. Maurhofer,, C. Blumer,, B. Duffy,, C. Gigot-Bonnefoy,, C. Reimmann,, R. Notz,, G. Défago,, D. Haas,, and C. Keel. 2000. Autoinduction of 2,4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J. Bacteriol. 182: 1215 1225.
99. Schripsema, J.,, K. E. de Rudder,, T. B. van Vliet,, P. P. Lankhorst,, E. de Vroom,, J. W. Kijne,, and A. A. 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 cotranscription factors. J. Bacteriol. 178: 366 371.
100. Simon, H.,, K. P. Smith,, J. E. Dodsworth,, B. Guenthner,, J. Handelsman,, and R. M. Goodman. 2001. Influence of tomato genotype on growth of inoculated and indigenous bacteria in the spermosphere. Appl. Environ. Microbiol. 67: 514 520.
101. Simons, M.,, A. J. vander Bij,, I. Brand,, L. A. de Weger,, C. A. Wijffelman,, and B. J. J. Lugtenberg. 1996. Gnotobiotic system for studying rhizosphere colonization by plant growthpromoting Pseudomonas bacteria. Mol. Plant-Microbe Interact. 9: 600 607.
102. Simpson, A. J. G.,, F. Reinach,, P. Arruda,, F. A. Abreu,, M. Acencio,, R. Alvarenga,, and L. M. C. Alves. 2000. The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406: 151 157.
103. Smith, K.,, J. Handelsman,, and R. M. Goodman. 1999a. Genetic basis in plants for interactions with disease-suppressive bacteria. Proc. Natl. Acad. Sci. USA 96: 4786 4790.
104. Smith, L. M.,, E. Tola,, P. deBoer,, and F. O’Gara. 1999b. Signalling by the fungus Pythium ultimum represses expression of two ribosomal RNA operons with key roles in the rhizosphere ecology of Pseudomonas fluorescens F113. Environ. Microbiol. 1: 495 502.
105. Smith, R. S., and B. H. Iglewski. 2003. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6: 56 60.
106. Sorensen, M.,, C. Lippuner,, T. Kaiser,, A. Misslitz,, T. Aebischer,, and D. Bumann. 2003. Rapidly maturing red fluorescent protein variants with strongly enhanced brightness in bacteria. FEBS Lett. 552: 110 114.
107. Spaink, H. P.,, A. Kondorosi,, and P. J. J. Hooykaas (ed.). 1998. The Rhizobiaceae. Kluwer Academic Publishers, Dordrecht, The Netherlands.
108. Spiers, A. J.,, J. Bohannon,, S. M. Gehrig,, and P. B. Rainey. 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol. Microbiol. 50: 15 27.
109. Steenhoudt, O.,, and J. Vanderleijden. 2000. Azospirillum, a free-living nitrogen-fixing bacteria closely associated with grasses: genetics, biochemical and ecological aspects. FEMS Microbiol. Rev. 24: 487 506.
110. Steidle, A.,, K. Sigl,, R. Schuhegger,, A. Ihring,, M. Schmid,, S. Gantner,, M. Stoffels,, K. Riedel,, M. Givskov,, A. Hartman,, C. Langebartels,, and L. Eberl. 2001. Visualisation of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67: 5761 5770.
111. Stover, C. K.,, X. Q. Pham,, A. L. Erwin,, S. D. Mizoguchi,, P. Warrener,, M. J. Hickey,, F. S. Brinkman,, W. O. Hufnagle,, D. J. Kowalik,, M. Lagrou,, R. L. Garber,, L. Goltry,, E. Tolentino,, S. Westbrock-Wadman,, Y. Yuan,, L. L. Brody,, S. N. Coulter,, K. R. Folger,, A. Kas,, K. Larbig,, R. Lim,, K. Smith,, D. Spencer,, G. K. Wong,, Z. Wu,, I. T. Paulsen,, J. Reizer,, M. H. Saier,, R. E. Hancock,, S. Lory,, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959 964.
112. Stuurman, N.,, C. Pacios Bras,, C. H. R. M. Schlaman,, A. H. M. Wijfjes,, G. V. Bloemberg,, and H. P. Spaink. 2000. The use of GFP color variants expressed on stable broad-host range vectors to visualize rhizobia interacting with plants. Mol. Plant-Microbe Interact. 13: 1063 1069.
