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Quorum-sensing in Rhizobium

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Abstract

Quorum-sensing signals are found in many species of legume-nodulating rhizobia. In a well-characterized strain of R. leguminosarum biovar viciae, a variety of autoinducers are synthesised, and all have been identified as N-acyl-homoserine lactones. One of these N-acyl-homoserine lactones, is N-(3-hydroxy-7-cis-tetradecenoyl)-L-homoserine lactone, previously known as small bacteriocin, which inhibits the growth of several R. leguminosarum strains. The cinRI locus is responsible for the production of small bacteriocin. CinR induces cinI in response to the AHL made by CinI, thus forming a positive autoregulatory induction loop. A complex cascade of quorum-sensing loops was characterized, in which the cinIR locus appears to be the master control for three other AHL-dependent quorum-sensing control systems. These systems include the raiI/raiR, traI/triR and rhiI/rhiR. Other rhizobial strains appear to share some of these quorum sensing loci, but not all loci are found in all strains. Small bacteriocin along with the other N-acyl-homoserine lactones produced by these three AHL-based control systems regulate (i) growth inhibition of sensitive strains, (ii) transfer of the symbiotic plasmid pRL1JI, and (iii) expression of the rhizosphere-expressed (rhi) genes that influence nodulation. Some of the genes regulated by these systems have been identified. While the functions of some, such as the trb operon regulated by triR are clear, several of the regulated genes have no homologues of known function. It is anticipated that several other genes regulated by these systems have yet to be identified. Therefore, despite the regulation of one of the most complex quorum-sensing cascade being understood, several of the functions regulated by the quorum-sensing genes remain to be elucidated.

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References

  • Andersen JB, Heydorn A, Hentzer M, Eberl L, Geisenberger O, Christensen BB, Molin S & Givskov M(2001) gfp-based N-acylhomoserine-lactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67: 575–585.

    Article  PubMed  CAS  Google Scholar 

  • Bassler BL, Wright M, Showalter RE & Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9: 773–786.

    PubMed  CAS  Google Scholar 

  • Bassler BL, Wright M & Silverman MR (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13: 273–286.

    PubMed  CAS  Google Scholar 

  • Beck von Bodman S, Hayman GT & Farrand SK (1992) Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. Proc. Natl. Acad. Sci. USA 89: 643–647.

    Article  PubMed  CAS  Google Scholar 

  • Brewin NJ, Beringer JE, Buchanan-Wollaston AV, Johnston AWB & Hirsch PR (1980) Transfer of symbiotic genes with bacteriocinogenic plasmids in Rhizobium leguminosarum. J. Gen. Microbiol. 116: 261–270.

    CAS  Google Scholar 

  • Callahan SM & Dunlap PV (2000) LuxR-and acyl-homoserinelactone-controlled non-lux genes define a quorum-sensing regulon in Vibrio fischeri. J. Bacteriol. 182: 2811–2822.

    Article  PubMed  CAS  Google Scholar 

  • Cha C, Gao P, Chen Y-C, Shaw PD & Farrand SK (1998) Production of acyl-homoserine lactone quorum-sensing signals by Gramnegative plant-associated bacteria. Mol. Plant-Microbe Interact. 11: 1119–1129.

    PubMed  CAS  Google Scholar 

  • Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL & Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545–549.

    Article  PubMed  CAS  Google Scholar 

  • Cubo MT, Economou A, Murphy G, Johnston AWB & Downie JA (1992) Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J. Bacteriol. 174: 4026–4035.

    PubMed  CAS  Google Scholar 

  • Daniels R, De Vos DE, Desair J, Raedschelders G, Luyten E, Rosemeyer V, Verreth C, Schoeters E, Vanderleyden J & Michiels J (2002) The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J. Biol. Chem. 277: 462–468.

    Article  PubMed  CAS  Google Scholar 

  • Dibb NJ, Downie JA & Brewin NJ (1984) Identification of a rhizosphere protein encoded by the symbiotic plasmid of Rhizobium leguminosarum. J. Bacteriol. 158: 621–627.

    PubMed  CAS  Google Scholar 

  • Dong YH, Xu JL, Li XZ & Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserinelactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97: 3526–3531.

    Article  PubMed  CAS  Google Scholar 

  • Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF & Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813–817.

    Article  PubMed  CAS  Google Scholar 

  • Dong YH, Gusti AR, Zhang Q, Xu JL & Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68: 1754–1759.

