SpringerLink
Log in

Molecular Signals and Receptors: Communication Between Nitrogen-Fixing Bacteria and Their Plant Hosts

  • Chapter
  • First Online:
Biocommunication of Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 14))

Abstract

Our understanding of the extent of communication taking place between the plant and its underground microbiome (rhizosphere microbes) as well as with other soil organisms has grown exponentially in the last decade. Much of this information has been obtained from studies of nitrogen-fixing organisms, particularly members of the family Rhizobiaceae(Alphaproteobacteria) that establish nodules on legume roots in which atmospheric nitrogen is converted to plant-utilizable forms. Signals exchanged among organisms in the rhizosphere via quorum sensing (QS) and the responses to these signals have been identified, but it is unclear how they influence the downstream stages of nodulation and nitrogen fixation. An exchange of signal molecules ensures that a high level of specificity takes place to optimize the nitrogen-fixing interaction between host legume and symbiont. Chitin-related molecules appear to be the microbial currency for communication between the symbiotic partners in both mutualistic and pathogenic interactions. Exceptions to the paradigms based on the legume-Rhizobiuminteraction, including the discovery of Betaproteobacteria (now called beta-rhizobia) that nodulate and fix nitrogen with legumes and the lack of nodulation (nod) genes in certain alpha-rhizobia, particularly those that nodulate Aeschynomeneand Arachis, bring into question the universality of some of the previous models. Moreover, new frontiers have opened that examine the coordination of information exchange that is needed for the induction and maintenance of nitrogen fixation and for bacteroid differentiation. Nevertheless, nitrogen-fixing organisms are just one small part of a highly interactive rhizosphere community. The challenge of the next decade will be to understand in greater depth the community dynamics that occur in soil, one of our planet’s most precious yet limited resources, in the hopes of maintaining the key signal webs that are critical not only for the promotion of agriculture but also for the preservation of the environment overall.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 160.49
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 213.99
Price includes VAT (Germany)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 213.99
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Ahlgren NA, Harwood CS, Schaefer AL, Giraud E, Greenberg EP (2011) Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia. Proc Natl Acad Sci USA 17:7183–7188

    Article  Google Scholar 

  • Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé J-C, Dénarié J, Truchet G (1994) Rhizobium melilotilipochitooligosaccharide nodulation factors: Different structural requirements for bacterial entry to target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6:1357–1374

    PubMed  CAS  Google Scholar 

  • Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650

    Article  PubMed  CAS  Google Scholar 

  • Bahlawane C, McIntosh M, Krol E, Becker A (2008) Sinorhizobium melilotiregulator MucR couples exopolysaccharide synthesis and motility. Mol Plant–Microbe Interact 21:1498–1509

    Article  PubMed  CAS  Google Scholar 

  • Banwart S (2011) Save our soils. Nature 474:151–152

    Article  PubMed  CAS  Google Scholar 

  • Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F, Boursot M, Vallenet D, Chaintreuil C, Prin Y, Nouwem N, Giraud E (2010) Large-scale transposon mutagenesis of photosynthetic Bradyrhizobiumsp. strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica. Mol Plant–Microbe Interact 23:760–770

    Article  PubMed  CAS  Google Scholar 

  • Bonfante P, Requena N (2011) Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 14:1–7

    Article  CAS  Google Scholar 

  • Bontemps C, Elliott GN, Simon MF, dos Reis Junior FB, Gross E, Lawton RC, Neto NE, Loureiro MF, de Faria SM, Sprent JI, James EK, Young JPW (2010) Burkholderiaspecies are ancient symbionts of legumes. Mol Ecol 19:44–52

    Article  PubMed  CAS  Google Scholar 

  • Boone CM, Olsthoorn MMM, Dakora FD, Spaink HP, Thomas-Oates JE (1999) Structural characterization of lipo-oligosaccharides isolated from Bradyrhizobium aspalati, microsymbionts of commercially important South African legumes. Carbohydr Res 317:155–163

    Article  PubMed  CAS  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  PubMed  CAS  Google Scholar 

