J. Bacteriol., Jan 1996, 372-376, Vol 178, No. 2
Copyright © 1996, American Society for Microbiology

Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes

KM Gray, JP Pearson, JA Downie, BE Boboye and EP Greenberg
Department of Microbiology, University of Iowa, Iowa City 52242, USA.

The Sym plasmid pRL1JI encodes functions for the formation of nitrogen- fixing pea root nodules by Rhizobium leguminosarum. Some of the nodulation genes are involved in recognition of chemical signals produced by the plant root, and others are required for production of chemical signals recognized by the plant. pRL1JI also contains a regulatory gene, rhiR, that is homologous to luxR, the transcriptional activator of luminescence genes in Vibrio fischeri. LuxR requires a signal compound, an autoinducer, for its activity. We have identified an R. leguminosarum autoinducer that, together with RhiR, is required to activate both the rhizosphere-expressed rhiABC operon and a growth- inhibiting function encoded by pRL1JI. This intercellular signal is an N-acylated homoserine lactone structurally related to the V. fischeri and other autoinducers. These findings indicate a new level of intercellular communication in root nodule formation.

This article has been cited by other articles:

• Zilliges, Y., Kehr, J.-C., Mikkat, S., Bouchier, C., de Marsac, N. T., Borner, T., Dittmann, E. (2008). An Extracellular Glycoprotein Is Implicated in Cell-Cell Contacts in the Toxic Cyanobacterium Microcystis aeruginosa PCC 7806. J. Bacteriol. 190: 2871-2879 [Abstract] [Full Text]  
• Flodgaard, L. R., Dalgaard, P., Andersen, J. B., Nielsen, K. F., Givskov, M., Gram, L. (2005). Nonbioluminescent Strains of Photobacterium phosphoreum Produce the Cell-to-Cell Communication Signal N-(3-Hydroxyoctanoyl)homoserine Lactone. Appl. Environ. Microbiol. 71: 2113-2120 [Abstract] [Full Text]  
• Ulrich, R. L. (2004). Quorum Quenching: Enzymatic Disruption of N-Acylhomoserine Lactone-Mediated Bacterial Communication in Burkholderia thailandensis. Appl. Environ. Microbiol. 70: 6173-6180 [Abstract] [Full Text]  
• Hoang, H. H., Becker, A., Gonzalez, J. E. (2004). The LuxR Homolog ExpR, in Combination with the Sin Quorum Sensing System, Plays a Central Role in Sinorhizobium meliloti Gene Expression. J. Bacteriol. 186: 5460-5472 [Abstract] [Full Text]  
• Llamas, I., Keshavan, N., Gonzalez, J. E. (2004). Use of Sinorhizobium meliloti as an Indicator for Specific Detection of Long-Chain N-Acyl Homoserine Lactones. Appl. Environ. Microbiol. 70: 3715-3723 [Abstract] [Full Text]  
• Gonzalez, J. E., Marketon, M. M. (2003). Quorum Sensing in Nitrogen-Fixing Rhizobia. Microbiol. Mol. Biol. Rev. 67: 574-592 [Abstract] [Full Text]  
• Chen, H., Teplitski, M., Robinson, J. B., Rolfe, B. G., Bauer, W. D. (2003). Proteomic Analysis of Wild-Type Sinorhizobium meliloti Responses to N-Acyl Homoserine Lactone Quorum-Sensing Signals and the Transition to Stationary Phase. J. Bacteriol. 185: 5029-5036 [Abstract] [Full Text]  
• Luo, Z.-Q., Smyth, A. J., Gao, P., Qin, Y., Farrand, S. K. (2003). Mutational Analysis of TraR. CORRELATING FUNCTION WITH MOLECULAR STRUCTURE OF A QUORUM-SENSING TRANSCRIPTIONAL ACTIVATOR. J. Biol. Chem. 278: 13173-13182 [Abstract] [Full Text]  
