Rhizobial Extracellular Signaling Molecules and Their Functions in Symbiotic Interactions with Legumes



Rhizobia (symbiotic nitrogen-fixing soil bacteria) and their legume host plants communicate with each other via signaling molecules such as flavonoids and Nod factors. In addition, rhizobia use separate “quorum sensing” (QS) systems to communicate among themselves. QS systems in rhizobia have been implicated as regulators of plasmid transfer, nodulation efficiency, nitrogen fixation, polysaccharide production and degradation, swarming motility, stress adaptation, and biofilm formation. Most rhizobial species studied to date appear to utilize one or more acyl homoserine lactone (AHL)-based QS systems. This chapter summarizes our current knowledge of QS signaling molecules and their functions in rhizobia, particularly the widespread genera Sinorhizobium, Mesorhizobium, Rhizobium, and Bradyrhizobium.


Quorum Sense Quorum Sense System Plasmid Transfer Acyl Homoserine Lactone Quorum Sense Signal 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This review and studies by the author’s group described herein were supported by grants from the Secretaría de Ciencia y Técnica (UNRC), Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), and Consejo Nacional de Investigaciones Científicas y Técnicas of the República Argentina (CONICET). WG is a Career Member of CONICET. Thanks to Dr. S. Anderson for English editing of the manuscript.