  • Brelles-Mariño G, Bedmar EJ (2001) Detection, purification and characterisation of quorum-sensing signal molecules in plant-associated bacteria. J Biotechnol 91:197–209

    Article  PubMed  Google Scholar 

  • Bucher M, Wegmüller S, Drissner D (2009) Chasing the structures of small molecules in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 12:500–507

    Article  PubMed  CAS  Google Scholar 

  • 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 191:283–289

    Article  PubMed  CAS  Google Scholar 

  • Chen W-M, James EK, Prescott AR, Kierans M, Sprent JI (2003a) Nodulation of Mimosaspp. by the β-proteobacterium Ralstonia taiwanensis. Mol Plant–Microbe Interact 16:1051–1061

    Article  PubMed  CAS  Google Scholar 

  • Chen W-M, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003b) Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  PubMed  CAS  Google Scholar 

  • Chen W-M, James EK, Coenye T, Chou J-H, Barrios E, de Faria SM, Elliott GN, Sheu S-Y, Sprent JI, Vandamme P (2006) Burkholderia mimosarumsp. nov., isolated from root nodules of Mimosaspp. from Taiwan and South America. Int J Syst Evol Microbiol 56:1847–1851

    Article  PubMed  CAS  Google Scholar 

  • Chen W-M, de Faria SM, James EK, Elliott GN, Lin K-Y, Chou J-H, Sheu S-Y, Cnockaert M, Sprent JI, Vandamme P (2007) Burkholderia nodosasp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronataand Mimosa scabrella. Int J Syst Evol Microbiol 57:1055–1059

    Article  PubMed  CAS  Google Scholar 

  • Chen W-M, de Faria SM, Chou J-H, James EK, Elliott GN, Sprent JI, Bontemps C, Young JPW, Vandamme P (2008) Burkholderia sabiaesp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179

    Article  PubMed  CAS  Google Scholar 

  • Cubo MT, Economou A, Murphy G, Johnston AW, Downie JA (1992) Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCRthat can influence nodulation by Rhizobium leguminosarumbiovar 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 cinquorum sensing locus of Rhizobium etliCNPAF512 affects growth and symbiotic nitrogen fixation. J Biol Chem 277:462–468

    Article  PubMed  CAS  Google Scholar 

  • Danino VE, Wilkinson A, Edwards A, Downie JA (2003) Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarumbv. viciaeis regulated by a quorum-sensing relay. Mol Microbiol 50:511–525

    Article  PubMed  CAS  Google Scholar 

  • Dart P (1977) Infection and development of leguminous nodules. In: Hardy RWF (ed) A treatise on biological nitrogen fixation. Wiley, New York, pp 367–472

    Google Scholar 

  • Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobia protein secretion systems. Nat Rev Microbiol 7:3312–3320

    Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631

    Article  PubMed  CAS  Google Scholar 

  • Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170

    Article  PubMed  CAS  Google Scholar 

  • Downie JA, González JE (2008) Cell-to-cell communication in rhizobia: Quorum sensing and plant signaling. In: Winans SC, Bassler BL (eds) Chemical communication among bacteria. ASM Press, Washington, DC, pp 213–232

    Google Scholar 

  • Egland KA, Greenberg EP (1999) Quorum sensing in Vibrio fischeri: elements of the luxIpromoter. Mol Microbiol 31:1197–1204

    Article  PubMed  CAS  Google Scholar 

  • Elasri M, Delorme S, Lemanceau P, Stewart G, Laue B, Glickmann E, Oger PM, Dessaux Y (2001) Acyl-homoserine lactone production is more common among plant-associated Pseudomonasspp. than among soilborne Pseudomonasspp. Appl Environ Microbiol 67:1198–1209

    Article  PubMed  CAS  Google Scholar 

  • Ercolin F, Reinhardt D (2011) Successful joint ventures of plants: Arbuscular mycorrhiza and beyond. Trends Plant Sci 16:356

    Article  PubMed  CAS  Google Scholar 

  • Foster RC, Rovira AD, Cock TW (1983) Ultrastructure of the root–soil interface. The American Phytopathological Society, St. Paul, pp 5–11

