Long- and short-chain plant-produced bacterial N-acyl-homoserine lactones become components of phyllosphere, rhizophere, and soil

Molecular Plant-Microbe Interactions

Volumn 19, Issue 3, 2006, Pages 227-239

  Scott, Russell A ^a   Weil, Jason ^a,d   Le, Phuong T ^a   Williams, Paul ^b   Fray, Rupert G ^b   Von Bodman, Susanne B ^c   Savka, Michael A ^a  

^a ROCHESTER INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Quorum sensing

Indexed keywords

DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; PLANT LEAF; PLANT ROOT; PSEUDOMONAS AERUGINOSA; SOIL; TOBACCO; TRANSGENIC PLANT; YERSINIA ENTEROCOLITICA;

4-BUTYROLACTONE; MOLECULAR STRUCTURE; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS AERUGINOSA; SOIL; TOBACCO; YERSINIA ENTEROCOLITICA;

BACTERIA (MICROORGANISMS); NICOTIANA TABACUM; PSEUDOMONAS AERUGINOSA; YERSINIA ENTEROCOLITICA;

EID: 33144471470     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-0227     Document Type: Article

References (67)

1. Barber, D. A., and Gunn, K. B. 1974. The effect of physical forces on the exudation of organic substances by the roots of cereal plants grown under sterile conditions. New Phytol. 73:39-45
2. Bevan, M. 1984. Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12:8711-8721.
3. Brelles-Marino, G., and Bedmar, E. J. 2001. Detection, purification and characterization of quorum sensing signal molecules in plant-associated bacteria. J. Biotechnol. 91:197-209.
4. Burmolle, M., Hansen, L. H., Oregaard, G., and Sorensen S. J. 2003. Presence of N-acyl homoserine lactones in soil detected by a whole-cell biosensor and flow cytometry. Microb. Ecol. 45:226-236.
5. Byer, J. J., Lucus, C., Salmond, G. P. C., and Welch M. 2002. Nonenzymatic turnover of an Erwinia carotovora quorum sensing signaling molecule. J. Bacteriol. 184:1163-1171.
6. Camara, M., Daykin, M., and Chhabra, S. R. 1998. Detection, Purification, and synthesis of N-acylhomoserine lactone quorum sensing signal molecules. Methods Microbiol. 27:319-330.
7. Cha, C., Gao, P., Chen, Y.-C., Shaw, P. D., and Farrand, S. K. 1998. Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11:1119-1129.
8. Chilton, M.-D., Currier, T. C., Farrand, S. K., Bendich, A. J., Gordon, M. P., and Nester, E. W. 1974. Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc. Natl. Acad. Sci. U.S.A. 71:3672-3676.
9. D'Angelo-Picard, C., Faure, D., Carlier, A., Uroz, S., Raffoux, A., Fray, R., and Dessaux, Y. 2004. Bacterial populations in the rhizosphere of tobacco plants producing the quorum-sensing signals hexanoyl-homoserine lactone and 3-oxo-hexanoyl-homoserine lactone. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 51:19-29.
10. Dong, Y. H., Xu, J. L., Li, X. Z., and Zhang, L. H. 2000. AiiA, and enzyme that inactivates the acyl-homoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. U.S.A. 97:3526-3531.
11. Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., and Zhang, L. H. 2001. Quenching quorum sensing-dependent bacterial infection by an N-acyl-homoserine lactonase. Nature 411:813-817.
12. Eberhard, A., Burlingame, A. L., Eberhard, C., Kenyon, G. L., and Nealson, K. H. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444-2449.
13. Eberl, L. 1999. N-acyl-homoserine-mediated gene regulation in Gram-negative bacteria. Syst. Appl. Microbiol. 22:493-506.
14. Farrand, S. K., Qin, Y., and Oger, P. 2002. Quorum-sensing system of Agrobacterium plasmids: Analysis and utility. Methods Enzymol. 358:452-484.
15. Fray, R. G., Throup, J. P., Daykin, M., Wallace, A., Williams, P., Stewart, G. S. A. B., and Grierson. D. 1999. Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nat. Biotechnol. 17:1017-1020.
16. Fuqua, C., Parsek, M. R., and Greenberg, E. P. 2001. Regulation of gene expression by cell-to-cell communication: Acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35:439-468.
17. Fuqua, C., and Winans, S. 1999. Signal generation in autoinduction systems: Synthesis of acylated homoserine lactones by LuxI-type proteins. Pages 211-230 in: Cell-Cell Signaling in Bacteria. G. M. Dunny and S. C. Winans, eds. American Society for Microbiology Press, Herndon, VA, U.S.A.
18. Gonzalez, J. E., and Marketon, M. M. 2003. Quorum sensing in nitrogen-fixing Rhizobia. Microbiol. Mol. Biol. Rev. 67(4):574-592.
19. Gould, T. A., Schweizer, H. P., and Churchill, M. E. A. 2004. Structure of the Pseudomonas aeruginosa acyl-homoserinelactone synthase LasI. Mol. Microbiol. 53(4):1135-1146.