  1. Ahlgren NA, Harwood CS, Schaefer AL, Giraud E, Greenberg P (2011) Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia. Proc Natl Acad Sci U S A 108:7183–7188PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ampomah OY, Huss-Danell K (2011) Nodulation of Thermopsis lupinoides by a Mesorhizobium huakuii strain with a unique nodA gene in Kamchatka, Russia. Appl Environ Microbiol 77:5513–5516PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bogino P, Banchio E, Rinaudi L, Cerioni G, Bonfiglio C, Giordano W (2006) Peanut (Arachis hypogaea) response to inoculation with Bradyrhizobium sp. in soils of Argentina. Ann Appl Biol 148:207–212CrossRefGoogle Scholar
  4. Bogino P, Oliva MM, Sorroche FG, Giordano W (2013) The role of bacterial biofilms and surface components in plant-bacterial associations. Int J Mol Sci 14:15838–15859PubMedCrossRefPubMedCentralGoogle Scholar
  5. Burmølle M, Ren D, Bjarnsholt T, Sørensen S (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91PubMedGoogle Scholar
  6. Cao H, Yang M, Zheng H, Zhang J, Zhong Z, Zhu J (2009) Complex quorum-sensing regulatory systems regulate bacterial growth and symbiotic nodulation in Mesorhizobium tianshanense. Arch Microbiol 191:283–289PubMedCrossRefGoogle Scholar
  7. Cha CE, Gao O, Chen YC, Shaw PD, Farrand SK (1998) Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol Plant Microbe Interact 11:1119–1129PubMedCrossRefGoogle Scholar
  8. Charoenpanich P, Meyer S, Becker A, McIntosh M (2013) Temporal expression program of quorum sensing-based transcription regulation in Sinorhizobium meliloti. J Bacteriol 195:3224–3236PubMedCrossRefPubMedCentralGoogle Scholar
  9. Cubo MT, Economou A, Murphy G, Johnston AW, Downie JA (1992) Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J Bacteriol 174:4026–4035PubMedPubMedCentralGoogle Scholar
  10. Daniels R, De Vos DE, Desair J et al (2002) The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J Biol Chem 277:462–468PubMedCrossRefGoogle Scholar
  11. Daniels R, Vanderleyden J, Michiels J (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28:261–289PubMedCrossRefGoogle Scholar
  12. Danino VE, Wilkinson A, Edwards A, Downie JA (2003) Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol Microbiol 50:511–525PubMedCrossRefGoogle Scholar
  13. Downie JA, Walker SA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2:483–489PubMedCrossRefGoogle Scholar
  14. Edwards A, Frederix M, Wisniewski-Dye F, Jones J, Zorreguieta A, Downie JA (2009) The cin and rai quorum-sensing regulatory systems in Rhizobium leguminosarum are coordinated by ExpR and CinS, a small regulatory protein coexpressed with CinI. J Bacteriol 191:3059–3067PubMedCrossRefPubMedCentralGoogle Scholar
  15. Frederix M, Edwards A, McAnulla C, Downie JA (2011) Co-ordination of quorum-sensing regulation in Rhizobium leguminosarum by induction of an anti-repressor. Mol Microbiol 81:994–1007PubMedCrossRefGoogle Scholar
  16. Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834PubMedCrossRefGoogle Scholar
  17. Gao M, Chen H, Eberhard A et al (2005) sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J Bacteriol 187:7931–7944PubMedCrossRefPubMedCentralGoogle Scholar
  18. Gao YJ, Zhong ZT, Sun KJ, Wang H, Zhu J (2006) The quorum sensing system in a plant bacterium Mesorhizobium huakuii affects growth rate and symbiotic nodulation. Plant Soil 286:53–60CrossRefGoogle Scholar
  19. Gao M, Coggin A, Yagnik K, Teplitski M (2012) Role of specific quorum-sensing signals in the regulation of exopolysaccharide II production within Sinorhizobium meliloti spreading colonies. PLoS One 7(8):e42611PubMedCrossRefPubMedCentralGoogle Scholar
  20. He X, Chang W, Pierce DL, Seib LO, Wagner J, Fuqua C (2003) Quorum sensing in Rhizobium sp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate. J Bacteriol 185:809–822PubMedCrossRefPubMedCentralGoogle Scholar
  21. Hoang HH, Gurich N, Gonzalez JE (2008) Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti. J Bacteriol 190:861–871PubMedCrossRefPubMedCentralGoogle Scholar
  22. Kaneko T, Nakamura Y, Sato S et al (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:381–406PubMedCrossRefGoogle Scholar
  23. Lang J, Faure D (2014) Functions and regulation of quorum-sensing in Agrobacterium tumefaciens. Front Plant Sci 5:14. doi: 10.3389/fpls.2014.00014 PubMedCrossRefPubMedCentralGoogle Scholar
  24. Li Z, Nair SK (2012) Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals? Protein Sci 21:1403–1417PubMedCrossRefPubMedCentralGoogle Scholar
  25. Lindemann A, Pessi G, Schaefer AL et al (2011) Isovaleryl-homoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum. Proc Natl Acad Sci U S A 108:16765–16770PubMedCrossRefPubMedCentralGoogle Scholar
  26. Lithgow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dye F, Williams P, Downie JA (2000) The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol Microbiol 37:81–97PubMedCrossRefGoogle Scholar
  27. Loh J, Stacey G (2001) Feedback regulation of the Bradyrhizobium japonicum nodulation genes. Mol Microbiol 41:1357–1364PubMedCrossRefGoogle Scholar
  28. Loh J, Carlson RW, York WS, Stacey G (2002) Bradyoxetin, a unique chemical signal involved in symbiotic gene regulation. Proc Natl Acad Sci U S A 99:14446–14451PubMedCrossRefPubMedCentralGoogle Scholar
  29. Marketon MM, González JE (2002) Identification of two quorum-sensing systems in Sinorhizobium meliloti. J Bacteriol 148:3466–3475CrossRefGoogle Scholar