    Google Scholar 

  • Fujishige NA, Lum MR, De Hoff PL, Whitelegge JP, Faull KF, Hirsch AM (2008) Rhizobiumcommon nodgenes are required for biofilm formation. Mol Microbiol 67:504–515

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatulathat affect bacterial quorum sensing. Mol Plant–Microbe Interact 16:827–834

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Chen H, Eberhard A, Gronquist MR, Robinson JB, Rolfe BG, Bauer WD (2005) sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J Bacteriol 187:7931–7944

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Zhong Z, Sun K, Wang H, Zhu J (2006) The quorum-sensing system in a plant-bacterium Mesorhizobium huakuiiaffects growth rate and symbiotic nodulation. Plant Soil 286:53–60

    Article  CAS  Google Scholar 

  • Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E et al (2007) Legume symbioses: absence of nodgenes in photosynthetic bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • Givskov M, de Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD, Kjelleberg S (1996) Eukaryotic interference with homoserine lactone mediated prokaryotic signaling. J Bacteriol 178:6618–6622

    PubMed  CAS  Google Scholar 

  • Glenn SA, Gurich N, Feeney MA, González JE (2007) The ExpR/Sin quorum sensing system controls succinoglycan production in Sinorhizobium meliloti. J Bacteriol 189:7077–7088

    Article  PubMed  CAS  Google Scholar 

  • González-Sama A, Lucas MM, de Felipe MR, Pueyo JJ (2004) An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus). New Phytologist 163:371–380

    Article  Google Scholar 

  • Gurich N, González JE (2009) Role of quorum sensing in the Sinorhizobium meliloti-alfalfa symbiosis. J Bacteriol 191:4372–4382

    Article  PubMed  CAS  Google Scholar 

  • Hamel L-P, Beaudoin N (2010) Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant–microbe interactions. Planta 232:787–806

    Article  PubMed  CAS  Google Scholar 

  • He X, Chang W, Pierce DL, Seib LO, Wagner J, Fuqua C (2003) Quorum sensing in Rhizobiumsp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate. J Bacteriol 185:809–822

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM (1992) Tansley Review No. 40. Developmental biology of legume nodulation. New Phytologist 122:211–237

    Article  Google Scholar 

  • Hirsch AM (2004) Plant-microbe symbioses: a continuum from commensalism to parasitism. Symbiosis 37:345–363

    CAS  Google Scholar 

  • Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium-legume symbiosis. Fungal Genet Biol 23:205–212

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868

    Article  Google Scholar 

  • Hirsch AM, Lum MR, Fujishige NA (2009) Microbial encounters of a symbiotic kind—attaching to roots and other surfaces. In: Emons AMC, Ketelaar T (eds) Root hairs. Plant cell monographs, vol 12. Springer, Berlin/Heidelberg, pp 295–314

    Google Scholar 

  • Hoang HH, Becker A, González JE (2004) The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium melilotigene expression. J Bacteriol 186:5460–5472

    Article  PubMed  CAS  Google Scholar 

  • Hoang HH, Gurich N, González JE (2008) Regulation of motility by the ExpR/Sin quorum sensing system in Sinorhizobium meliloti.J Bacteriol 190:861–871

    Google Scholar 

  • Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P et al (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signal cascade. Plant Physiol 156:700–711

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Cook DM, Farrand SK (1995) A new regulatory element modulates homoserine lactone-mediated autoinduction of Ti plasmid conjugal transfer. J Bacteriol 177:449–458

    PubMed  CAS  Google Scholar 

  • Iizasa E, Mitsutomi M, Nagano Y (2010) Direct binding of a plant LysM receptor kinase, LysM RlK1/CERK1, to chitin in vitro. J Biol Chem 285:2996–3004

    Article  PubMed  CAS  Google Scholar 

  • Innes Roger William (1988). A molecular genetic analysis of host-range control in Rhizobium trifolii. Ph.D. dissertation, University of Colorado at Boulder, United States, Colorado. Retrieved June 3, 2011, from Dissertations & Theses: A&I. (Publication No. AAT 8819666)