    Article  PubMed  CAS  Google Scholar 

  • Eberhard A, Burlingame AL, Eberhard C, Keenyon GL, Nealson KH & Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444–2449.

    Article  PubMed  CAS  Google Scholar 

  • Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S & Givskov M (1996) Involvement of N-acyl-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20: 127–136.

    PubMed  CAS  Google Scholar 

  • Eberl L (1999) N-acyl homoserine lactone-mediated gene regulation in gram-negative bacteria. Syst. Appl. Microbiol. 22: 493–506.

    PubMed  CAS  Google Scholar 

  • Economou A, Hawkins FKL, Downie JA & Johnston AWB (1989) Transcription of rhiA, a gene on a Rhizobium leguminosarum bv. viciae Sym plasmid, requires rhiR and is repressed by flavonoids that induce nod genes. Mol. Microbiol. 3: 87–93.

    PubMed  CAS  Google Scholar 

  • Engebrecht J, Nealson K & Silverman M (1983) Bacterial luminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32: 773–781.

    Article  PubMed  CAS  Google Scholar 

  • Engebrecht J & Silverman M (1984) Identification of genes and gene products necessary for bacterial luminescence. Proc. Natl. Acad. Sci. USA 81: 4154–4158.

    Article  PubMed  CAS  Google Scholar 

  • Flavier AB, Ganova-Raeva LM, Schell MA & Denny TP (1997) Hierarchical atoinduction 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.

    PubMed  CAS  Google Scholar 

  • Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stewart GSAB & Grieson D (1999) Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nature Biotech. 17: 1017–1020.

    Article  CAS  Google Scholar 

  • Freiberg C, Fellay R, Bairoch A, BroughtonWJ, Rosenthal A & Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387: 394–401.

    Article  PubMed  CAS  Google Scholar 

  • Fuqua WC, Winans SC & Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269–275.

    PubMed  CAS  Google Scholar 

  • Fuqua C & Greenberg EP (1998) Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr. Opin. Microbiol. 1: 183–189.

    Article  PubMed  CAS  Google Scholar 

  • Gill RE & Cull MG (1986) Control of developmental gene expression by cell-to-cell interactions in Myxococcus xanthus. J Bacteriol. 168: 341–347.

    PubMed  CAS  Google Scholar 

  • Gilson L, Kuo A & Dunlap PV (1995) AinS and a new family of autoinducer synthesis proteins. J. Bacteriol. 177: 6946–6951.

    PubMed  CAS  Google Scholar 

  • Goel AK, Sindhu SS & Dadarwal KR (1999) Bacteriocin-producing native rhizobia of green gram (Vigna radiata) having competitive advantage in nodule occupancy. Microbiol. Res. 154: 43–48.

    CAS  Google Scholar 

  • Gray KM, Pearson JP, Downie JA, Boboye BEA & Greenberg EP (1996) Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372–376.

    PubMed  CAS  Google Scholar 

  • Hirsch PR (1979) Plasmid-determined bacteriocin production by Rhizobium leguminosarum. J. Gen. Microbiol. 113: 219–228.

    CAS  Google Scholar 

  • Hirsch PR, van Montagu M, Johnston AWB, Brewin NJ & Schell J (1980) Physical identification of bacteriocinogenic, nodulation plasmids in strains of Rhizobium leguminosarum. J. Gen. Microbiol. 120: 403–412.

    Google Scholar 

  • Holden MTG, Chhabra SR, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg S & Williams P (1999) Quorum-sensing cross-talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol. Microbiol. 33: 1254–1266.

    Article  PubMed  CAS  Google Scholar 

  • Horinouchi S & Beppu T (1990) Autoregulatory factors of secondary metabolism and morphogenesis in actinomycetes. Crit. Rev. Biotechnol. 10: 191–204.

    PubMed  CAS  Google Scholar 

  • Johnston AWB, Beynon JL, Buchanan-Wollaston AV, Stetchell SM, Hirsch P & Beringer JE (1978) High frequency transfer of nodulating ability between strains and species of Rhizobium. Nature 276: 634–636.

    Article  Google Scholar 

  • Hwang I, Li P-L, Zhang L, Piper KR, Cook DM, Tate ME & Farrand SK (1994) TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. Proc. Natl. Acad. Sci. USA 91: 4639–4643.

    Article  PubMed  CAS  Google Scholar 

  • Laue RE, Jiang Y, Chhabra SR, Jacob S, Stewart GSAB, Hardman A, Downie JA, O'Gara F & Williams P (2000) The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146: 2469–2480.