  30. Marketon MM, Gronquist MR, Eberhard A, Gonzalez JE (2002) Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J Bacteriol 184:5686–5695PubMedCrossRefPubMedCentralGoogle Scholar
  31. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci U S A 100:1444–1449PubMedCrossRefPubMedCentralGoogle Scholar
  32. McIntosh M, Meyer S, Becker A (2009) Novel Sinorhizobium meliloti quorum sensing positive and negative regulatory feedback mechanisms respond to phosphate availability. Mol Microbiol 74:1238–1256PubMedCrossRefGoogle Scholar
  33. Nievas F, Bogino P, Sorroche F, Giordano W (2012) Detection, characterization, and biological effect of quorum-sensing signaling molecules in peanut-nodulating bradyrhizobia. Sensors-Basel 12:2851–2873PubMedCrossRefPubMedCentralGoogle Scholar
  34. Pellock BJ, Teplitski M, Boinay RP, Bauer WD, Walker GC (2002) A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J Bacteriol 184:5067–5076PubMedCrossRefPubMedCentralGoogle Scholar
  35. Pongsilp N, Triplett EW, Sadowsky MJ (2005) Detection of homoserine lactone like quorum sensing molecules in Bradyrhizobium strains. Curr Microbiol 51:250–254PubMedCrossRefGoogle Scholar
  36. Ramsay JP, Sullivan JT, Jambari N et al (2009) A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Mol Microbiol 73:1141–1155PubMedCrossRefGoogle Scholar
  37. Ramsay JP, Major AS, Komarovsky VM et al (2013) A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator. Mol Microbiol 87:1–13PubMedCrossRefGoogle Scholar
  38. Rinaudi L, Giordano W (2010) An integrated view of biofilm formation in Rhizobia. FEMS Microbiol Lett 304:1–11PubMedCrossRefGoogle Scholar
  39. Rodelas B, Lithgow JK, Wisniewski-Dye F et al (1999) Analysis of quorum-sensing dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. J Bacteriol 181:3816–3823PubMedPubMedCentralGoogle Scholar
  40. 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 180:815–821PubMedPubMedCentralGoogle Scholar
  41. Russo DM, Williams A, Edwards A et al (2006) Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 188:4474–4486PubMedCrossRefPubMedCentralGoogle Scholar
  42. Ryan RP, Dow JM (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154:1845–1858PubMedCrossRefGoogle Scholar
  43. Sanchez-Contreras M, Wolfgang BD, Mengsheng G, Robinson JB, Downie A (2007) Quorum sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc B 362:1149–1163CrossRefGoogle Scholar
  44. Schmeisser C, Liesegang H, Krysciak D et al (2009) Rhizobium sp. Strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75:4035–4045PubMedCrossRefPubMedCentralGoogle Scholar
  45. Schripsema J, de Rudder KE, van Vliet TB et al (1996) Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-L-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J Bacteriol 178:366–371PubMedPubMedCentralGoogle Scholar
  46. Sorroche F, Rinaudi L, Zorreguieta A, Giordano W (2010) EPS II-dependent autoaggregation of Sinorhizobium meliloti planktonic cells. Curr Microbiol 61:465–470PubMedCrossRefGoogle Scholar
  47. Teplitski M, Eberhard A, Gronquist MR, Gao M, Robinson JB, Bauer WD (2003) Chemical identification of N-acyl homoserine lactone quorum-sensing signals produced by Sinorhizobium meliloti strains in defined medium. Arch Microbiol 180:494–497PubMedCrossRefGoogle Scholar
  48. 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 181:981–990PubMedPubMedCentralGoogle Scholar
  49. Wang H, Zhong Z, Cai T, Li S, Zhu J (2004) Heterologous overexpression of quorum-sensing regulators to study cell-density-dependent phenotypes in a symbiotic plant bacterium Mesorhizobium huakuii. Arch Microbiol 182:520–525PubMedCrossRefGoogle Scholar
  50. Westenberg DJ (2002) Evidence of AHL autoinducer production by the soybean symbiont Bradyrhizobium japonicum. In: Finan et al (eds) Nitrogen fixation: global perspectives. CABI Publishing/Oxford University Press, CaryGoogle Scholar
  51. Wilkinson A, Danino V, Wisniewski-Dye 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 184:4510–4519PubMedCrossRefPubMedCentralGoogle Scholar
  52. Wisniewski-Dye F, Downie JA (2002) Quorum-sensing in Rhizobium. Antonie Van Leeuwenhoek 81:397–407PubMedCrossRefGoogle Scholar
  53. Yang M, Sun K, Zhou L, Yang R, Zhong Z, Zhu J (2009) Functional analysis of three AHL autoinducer synthase genes in Mesorhizobium loti reveals the important role of quorum sensing in symbiotic nodulation. Can J Microbiol 55:210–214PubMedCrossRefGoogle Scholar
  54. Zarkani AA, Stein E, Röhrich CR, Schikora M, Evguenieva-Hackenberg E, Degenkolb T, Vilcinskas A, Klug G, Kogel KH, Schikora A (2013) Homoserine lactones influence the reaction of plants to rhizobia. Int J Mol Sci 14:17122–17171PubMedCrossRefPubMedCentralGoogle Scholar
  55. Zheng Z, Fuqua C, Chen L (2012) The quorum sensing transcriptional regulator TraR has separate binding sites for DNA and the anti-activator. Biochem Biophys Res Commun 418:396–401PubMedCrossRefGoogle Scholar
  56. Zhu J, Chai Y, Zhong Z, Li S, Winans SC (2003) Agrobacterium bioassay strain for ultrasensitive detection of N-acylhomoserine lactone-type quorum sensing molecules: detection of autoinducers in Mesorhizobium huakuii. Appl Environ Microbiol 69:6949–6953PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer India 2015

Authors and Affiliations

  1. 1.Departamento de Biología MolecularUniversidad Nacional de Río CuartoRío CuartoArgentina

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