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

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Bacterial Biofilms on Plants: Relevance and Phenotypic Aspects, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap08-2.gif


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
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


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. 19:23042314.
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. 3:397406.
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. 67:575585.
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. 64:22402246.
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 417:141147.
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 99:1240312408.
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. 45:3949.
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. 66:45034509.
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. 63:45434551.
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. 13:11701176.
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. 16:983993.
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 100:1018110186.
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. 69:49894993.
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. 11:11191129.
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. 13:13401345.
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. 11:10691077.
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. 10:7986.
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. 14:969979.
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. 60:473481.
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. 185:10271036.
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 280:295298.
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. 13:11771183.
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. 15:11731180.
25. D’Haeze, W.,, and M. Holsters. 2002. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79105.
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: 17541759.
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 411:813817.
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 97:35263531.
29. Dorr, J.,, T. Hurek,, and B. Reinhold-Hurek. 1998. Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol. Microbiol. 30:717.
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 87:12501257.
31. Duffy, B.,, A. Schouten,, and J. M. Raaijmakers. 2003. Pathogen self-defense: mechanism to counteract microbial antagonism. Annu. Rev. Phytopathol. 41:501538.
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: 11981209.
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. 182:23632369.
34. Fett, W. F.,, and P. H. Cooke. 2003. Scanning electron microscopy of native biofilms on mung bean sprouts. Can. J. Microbiol. 49:4550.
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. 179:70897097.
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. 17:10171020.
37. Fuqua, C.,, and E. P. Greenberg. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3:685695.
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. 63:43404345.
39. Gage, D. J. 2002. Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J. Bacteriol. 184:70427046.
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. 178:71597166.
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 293:668672.
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 294:23232328.
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. 178:372376.
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. 6:2028.
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 295:17221726.
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. 14:13511363.
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. 13:232237.
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 148:87102.
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. 22:38033815.
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. 14:10111020.
51. Hogan, D. A.,, and R. Kolter. 2002. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296:22292232.
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 33:10381043.
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. 7:331338.
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. 9:189197.
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. 48:15111524.
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. 14:10961104.
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. 15:734741.
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. 51:97113.
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 390:249256.
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. 15:172179.
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 146:24692480.
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: 39193924.
63. Lee, S. W.,, and D. A. Cooksey. 2000. Genes expressed in Pseudomonas putida during colonization of a plant-pathogenic fungus. Appl. Environ. Microbiol. 66:27642772.
64. Leveau, J. H.,, and S. E. Lindow. 2002b. Bioreporters in microbial ecology. Curr. Opin. Microbiol. 5:259265.
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 98:34463453.
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. 47:849860.
67. Lindow, S. E.,, and J. H. J. Leveau. 2002. Phyllosphere microbiology. Curr. Opin. Biotechnol. 13:238243.
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 147:32153229.
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. 5:285290.
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. 33:1119.
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 81:373383.
72. Lugtenberg, B. J. J.,, L. Dekkers,, and G. V. Bloemberg. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39:461490.
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. 1:439446.
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. 14:10351042.
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: 131138.
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. 16:743751.
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 0:14441449.
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. 64:23412345.
79. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289314.
80. Miller, M. B.,, and B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165199.
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. 4:799808.
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 91:873881.
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. 68:22292235.
84. O’Toole, G.,, H. B. Kaplan,, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:4979.
85. O’Toole, G. A.,, and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295304.
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 149:15411550.
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. 11:10781084.
88. Preston, G. M.,, N. Bertrand,, and P. B. Rainey. 2001. Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25 . Mol. Microbiol. 41:9991014.
89. Raaijmakers, J. M.,, M. Vlami,, and J. T. de Souza. 2002. Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek 81:537547.
90. Rainey, P. B. 1999. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1:243257.
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. 97:243252.
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: 801809.
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 12:32373244.
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: 923932.
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. 11:10481056.
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: 497502.
97. Schembri, M. A.,, K. Kjaergaard,, and P. Klemm. 2003. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48:253267.
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. 182:12151225.
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. 178:366371.
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: 514520.
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. 9:600607.
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 406:151157.
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 96:47864790.
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. 1:495502.
105. Smith, R. S., and B. H. Iglewski. 2003. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6:5660.
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. 552:110114.
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. 50:1527.
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. 24:487506.
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. 67:57615770.
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 406:959964.
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. 13:10631069.
113. Sutherland, I. W. 2001. The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol. 9:222227.
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. 45:199270.
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: 637648.
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. 65:36743680.
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. 41:290300.
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. 65:813821.
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 149:19811989.
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. 16:10031012.
121. vanLoon, L. C.,, P. A. H. M. Bakker,, and C. M. J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453483.
122. von Bodman, S. B.,, W. D. Bauer,, and D. L. Coplin. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:455482.
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 95:76877692.
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. 185:20802095.
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: 223231.
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: 860864.
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 96:1390413909.
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: 45104509.
129. Wisniewski-Dye, F.,, and J. A. Downie. 2002. Quorum-sensing in Rhizobium. Antonie Van Leeuwenhoek 81:397407.
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. 179:76637670.
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 35:8592.
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. 67:43054315.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error