• Tun-Garrido, C., Bustos, P., Gonzalez, V., Brom, S. (2003). Conjugative Transfer of p42a from Rhizobium etli CFN42, Which Is Required for Mobilization of the Symbiotic Plasmid, Is Regulated by Quorum Sensing. J. Bacteriol. 185: 1681-1692 [Abstract] [Full Text]  
• He, X., Chang, W., Pierce, D. L., Seib, L. O., Wagner, J., Fuqua, C. (2003). Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate. J. Bacteriol. 185: 809-822 [Abstract] [Full Text]  
• Loh, J., Carlson, R. W., York, W. S., Stacey, G. (2002). Bradyoxetin, a unique chemical signal involved in symbiotic gene regulation. Proc. Natl. Acad. Sci. USA 99: 14446-14451 [Abstract] [Full Text]  
• Marketon, M. M., Gronquist, M. R., Eberhard, A., Gonzalez, J. E. (2002). Characterization of the Sinorhizobium meliloti sinR/sinI Locus and the Production of Novel N-Acyl Homoserine Lactones. J. Bacteriol. 184: 5686-5695 [Abstract] [Full Text]  
• Pellock, B. J., Teplitski, M., Boinay, R. P., Bauer, W. D., Walker, G. C. (2002). A LuxR Homolog Controls Production of Symbiotically Active Extracellular Polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 184: 5067-5076 [Abstract] [Full Text]  
• Wilkinson, A., Danino, V., Wisniewski-Dye, F., Lithgow, J. K., Downie, J. A. (2002). N-Acyl-Homoserine Lactone Inhibition of Rhizobial Growth Is Mediated by Two Quorum-Sensing Genes That Regulate Plasmid Transfer. J. Bacteriol. 184: 4510-4519 [Abstract] [Full Text]  
• Gram, L., Grossart, H.-P., Schlingloff, A., Kiorboe, T. (2002). Possible Quorum Sensing in Marine Snow Bacteria: Production of Acylated Homoserine Lactones by Roseobacter Strains Isolated from Marine Snow. Appl. Environ. Microbiol. 68: 4111-4116 [Abstract] [Full Text]  
• Marketon, M. M., Gonzalez, J. E. (2002). Identification of Two Quorum-Sensing Systems in Sinorhizobium meliloti. J. Bacteriol. 184: 3466-3475 [Abstract] [Full Text]  
• Wisniewski-Dye, F., Jones, J., Chhabra, S. R., Downie, J. A. (2002). raiIR Genes Are Part of a Quorum-Sensing Network Controlled by cinI and cinR in Rhizobium leguminosarum. J. Bacteriol. 184: 1597-1606 [Abstract] [Full Text]  
• FRAY, R. G. (2002). Altering Plant-Microbe Interaction Through Artificially Manipulating Bacterial Quorum Sensing. ANN BOT (LOND) 89: 245-253 [Abstract] [Full Text]  
• Daniels, R., De Vos, D. E., 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 [Abstract] [Full Text]  
• Steidle, A., Sigl, K., Schuhegger, R., Ihring, A., Schmid, M., Gantner, S., Stoffels, M., Riedel, K., Givskov, M., Hartmann, A., Langebartels, C., Eberl, L. (2001). Visualization of N-Acylhomoserine Lactone-Mediated Cell-Cell Communication between Bacteria Colonizing the Tomato Rhizosphere. Appl. Environ. Microbiol. 67: 5761-5770 [Abstract] [Full Text]  
• Blosser-Middleton, R. S., Gray, K. M. (2001). Multiple N-Acyl Homoserine Lactone Signals of Rhizobium leguminosarum Are Synthesized in a Distinct Temporal Pattern. J. Bacteriol. 183: 6771-6777 [Abstract] [Full Text]  
• Dittmann, E., Erhard, M., Kaebernick, M., Scheler, C., Neilan, B. A., von Dohren, H., Borner, T. (2001). Altered expression of two light-dependent genes in a microcystin-lacking mutant of Microcystis aeruginosa PCC 7806. Microbiology 147: 3113-3119 [Abstract] [Full Text]  