20. Hawes, M. C., and Pueppke, S. G. 1986. Sloughed peripheral root cap cells: Yields from different plant species and callus formation from single cells. Am. J. Bot. 73:1466-1473.
21. Hawes, M. C., Gunawardena, U., Miyasaka, S., and Zhao, X. 2000. The role of root border cells in plant defense. Trends Plant Sci. 5(3):128-133.
22. Hood, E. E., Gelvin, S. B., Melchers, L. S., and Hoekema, A. 1993. New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 2:208-218.
23. Joseph, C. M., and Phillips, D. A. 2003. Metabolites from soil bacteria affect plant water relations. Plant Physiol. Biochem. 41:189-192.
24. Laue, B. E., Jiang, Y., Chhabra, S. R., Jacob, G., Stewart, G. S. A. B., Hardman, A., Downie, J. A., O'Gara, F., and Williams, P. 2000. The biocontrol strain Pseudomonas fluorsecens F113 produces the Rhizobium small bacteriocin, N-(3-hydro-7-cis-tetradesenoyl) homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146:2469-2480.
25. Leadbetter, J. R., and Greenberg, E. P. 2000. Metabolism of acyl-homoserine lactones quorum sensing signals by Variovorax paradoxus. J. Bacteriol. 182:6921-6926.
26. Loh, J., Pierson, E. A., Pierson, L. S., Stacey, G., and Chatterjee, A. 2002. Quorum sensing in plant-associated bacteria. Curr. Opin. Plant Biol. 5:285-290.
27. Lugtenberg, B. J. J., Dekker, L., and Bloemberg, G. V. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39:461-490.
28. Luo, Z.-Q., Clemente, T. E., and Farrand, S. K. 2001. Construction of a derivative of Agrobacterium tumefaciens C58 that does not mutate to tetracycline resistance. Mol. Plant-Microbe Interact. 14:98-103.
29. Mae, A., Montesano, M., Koiv, V., and Palva, E. T. 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.
30. Manefield, M., and Turner, S. L. 2002. Quorum sensing in context: Out of molecular biology and into microbial ecology. Microbiology 148:3762-3764.
31. McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S., Bycroft, B. W., Stewart, G. S. A. B., and Williams, P. 1997. Quorum-sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703-3711.
32. Miller, M. B., and Bassler, B. L. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165-199.
33. Minogue, T. D., Wehland-von Trebra, M., Bernhard, F., and von Bodman, S. B. 2002. Autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: Evidence for a repressor function. Mol. Microbiol. 44:1625-1635.
34. Minogue, T. D., Carlier, A.L., Koutsoudis, M. D., and von Bodman, S. B. 2005. The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. stewartii is a function of EsaR-mediated repression of the rcsA gene. Mol. Microbiol. 56:189-203.
35. Nealson, K. H. 1977. Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Arch. Microbiol. 112:73-79.
36. Newton, J. A., and Fray, R. G. 2004. Integration of environmental signals and host-derived signals with quorum sensing during plant-microbe interactions. Cell. Microbiol. 6(3):213-224.
37. Pearson, J. P., van Delden, C., and Iglewski, B. H. 1999. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 181:1203-1210.
38. Pierson, E. A., Wood, D. W., Cannon, J. A., Blachere, F. M., and Pierson, L. S., III. 1998. Interpopulation signaling via N-acylhomoserine lactones among bacteria in the wheat rhizosphere. Mol. Plant-Microbe Interact. 11:1078-1084.
39. Pierson, L. S., III, Wood, D. W., and von Bodman, S. B. 1999. Quorum sensing in plant-associated bacteria. Pages 101-116 in: Cell-Cell Signaling in Bacteria. G. M. Dunny and S. C. Winans, eds. American Society for Microbiology Press, Herndon, VA, U.S.A.
40. Ramey, B. E., Koutsoudis, M., von Bodman, S. B., and Fuqua, C. 2004. Biofilm formation in plant-microbe associations. Curr. Opin. Microbiol. 6:602-9.
41. Ravn, L., Christensen, A. B., Molin, S., Givskov, M., and Gram, L. 2001. Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of acyl-HSL-production kinetics. J. Microbiol. Methods 44:239-251.
42. Redfield, R. J. 2002. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10:365-370.
43. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, U.S.A.
44. Savka, M., A., and Binns, A. N. 2000. Introduction of DNA into plants. Pages 159-192 in: Gene Transfer Methods: Introduction of Genes into Living Cells and Organisms. P. A. Norton and L. F. Steel, eds. BioTechniques Books, Eaton Publishing, Natick, MA, U.S.A.
45. Savka, M. A., and Farrand, S. K. 1992. Mannityl opine accumulation and exudation by transgenic tobacco. Plant Physiol. 98:784-789.