    Google Scholar 

  • Jitacksorn S, Sadowsky MJ (2008) Nodulation gene regulation and quorum sensing control density dependent suppression and restriction of nodulation in the Bradyrhizobium japonicum-soybean symbiosis. Appl Environ Microbiol 74:3749–3756

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl J (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicagomodel. Nat Rev Microbiol 5:619–633

    Article  PubMed  CAS  Google Scholar 

  • Lanou A, Burlat V, Schurr U, Röse USR (2010) Induced root-secreted phenolic compounds as a belowground plant defense. Plant Signal Behav 5:1037–1038

    Article  Google Scholar 

  • LaRue TA, Weeden NF (1994). The symbiosis genes of the host. In: Kiss GB, Endre G (eds) Proceedings of the 1st European nitrogen fixation conference, Officia Press, Szeged, 147–151

    Google Scholar 

  • Lazdunski AM, Ventre I, Sturgis JN (2004) Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2:581–592

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Loh J, Stacey G (2003) Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Appl Environ Microbiol 69:10–17

    Article  PubMed  CAS  Google Scholar 

  • Loh J, Carlson RW, York WS, Stacey G (2002) Bradyoxetin, a unique chemical signal involved in symbiotic gene regulation. Proc Natl Acad Sci USA 99:14446–14451

    Article  PubMed  CAS  Google Scholar 

  • Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckman AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:10

    Article  PubMed  CAS  Google Scholar 

  • Maillet F, Poinsot V, André L, Puech-Pagè V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhizae. Nature 469:58–64

    Article  PubMed  CAS  Google Scholar 

  • Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchrainhibit 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, Rasmussen TB, Hentzer M, Andersen JB, Steinberg P, Kjelleberg S, Givskov M (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148:119–1127

    Google Scholar 

  • Marketon MM, González JE (2002) Identification of two quorum-sensing systems in Sinorhizobium meliloti. J Bacteriol 185:3466–3475

    Article  CAS  Google Scholar 

  • Marketon MM, Gronquist MR, Eberhard A, González JE (2002) Characterization of the Sinorhizobium meliloti sinR/sinIlocus and the production of novel N-acyl homoserine lactones. J Bacteriol 184:5686–5695

    Article  PubMed  CAS  Google Scholar 

  • Marketon MM, Glenn SA, Eberhard A, González JE (2003) Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 185:325–331

    Article  PubMed  CAS  Google Scholar 

  • Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe RB, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449

    Article  PubMed  CAS  Google Scholar 

  • McIntosh M, Krol E, Becker A (2008) Competitive and cooperative effects in quorum sensing regulated galactoglucan biosynthesis in Sinorhizobium meliloti. J Bacteriol 190:5308–5317

    Article  PubMed  CAS  Google Scholar 

  • Merker R, Smit J (1988) Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl Environ Microbiol 54:2078–2085

    PubMed  CAS  Google Scholar 

  • Moulin L, Mundive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by the beta-subclass of Proteobacteria. Nature 411:948–950

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Chen WM, Béna G, Dreyfus B, Boivin-Masson C (2002). Rhizobia: the family is expanding. In: Finan T, O’Brian M, Layzell D, Vessey K, Newton, W (eds) Nitrogen fixation: global perspectives, CAB International, Wallingford, UK, New York, NY, pp 61–65

    Google Scholar 

  • Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N et al (2007) Evaluation of Frankiastrains isolated from provenances of two Alnusspecies. Genome Res 17:7–15

    Article  PubMed  Google Scholar 

  • Ong CJ, Wong MLY, Smit J (1990) Attachment of the adhesive holdfast organelle to the cellular stalk of Caulobacter crescentus. J Bacteriol 172:1448–1456

    PubMed  CAS  Google Scholar 

  • Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331:909–912

    Article  PubMed  CAS  Google Scholar 

  • Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríquez L, López-Bucio L (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712

