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  • Research Article
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Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria

Abstract

N-acylhomoserine lactones (AHLs) play a critical role in plant/microbe interactions. The AHL, N-(3-oxohexanoyl)-L-homoserine lactone (OHHL), induces exoenzymes that degrade the plant cell wall by the pathogenic bacterium Erwinia carotovora. Conversely, the antifungal activity of the biocontrol bacterium Pseudomonas aureofaciens 30–84 is due (at least in part) to phenazine antibiotics whose synthesis is regulated by N-hexanoylhomoserine lactone (HHL). Targeting the product of an AHL synthase gene (yenI) from Yersinia enterocolitica to the chloroplasts of transgenic tobacco plants caused the synthesis in plants of the cognate AHL signaling molecules (OHHL and HHL). The AHLs produced by the transgenic plants were sufficient to induce target gene expression in several recombinant bacterial AHL biosensors and to restore biocontrol activity to an HHL-deficient P. aureofaciens strain. In addition, pathogenicity was restored to an E. carotovora strain rendered avirulent as a consequence of a mutation in the OHHL synthase gene, carI. The ability to generate bacterial quorum-sensing signaling molecules in the plant offers novel opportunities for disease control and for manipulating plant/microbe interactions.

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Figure 1: Production of signaling molecules by transgenic plants.
Figure 2
Figure 3: Bacterial responses to leaves and roots of transgenic plants.

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References

  1. Fuqua, W.C., Winans, S.C. & Greenberg, E.P. Quorum sensing in bacteria: the LuxR-LuxI family of cell density responsive transcriptional regulators. J. Bacteriol. 176, 269–275 ( 1994).

    Article  CAS  Google Scholar 

  2. Salmond, G.P.C., Bycroft, B.W., Stewart, G.S.A.B. & Williams, P. The bacterial enigma: cracking the code of cell-cell communication. Mol. Microbiol. 16, 615–624 (1995).

    Article  CAS  Google Scholar 

  3. Swift, S., Throup, J.P., Williams, P., Salmond, G.P.C. & Stewart, G.S.A.B. Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends in Biological Science 21, 214–219 (1996).

    Article  CAS  Google Scholar 

  4. Swift, S. et al. A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria. Mol. Microbiol. 10, 511– 520 (1993).

    Article  CAS  Google Scholar 

  5. Bainton, N.J. et al. N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288, 997–1004 (1992).

    Article  CAS  Google Scholar 

  6. Jones, S. et al. The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12, 2477–2482 (1993).

    Article  CAS  Google Scholar 

  7. McGowan, S.J. et al. Analysis of bacterial carbapenem antibiotic production genes reveals a novel β-lactam biosynthesis pathway. Mol. Microbiol. 22, 415–426 (1996).

    Article  CAS  Google Scholar 

  8. McClean, K.H. et al. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143, 3703– 3711 (1997).

    Article  CAS  Google Scholar 

  9. Cherenin, L.S. et al. Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J. Bacteriol. 180 4435–4441 (1998).

    Google Scholar 

  10. Wood, D.W. & Pierson, L.S. The phzI gene of Pseudomonas aureofaciens 30–84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene 168, 49–53 (1996).

    Article  CAS  Google Scholar 

  11. Wood, D.W., Gong, F.C., Daykin, M.M., Williams, P. & Pierson, L.S. N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30–84 in the wheat rhizosphere. J. Bacteriol 179, 7663–7670 (1997).

    Article  CAS  Google Scholar 

  12. Throup, J.P. et al. Characterization of the YenI/YenR locus from Yersinia enterocolitica mediating the synthesis of 2 N-acylhomoserine lactone signal molecules. Mol. Microbiol. 17, 345– 356 (1995).

    Article  CAS  Google Scholar 

  13. More, M.L. et al. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272, 1655– 1658 (1996).

    Article  CAS  Google Scholar 

  14. Val, D.E. & Cronan, J.E. Jr. In vivo evidence that S-adenosylmethionine and fatty acid synthesis intermediates are the substrates for the LuxI family of autoinducer synthases. J. Bacteriol. 180, 2644–2651 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Jiang, Y. et al. In vitro biosynthesis of the Pseudomonas aeruginosa quorum sensing signal molecule, N-butanoyl-L-homoserine lactone. Mol. Microbiol. 28, 193–203 (1998).