    PubMed  CAS  Google Scholar 

  • Leadbetter JR & Greenberg EP (2000) Metabolism of acylhomoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182: 6921–6926.

    Article  PubMed  CAS  Google Scholar 

  • Lilley BN & Bassler BL (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma-54. Mol. Microbiol. 36: 940–954.

    Article  PubMed  CAS  Google Scholar 

  • Lithgow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P & Downie JA (2000) The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol. Microbiol. 37: 81–97.

    Article  PubMed  CAS  Google Scholar 

  • Lithgow JK, Danino VE, Jones J & Downie JA (2001) Analysis of N-acyl homoserine-lactone quorum-sensing molecules made by different strains and biovars of Rhizobium leguminosarum containing different symbiotic plasmids. Plant and Soil 232: 3–12.

    Article  CAS  Google Scholar 

  • Loh JT, Yuen-Tsai JPY, Stacey MG, Lohar D, Welborn A & Stacey G (2001) Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes. Mol. Microbiol. 42: 37–46.

    Article  PubMed  CAS  Google Scholar 

  • Lotz W & Mayer F (1982) Isolation and characterization of a bacteriophage tail-like bacteriocin from a strain of Rhizobium. J. Virol. 9: 160–173.

    Google Scholar 

  • Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P & Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145: 283–291.

    Article  PubMed  CAS  Google Scholar 

  • Manefield M, Welch M, Givskov M, Salmond GPC & Kjelleberg S (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.

    Article  PubMed  CAS  Google Scholar 

  • McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Swift S, Bycroft BW, Stewart GSAB & 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.

    PubMed  CAS  Google Scholar 

  • McKenney D, Brown KE & Allison DG (1995) Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication. J. Bacteriol. 177: 6989–6992.

    PubMed  CAS  Google Scholar 

  • Nealson KH, Platt T & Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104: 313–322.

    PubMed  CAS  Google Scholar 

  • Oresnik IJ, Twelker S & Hynes MF (1999) Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl. Environ. Microbiol. 65: 2833–2840.

    PubMed  CAS  Google Scholar 

  • Passador L, Cook JM, Gambello MJ, Rust L & Iglewski BH (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260: 1127–1130.

    PubMed  CAS  Google Scholar 

  • Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS, Greenberg EP & Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96: 11229–11234.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Priem WJE & Wijffelman CA (1984) Selection of strains cured of the Rhizobium leguminosarum Sym-plasmid pRL1JI by using small bacteriocin. FEMS Microbiol. Lett. 25: 247–251.

    Article  CAS  Google Scholar 

  • Puskas A, Greenberg EP, Kaplan S & Schaefer AL (1997) A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J. Bacteriol. 179: 7530–7537.

    PubMed  CAS  Google Scholar 

  • Reverchon S, Bouillant ML, Salmond G & Nasser W (1998) Integration of the quorum-sensing system in the regulatory networks controlling virulence factor synthesis in Erwinia chrysanthemi. Mol Microbiol. 29: 1407–1418.

    Article  PubMed  CAS  Google Scholar 

  • Rodelas B, Gonzalez-Lopez J, Salmeron V, Martinez-Toledo MV & Pozo C (1998) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv viceae isolated from agricultural soils in Spain. Appl. Soil Ecol. 8: 51–60.

    Article  Google Scholar 

  • Rodelas B, Lithgow JK, Wisniewski-Dyé F, Hardman A, Wilkinson A, Economou A, Williams P & Downie JA (1999) Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 181: 3816–3823.

    PubMed  CAS  Google Scholar 

  • Rosemeyer V, Michiels J, Verreth C & Vanderleyden J (1998) luxIand luxR-homologous genes of Rhizobium etli CNPAF512 contribute to synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J. Bacteriol. 180: 815–821.

    PubMed  CAS  Google Scholar 

  • Schripsema J, deRudder KEE, vanVliet TB, Lankhorst PP, deVroom E, Kijne JW & vanBrussel AAN (1996) Bacteriocin small of Rhizobium leguminosarium belongs to the class of N-acyl-1-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J. Bacteriol. 178: 366–371.

    PubMed  CAS  Google Scholar 

  • Schwinghamer EA & Brockwell J (1978) Competitive advantage of bacteriocin and phage-producing strains of Rhizobium trifolii in mixed culture. Soil Biol. Biochem. 10: 383–387.