    Article  PubMed  Google Scholar 

  • 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 184:5067–5076

    Article  PubMed  CAS  Google Scholar 

  • Pereira CS, McAuley JR, Taga ME, Xavier KB, Miller ST (2008) Sinorhizobium meliloti, a bacterium lacking autoinducer-2 (AI-2) synthase responds to AI-2 supplied by other bacteria. Mol Microbiol 70:1223–1235

    Article  PubMed  CAS  Google Scholar 

  • Piper KR, von Bodman SB, Farrand SK (2004) Conjugation factor of Agrobacterium tumefaciensregulates Ti plasmid transfer by autoinduction. Nature 362:448–450

    Article  Google Scholar 

  • Pongsilp N, Triplett EW, Sadowsky MJ (2005) Detection of homoserine lactone-like quorum sensing molecules in Bradyrhizobiumstrains. Curr Microbiol 51:250–254

    Article  PubMed  CAS  Google Scholar 

  • Prell J, Poole P (2006) Metabolic changes of rhizobia in legume nodules. Trends Microbiol 14:161–168

    Article  PubMed  CAS  Google Scholar 

  • Prell J, Bourdès A, Kumar S, Lodwig E, Hosie A, Kinghorn S, White J, Poole P (2010) Role of symbiotic auxotrophy in the Rhizobium-legume symbiosis. PLoS One 5:e13933

    Article  PubMed  CAS  Google Scholar 

  • Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, Ronson CW (2006) Excision and transfer of the Mesorhizobium lotiR7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62:723–734

    Article  PubMed  CAS  Google Scholar 

  • Ramsay JP, Sullivan JT, Jambari N, Ortori CA, Heeb S, Williams P, Barrett DA, Lamont IL, Ronson CW (2009) A LuxRI-family regulatory system controls excisions and transfer of the Mesorhizobium lotiR7A symbiosis island by activating expression of two conserved hypothetical genes. Mol Microbiol 73:1141–1155

    Article  PubMed  CAS  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million year old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    Article  PubMed  CAS  Google Scholar 

  • Rodelas B, Lithgow JK, Wisniewski-Dye 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 leguminosarumbv. viciae. J Bacteriol 181:3816–3823

    PubMed  CAS  Google Scholar 

  • Rosemeyer V, Michiels J, Verreth C, Vanderleyden J (1998) luxI- and luxR-homologous genes of Rhizobium etliCNPAF512 contribute to the synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J Bacteriol 180:815–821

    PubMed  CAS  Google Scholar 

  • Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, Mazmanian SK (2011) The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974–977

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Contreras M, Bauer WD, Gao M, Robinson JB, Downie JA (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Phil Trans R Soc B 362:1149–1163

    Article  PubMed  CAS  Google Scholar 

  • Scheu S (2001) Plants and generalist predators as links between the below-ground and above-ground system. Basic Appl Ecol 2:3–13

    Article  Google Scholar 

  • Sinharoy S, DasGupta M (2009) RNA interference highlights the role of CCaMK in dissemination of endosymbionts in the Aeschynomeneae legume Arachis. Mol Plant–Microbe Interact 22:1466–1475

    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 

  • Sprent JI (2007) Tansley review. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174:11–25

    Article  PubMed  CAS  Google Scholar 

  • Suarez-Moreno ZR, Caballero-Mellado J, Venturi V (2008) The new group of non-pathogenic plant-associated Burkholderiaspp. shares a conserved quorum sensing system which is tightly regulated by the RsaL repressor. Microbiology 154:2048–2059

    Article  PubMed  CAS  Google Scholar 

  • Suarez-Moreno ZR, Devescovi G, Myers M, Hallack L, Mendonca-Previato L, Caballero-Mellado J, Venturi V (2010) Commonalities and differences in regulation of N-acyl homoserine lactone quorum sensing in the beneficial plant associated Burkholderiaspecies cluster. Appl Environ Microbiol 76:4302–4317

    Article  PubMed  CAS  Google Scholar 

  • Taylor TN, Remy W, Hass H (1992) Fungi from the lower Devonian Rhynie chert: Chytridiomycetes. Am J Bot 79:1233–1241

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • 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 melilotistrains in defined medium. Arch Microbiol 180:494–497