• Weichart, D. H., Kell, D. B. (2001). Characterization of an autostimulatory substance produced by Escherichia coli. Microbiology 147: 1875-1885 [Abstract] [Full Text]  
• Bringhurst, R. M., Cardon, Z. G., Gage, D. J. (2001). Galactosides in the rhizosphere: Utilization by Sinorhizobium meliloti and development of a biosensor. Proc. Natl. Acad. Sci. USA 10.1073/pnas.071375898v1 [Abstract] [Full Text]  
• McDougald, D., Rice, S. A., Kjelleberg, S. (2001). SmcR-Dependent Regulation of Adaptive Phenotypes in Vibrio vulnificus. J. Bacteriol. 183: 758-762 [Abstract] [Full Text]  
• Laue, B. E., Jiang, Y., Chhabra, S. R., Jacob, S., Stewart, G. S. A. B., Hardman, A., Downie, J. A., 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 [Abstract] [Full Text]  
• de Kievit, T. R., Iglewski, B. H. (2000). Bacterial Quorum Sensing in Pathogenic Relationships. Infect. Immun. 68: 4839-4849 [Full Text]  
• 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 [Abstract] [Full Text]  
• Oresnik, I. J., Twelker, S., Hynes, M. F. (1999). Cloning and Characterization of a Rhizobium leguminosarum Gene Encoding a Bacteriocin with Similarities to RTX Toxins. Appl. Environ. Microbiol. 65: 2833-2840 [Abstract] [Full Text]  
• Rodelas, B., Lithgow, J. K., Wisniewski-Dye, F., Hardman, A., Wilkinson, A., Economou, A., Williams, P., Downie, J. A. (1999). Analysis of Quorum-Sensing-Dependent Control of Rhizosphere-Expressed (rhi) Genes in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 181: 3816-3823 [Abstract] [Full Text]  
• Pearson, J. P., Van Delden, C., Iglewski, B. H. (1999). Active Efflux and Diffusion Are Involved in Transport of Pseudomonas aeruginosa Cell-to-Cell Signals. J. Bacteriol. 181: 1203-1210 [Abstract] [Full Text]  
• Thorne, S. H., Williams, H. D. (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 [Abstract] [Full Text]  
• Zhu, J., Beaber, J. W., Moré, M. I., Fuqua, C., Eberhard, A., Winans, S. C. (1998). Analogs of the Autoinducer 3-Oxooctanoyl-Homoserine Lactone Strongly Inhibit Activity of the TraR Protein of Agrobacterium tumefaciens. J. Bacteriol. 180: 5398-5405 [Abstract] [Full Text]  
• von Bodman, S. B., Majerczak, D. R., Coplin, D. L. (1998). A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA 95: 7687-7692 [Abstract] [Full Text]  
• Storey, D. G., Ujack, E. E., Rabin, H. R., Mitchell, I. (1998). Pseudomonas aeruginosa lasR Transcription Correlates with the Transcription of lasA, lasB, and toxA in Chronic Lung Infections Associated with Cystic Fibrosis. Infect. Immun. 66: 2521-2528 [Abstract] [Full Text]  
• Rosemeyer, V., Michiels, J., Verreth, C., Vanderleyden, J. (1998). luxI- and luxR-Homologous Genes of Rhizobium etli CNPAF512 Contribute to Synthesis of Autoinducer Molecules and Nodulation of Phaseolus vulgaris. J. Bacteriol. 180: 815-821 [Abstract] [Full Text]  
• Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E. Jr., Rinehart, K. L., Farrand, S. K. (1997). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. USA 94: 6036-6041 [Abstract] [Full Text]  
• Bringhurst, R. M., Cardon, Z. G., Gage, D. J. (2001). Galactosides in the rhizosphere: Utilization by Sinorhizobium meliloti and development of a biosensor. Proc. Natl. Acad. Sci. USA 98: 4540-4545 [Abstract] [Full Text]