    Article  CAS  Google Scholar 

  • Shadel GS & Baldwin TO (1991) The Vibrio fischeri LuxR protein is capable of bidirectional stimulation of transcription and both positive and negative regulation of the luxR gene. J. Bacteriol. 173: 568–574.

    PubMed  CAS  Google Scholar 

  • Shaw PD, Ping G, Daly SL, Cha C, Cronan JE, Rinehart KL & Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin layer chromatography. Proc. Natl. Acad. Sci. USA 94: 6036–6041.

    Article  PubMed  CAS  Google Scholar 

  • Sourjik V, Muschler P, Scharf B & Schmitt R (2000) VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J Bacteriol. 182: 782–788.

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Robinson JB & Bauer WD (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.

    PubMed  CAS  Google Scholar 

  • Thorne SH & Williams HD (1997) Adaptation to nutrient starvation in Rhizobium leguminosarum bv. phaseoli: analysis of survival, stress resistance, and changes in macromolecular synthesis during entry to and exit from stationary phase. J. Bacteriol. 179: 6894–6901.

    PubMed  CAS  Google Scholar 

  • Thorne SH & Williams HD (1999) Cell density-dependent starvation survival of Rhizobium leguminosarum bv. phaseoli: identification of the role of an N-acyl homoserine lactone in adaptation to stationary-phase survival. J. Bacteriol. 181: 981–990.

    PubMed  CAS  Google Scholar 

  • van Brussel AA, Zaat SA, Wijffelman CA, Pees E & Lugtenberg BJ (1985) Bacteriocin small of fast-growing rhizobia is chloroform soluble and is not required for effective nodulation. J. Bacteriol. 162: 1079–1082.

    PubMed  CAS  Google Scholar 

  • Whiteley M, Lee KM & Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96: 13904–13909.

    Article  PubMed  CAS  Google Scholar 

  • Whiteley M, Parsek MR & Greenberg (2000) Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J. Bacteriol. 182: 4356–4360.

    Article  PubMed  CAS  Google Scholar 

  • Wijffelman CA, Pees E, van Brussel AAN & Hooykaas PJJ (1983) Repression of small bacteriocin excretion in Rhizobium leguminosarum and Rhizobium trifolii by transmissible plasmids. Mol. Gen. Genet. 192: 171–176.

    Article  CAS  Google Scholar 

  • Wilkinson A, Danino V, Wisniewski-Dyé F, Lithgow JK & Downie JA (2002) N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J. Bacteriol. in press.

  • Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GPC, Bycroft BW, Lazdunski A, Stewart GSAB & Williams P (1995) Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92: 9427–9431.

    Article  PubMed  CAS  Google Scholar 

  • Winson MK, Swift S, Fish L, Throup JP, Jφrgensen F, Chhabra SR, Bycroft B, Williams P & Stewart GSAB (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum-sensing. FEMS Microbiol. Lett. 163: 185–192.

    Article  PubMed  CAS  Google Scholar 

  • Winzer K, Hardie KR & Williams P (2002a) Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch ! Curr. Opin. Microbiol. 5: 216–222.

    Article  PubMed  CAS  Google Scholar 

  • Winzer K, Hardie KR, Burgess N, Doherty N, Kirke D, Holden MTG, Linforth R, Cornell KA, Taylor AJ, Hill PJ & Williams P (2002b) LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148: 909–922.

    PubMed  CAS  Google Scholar 

  • Wisniewski-Dyé F, Jones J, Chhabra SR & Downie JA (2002) raiIR genes are part of a quorum-sensing network controlled by CinI and CinR in Rhizobium leguminosarum J. Bacteriol. 184: 1597–1606.

    Article  PubMed  CAS  Google Scholar 

  • Young JPW & Wexler M (1988) Sym plasmid and chromosomal genotypes are correlated in field populations of Rhizobium leguminosarum. J. Gen. Microbiol. 134: 2371–2391.

    Google Scholar 

  • Zhang L, Murphy PJ, Kerr A & Tate ME (1993) Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones. Nature 362: 446–448.

    Article  PubMed  CAS  Google Scholar 

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  1. Laboratoire d'Écologie Microbienne, UMR-CNRS 5557, Université, Lyon 1, 69622, Villeurbanne cedex, France

    Florence Wisniewski-Dyé

  2. John Innes Centre, Colney, Norwich, NR4 7UH, UK

    J. Allan Downie

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Wisniewski-Dyé, F., Downie, J.A. Quorum-sensing in Rhizobium . Antonie Van Leeuwenhoek 81, 397–407 (2002). https://doi.org/10.1023/A:1020501104051

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