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Merighi M, Gao M, Robinson J (2011) Interaction of cell-to-cell signals in soil bacterial communities. In: Witzany G (ed) Biocommunication in soil microorganisms, soil biology, vol 23. Springer, Berlin/Heidelberg, pp 369–401

    Chapter  Google Scholar 

  • Tun-Garrido C, Bustos P, Gonzalez V, Brom S (2003) Conjugative transfer of p42a from Rhizobium etliCFN42, which is required for mobilization of the symbiotic plasmid, is regulated by quorum sensing. J Bacteriol 185:1681–1692

    Article  PubMed  CAS  Google Scholar 

  • Uheda E, Daimon H, Yoshizako F (2001) Colonization and invasion of peanut (Arachis hypogeaL.) roots by gusA-marked Bradyrhizobiumsp. Can J Bot 79:733–739

    Google Scholar 

  • Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H et al (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126

    Article  PubMed  CAS  Google Scholar 

  • Vandamme P, Goris J, Chen WM, de Vos P, Willems A (2002) Burkholderia tuberumsp. nov. and Burkholderia phymatumsp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 5:507–512

    Article  Google Scholar 

  • von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482

    Article  CAS  Google Scholar 

  • Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signalling and fungal resistance in Arabidopsis. Plant Cell 20:471–481

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Yeun LH, Xue J-Y, Liu Y, Ané JM, Qiu Y-L (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytologist 186:514–525

    Article  PubMed  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: Cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    Article  PubMed  CAS  Google Scholar 

  • 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 184:4510–4519

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski-Dye F, Downie JA (2002) Quorum sensing in Rhizobium. Antonie Van Leeuwenhoek 81:397–407

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski-Dye F, Jones J, Chhabra SR, Downie JA (2002) raiRgenes are part of the quorum sensing network controlled by cinIand cinRin Rhizobium leguminosarum. J Bacteriol 184:1597–1606

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Sun K, Zhou L, Yang R, Zhong Z, Zhu J (2009) Functional analysis of three AHL autoinducer synthase genes in Mesorhizobium lotireveals the important role of quorum sensing in symbiotic nodulation. Can J Microbiol 55:210–214

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Zhong Z, Lai X, Chen W-X, Li S, Zhu J (2006) A LuxR/LuxI-type quorum sensing system in a plant bacterium Mesorhizobium tianshanensecontrols symbiotic nodulation. J Bacteriol 188:1943–1949

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments.

Research in the Hirsch laboratory is funded by grants from the National Science Foundation and from the support of the Shanbrom Family Foundation. We are grateful to Philip Poole and Roger Innes for answering our e-mails about nitrogen fixation. We thank Stefan J. Kirchanski thanked for his helpful comments on a draft of the manuscript. We also thank Michelle Lum for Fig. 1c and Benny Gee for Fig. 2.

We dedicate this chapter to the late W. Dietz Bauer, one of the pioneers in the field of plant-microbe communication.

Author information

Authors and Affiliations

  1. Department of Molecular, Cell and Developmental Biology, University of California-Los Angeles, Los Angeles, CA, USA

    Ann M. Hirsch & Nancy A. Fujishige

  2. Molecular Biology Institute, University of California-Los Angeles, Los Angeles, CA, USA

    Ann M. Hirsch

Authors
  1. Ann M. Hirsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nancy A. Fujishige
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ann M. Hirsch .

Editor information

Editors and Affiliations

  1. Telos - Philosophische Praxis, Vogelsangstr. 18c, Bürmoos, 5111, Austria

    Günther Witzany

  2. Inst. Zelluläre und Molekulare, Botanik (IZMB), Universität Bonn, Kirschallee 1, Bonn, 53115, Germany

    František Baluška

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Hirsch, A.M., Fujishige, N.A. (2012). Molecular Signals and Receptors: Communication Between Nitrogen-Fixing Bacteria and Their Plant Hosts. In: Witzany, G., Baluška, F. (eds) Biocommunication of Plants. Signaling and Communication in Plants, vol 14. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23524-5_14

Download citation

Publish with us

Policies and ethics

Search

Navigation