46. Savka, M. A., and Farrand, S. K. 1997. Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat. Biotechnol. 15:363-368.
47. Savka, M. A., Dessaux, Y., Oger, P., and Rossbach, S. 2002. Engineering bacterial competitiveness and persistence in the phytosphere. Mol. Plant-Microbe Interact. 15:866-874.
48. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E., Rinehart, K. L., and Farrand, S. K. 1997. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. U.S.A. 94:6036-6041.
49. Steidle, A., Sigl, K., Schuhegger, R., Ihring, A., Schmid, M., Gantner, S., Stoffels, M., Riedel, K., Givskov, M., Hartman, A., Langebartels, C., and Eberl, L. 2001. Visualization of N-acylhomoserine lactones-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67(12):5761-5770.
50. Stevens, A. M., and Greenberg, E. P. 1997. Quorum sensing in Vibrio fischeri: Essential elements for activation of the luminescence genes. J. Bacteriol. 179:557-562.
51. Swift, S., Karlyshev, A. V., Fish, L., Durant, E. L., Winson, M. K., Chhabra, S. R., Williams, P., Macintyre, S., and Stewart, G. S. 1997. Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: Identification of the LuxI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J. Bacteriol. 179:5271-5281.
52. Taga, M. E., and Bassler, B. L. 2003. Chemical communication among bacteria. Proc. Natl. Acad. Sci. U.S.A. 100:14549-14554.
53. Toth, I. K., Newton, J. A., Hyman, L. J., Lees, A. K., Daykin, M., Ortori, C., Williams, P., and Fray, R. G. 2004. Potato plants genetically modified to produce N-acylhomoserine lactones increase susceptibility to soft rot Erwinia. Mol. Plant-Microbe Interact. 17:880-887.
54. von Bodman, S. B., Majerczak, D. R., and Coplin D. L. 1998. Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by the N-acyl-homoserine lactone autoinducer. J. Bacteriol. 177:5000-5008.
55. von Bodman, S. B., Bauer, W. D., and Coplin D. L. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:455-482.
56. Wang, Y.-J. and Leadbetter, J. R. 2005. Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Appl. Environ. Microbiol. 71:1291-1299.
57. Watson, T. W., Minogue, T. D., Val, D. L., von Bodman, S. B., and Churchill, M. E. A. 2002. Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol. Cell 9:685-694.
58. Whitehead, N. A., Barnard A. M. I., Slater, H., Simpson N. J. L., and Salmond, G. P. C. 2001. Quorum sensing in gram-negative bacteria. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 25:365-404.
59. Whitehead, N. A., Byers, J. T., Commander, P., Corbett, M. J., Coulthurst, S. J., Everson, L., Harris, A. K. P., Pemberton. C. L., Simpson, N. J. L., Slater, H., Smith, D. S., Welch, M., Williamson, N., and Salmond, G. P. C. 2002. The regulation of virulence in phytopathogenic Erwinia species: Quorum sensing, antibiotics and ecological considerations. Antonie Leeuwenhoek 81:223-231.
60. Winans, S. C., Zhu, J., and More, M. I. 1999. Cell density-dependent gene expression by Agrobacterium tumefaciens during colonization of crown gall tumors. Pages 117-128 in: Cell-Cell Signaling in Bacteria. G. M. Dunny and S. C. Winans, eds. ASM Press.
61. Winson, M. K., Swift, S., Fish, L., Throup, J. P., Jorgensen, F., Chhabra, S. R., Bycroft, B. W., Williams, P., and Stewart, G. S. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl-homoserine lactone-mediated quorum sensing. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 163:185-192.
62. Winzer, K., and Williams, P. 2001. Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. Int. J. Med. Microbiol. 291:131-143.
63. Yanisch-Perron, C., Vierira, J., and Messing, J. 1985. Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
64. Yates, E. A., Philipp, B., Buckley, C., Atkinson, S., Chhabra, S.R., Sockett, R. E., Goldner, M., Dessaux, Y., Camara, M., Smith, H., and Williams, P. 2002. N-acylhomoserine lactones undergo lactonlysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 70(10):5635-5646.
65. Zhang, L.-H. 2003. Quorum quenching and proactive host defense. Trends Plant Sci. 8(5):238-244.
66. Zhang, L.-H., and Dong, Y.-H. 2004. Quorum sensing and signal interference: Diverse implications. Mol. Microbiol. 53(6):156-1571.
67. Zheng, D. H., Zhang, S., Carle, S., Hao, G., Holden, M. R., and Burr, T. J. 2003. A luxR homolog, aviR, in Agrobacterium vitis is associated with induction of necrosis on grape and a hypersensitive response on tobacco. Mol. Plant-Microbe Interact. 16:650-658.