113. Sutherland, I. W. 2001. The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol. 9: 222 227.
114. Swift, S.,, J. A. Downie,, N. A. Whitehead,, A. M. Barnard,, G. P. Salmond,, and P. Williams. 2001. Quorum sensing as a population-densitydependent determinant of bacterial physiology. Adv. Microb. Physiol. 45: 199 270.
115. Teplitski, M.,, J. B. Robinson,, and W. D. Bauer. 2000. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe Interact. 13: 637 648.
116. Tombolini, R.,, D. J. van der Gaag,, B. Gerhardson,, and J. K. Jansson. 1999. Colonization pattern of the biocontrol strain Pseudomonas chlororaphis MA342 on barley seeds visualized by using green fluorescent protein. Appl. Environ. Microbiol. 65: 3674 3680.
117. Unge, A.,, and J. Jansson. 2001. Monitoring population size, activity, and distribution of gfp-luxABtagged Pseudomonas fluorescens SBW25 during colonization of wheat. Microb. Ecol. 41: 290 300.
118. Unge, A.,, R. Tombolini,, L. Molbak,, and J. K. Jansson. 1999. Simultaneous monitoring of cell number and metabolic activity of specific bacterial populations with a dual gfp-luxAB marker system. Appl. Environ. Microbiol. 65: 813 821.
119. Uroz, S.,, C. D’Angelo-Picard,, A. Carlier,, M. Elasri,, C. Sicot,, A. Petit,, P. Oger,, D. Faure,, and 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.
120. Van den Broek, D.,, T. F. C. Chin-A-Woeng,, K. Eijkemans,, I. H. M. Mulders,, G. V. Bloemberg,, and B. J. J. Lugtenberg. 2003. Biocontrol traits of Pseudomonas spp. are regulated by phase variation. Mol. Plant-Microbe Interact. 16: 1003 1012.
121. vanLoon, L. C.,, P. A. H. M. Bakker,, and C. M. J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36: 453 483.
122. von Bodman, S. B.,, W. D. Bauer,, and D. L. Coplin. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41: 455 482.
123. von Bodman S. B.,, D. R. Majerczak,, and D. L. Coplin. 1998. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA 95: 7687 7692.
124. 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.
125. Whitehead, N. A.,, J. T. Byers,, P. Commander,, M. J. Corbett,, S. J. Coulthurst,, L. Everson,, A. K. Harris,, C. L. Pemberton,, N. J. Simpson,, H. Slater,, D. S. Smith,, M. Welch,, N. Williamson,, and G. P. Salmond. 2002. The regulation of virulence in phytopathogenic Erwinia species: quorum sensing, antibiotics and ecological considerations. Antonie Van Leeuwenhoek 81: 223 231.
126. Whiteley, M.,, M. G. Bangera,, R. E. Bumgarner,, M. R. Parsek,, G. M. Teitzel,, S. Lory,, and E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413: 860 864.
127. Whitely, M.,, K. M. Lee,, and E. P. Greenberg. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96: 13904 13909.
128. Wilkinson, A.,, V. Danino,, F. Wisniewski-Dye,, J. K. Lithgow,, and J. A. Downie. 2002. Nacyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J. Bacteriol. 184: 4510 4509.
129. Wisniewski-Dye, F.,, and J. A. Downie. 2002. Quorum-sensing in Rhizobium. Antonie Van Leeuwenhoek 81: 397 407.
130. Wood, D. W.,, F. Gong,, M. M. Daykin,, P. Williams,, and L. S. Pierson III. 1997. N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. J. Bacteriol. 179: 7663 7670.
131. Xi, C.,, M. Lambrecht,, J. Vanderleyden,, and J. Michiels. 1999. Bi-functional gfp- and gusAcontaining mini-Tn5 transposon derivatives for combined gene expression and bacterial localization studies. J. Microbiol. Methods 35: 85 92.
132. Zhang, Z.,, and L. S. Pierson III. 2001. A second quorum-sensing system regulates cell surface properties but not phenazine antibiotic production in Pseudomonas aureofaciens. Appl. Environ. Microbiol. 67: 4305 4315.

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