    Article  CAS  Google Scholar 

  16. Winson, M.K. et al. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163, 185– 192 (1998).

    Article  CAS  Google Scholar 

  17. Pirhonen, M., Flego, D., Heikineimo, R. & Palva, E.T. A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora . EMBO J. 12, 2467– 2476 (1993).

    Article  CAS  Google Scholar 

  18. Perombelon, M.C.M. & Kelman, A. Ecology of the soft rot erwinias. Annu. Rev. Phytopathol. 18, 361–387 (1980).

    Article  Google Scholar 

  19. Palva, T.K., Hurtig, M., Saindrenan, P. & Palva E.T. Salicylic acid induced resistance to Erwinia carotovora subsp. carotovora in tobacco. Molecular Plant-Microbe Interactions 7, 356–363 ( 1994).

    Article  CAS  Google Scholar 

  20. Gray, K.M., Pearson, J.P., Downie, J.A., Boboye, B.E.A. & Greenberg, E.P. Cell-to-cell signalling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178, 372–376 ( 1996).

    Article  CAS  Google Scholar 

  21. Schripsema, J. et al. Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-L-homoserine lactone molecules known as autoinducers and as quorum sensing co-transcriptional factors. J. Bacteriol. 178, 366–371 ( 1996).

    Article  CAS  Google Scholar 

  22. Toyota, K. & Ikeda, K. Relative importance of motility and antibibiosis in the rhizoplane competence of a biocontrol agent Pseudomonas fluorescens MelRC2Rif. Biol. Fert. Soils 25, 416–420 (1997).

    Article  Google Scholar 

  23. Becker, J.O. & Schwinn, F.J. Control of soil-borne pathogens with living bacteria and fungi—status and outlook. Pesticide Science 37, 355–363 ( 1993).

    Article  Google Scholar 

  24. Shaw, P.D. et al. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. USA 94, 6036–6041 (1997).

    Article  CAS  Google Scholar 

  25. Datla, R.S.S. et al. Improved high-level constitutive foreign gene expression in plants using an AMV RNA4 untranslated leader sequence. Plant Sci. 94, 139–149 (1993).

    Article  CAS  Google Scholar 

  26. Pietrzak, M., Shillito, R.D., Hohn, T. & Potrykus, I. Expression in plants of two bacterial antibiotic resistance genes after protoplast transformation with a new plant expression vector. Nucleic Acids Res. 14, 5857–5868 (1986).

    Article  CAS  Google Scholar 

  27. Bevan, M. Binary agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711–8721 (1984).

    Article  CAS  Google Scholar 

  28. Dean, C. et al. Molecular characterization of the rbcS multi-gene family of petunia (Mitchell). Mol. Gen. Genet. 206, 465– 474 (1987).

    Article  CAS  Google Scholar 

  29. Draper, J., Scott, R., & Hamil, J. in Plant genetic transformation and gene expression, a laboratory manual. (eds Draper J., Scott R., Armitage P. & Walden R) 69–160 (Blackwell Scientific Publications, London; 1988).

    Google Scholar 

  30. Camara, M., Daykin, M. & Chhabra, S.K. in Methods in microbiology: bacterial pathogenesis. Vol. 27 (eds Williams P.H., Salmond G. & Ketley J.) 319–330 Academic Press, London; 1998 ).

    Book  Google Scholar 

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Acknowledgements

We thank Barrie Bycroft for helpful discusions, Siri Ram Chhabra for providing synthetic AHLs, and Sandy Pierson for the P. aureofaciens phzI mutant. This work was supported by a Biotechnology and Biological Sciences Research Council Sir David Phillips Fellowship awarded to R.G.F. and by grants from the Biotechnology and Biological Sciences Research Council and the Wellcome Trust to D.G., P.W., and G.S.A.B.S., which are gratefully acknowledged.

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Correspondence to Rupert G. Fray.

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Fray, R., Throup, J., Daykin, M. et al. Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nat Biotechnol 17, 1017–1020 (1999). https://doi.org/10.1038/13717

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