Skip to main content

Key Molecules Involved in Beneficial Infection Process in Rhizobia–Legume Symbiosis

  • Chapter
Microbes for Legume Improvement

Abstract

The symbiotic relationships between nitrogen-fixing rhizobia and their legume hosts are the result of an intricate signaling network between the host and symbiont. The success of the symbiotic process depends on the competitiveness, specificity, infectivity, and effectiveness of rhizobia and follows a series of events, which are the result of the expression of different molecules from the bacteria, the host plant, or both partners. In this chapter, we review a serial of key molecules involved in the establishment of an efficient rhizobia–legume symbiosis and their role in the different steps of this process.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albrecht SL, Maier RJ, Hanus FJ, Russell SA, Emerich DW, Evans HJ (1979) Hydrogenase in Rhizobium japonicum increases nitrogen fixation by nodulated soybeans. Science 203:1255–1257

    Article  PubMed  CAS  Google Scholar 

  • Andersen OM, Markham KR (2006) Flavonoids: Chemistry. CRC Press, Boca Raton, Biochemistry and Applications

    Google Scholar 

  • Andersson CR, Jensen EO, Llewellyn DJ, Dennis ES, Peacock WJ (1996) A new hemoglobin gene from soybean: a role for hemoglobin in all plants. Proc Natl Acad Sci USA 93:5682–5687

    Article  CAS  Google Scholar 

  • Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 Required for Bacterial and Fungal Symbioses in Legumes. Science 303:1364–1367

    Article  PubMed  CAS  Google Scholar 

  • Appleby CA (1992) The origin and functions of haemoglobin in plants. Sci Prog 76:365–398

    CAS  Google Scholar 

  • Appleby CA, Tjepkema JD, Trinick MJ (1980) Hemoglobin in a nonleguminous plant Parasponia: possible genetic origin and function in nitrogen fixation. Science 220:951–953

    Article  Google Scholar 

  • Appleby CA, Bogusz D, Dennis ES, Peacock WJ (1998) A role for haemoglobin in all plant roots? Plant Cell Environ 11:359–367

    Article  Google Scholar 

  • Arredondo-Peter R, Hargrove MS, Sarath G, Moran JF, Lohrman J, Olson JS, Klucas RV (1997) Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiol 115:1259–1266

    Article  PubMed  CAS  Google Scholar 

  • Asad S, Fang Y, Wycoff KL, Hirsch AM (1994) Isolation and characterization of cDNA and genomic clones of MsENOD40: transcripts are detected in meristematic cells of alfalfa. Protoplasma 183:10–23

    Article  CAS  Google Scholar 

  • Baginsky C, Brito B, Imperial J, Palacios JM, Ruiz-Argüeso T (2002) Diversity and evolution of hydrogenase systems in rhizobia. Appl Environ Microbiol 68:4915–4924

    Article  PubMed  CAS  Google Scholar 

  • Baginsky C, Palacios JM, Imperial J, Ruiz-Argüeso T, Brito B (2004) Molecular and functional characterization of the Azorhizobium caulinodans ORS571 hydrogenase gene cluster. FEMS Microbiol Lett 237:399–405

    PubMed  CAS  Google Scholar 

  • Baginsky C, Brito B, Imperial J, Ruiz-Argüeso T, Palacios JM (2005) Symbiotic hydrogenase activity in Bradyrhizobium sp. (vigna) increases nitrogen content in Vigna unguiculata plants. Appl Environ Microbiol 71:7536–7538

    Article  PubMed  CAS  Google Scholar 

  • Bahyrycz A, Konopinska D (2007) Plant signalling peptides: some recent developments. J Pept Sci 13:787–797

    Article  PubMed  CAS  Google Scholar 

  • Barnett MJ, Fisher RF (2006) Global gene expression in the rhizobial–legume symbiosis. Symbiosis 42:1–24

    CAS  Google Scholar 

  • Becker A, Fraysse N, Sharypova L (2005) Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol Plant Microbe Interact 18:899–905

    Article  PubMed  CAS  Google Scholar 

  • Begum AA, Leibovitch S, Migner P, Zhang F (2001) Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. J Exp Bot 52:1537–1543

    Article  PubMed  CAS  Google Scholar 

  • Bladergroen MR, Spaink HP (1998) Genes and signal molecules involved in the rhizobia-leguminoseae symbiosis. Curr Opin Plant Biol 1:353–359

    Article  PubMed  CAS  Google Scholar 

  • Blosser-Middleton RS, Gray KM (2001) Multiple N-acyl homoserine lactone signals of Rhizobium leguminosarum are synthesized in a distinct temporal pattern. J Bacteriol 183:6771–6777

    Article  PubMed  CAS  Google Scholar 

  • Bohlool BB, Schmidt EL (1974) Lectins: A possible basis for specificity in the Rhizobium-legume symbiosis. Science 185:269–271

    Article  PubMed  CAS  Google Scholar 

  • Braeken K, Daniels R, Vos K, Fauvart M, Bachaspatimayum D, Vanderleyden J, Michiels J (2008) Genetic determinants of swarming in Rhizobium etli. Microb Ecol 55:54–64

    Article  PubMed  Google Scholar 

  • Breedveld MW, Miller KJ (1994) Cyclic b-glucans of members of the family. Rhizobiaceae Microbiol Rev 58:145–161

    CAS  Google Scholar 

  • Breedveld MW, Miller KJ (1998) Cell surface b-glucans. In: Spaink HP, Kondorosi A, Hooykaas JJ (eds) The Rhizobiaceae. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 81–96

    Chapter  Google Scholar 

  • Brito B, Palacios JM, Imperial J, Ruiz-Argüeso T (2002) Engineering the Rhizobium leguminosarum bv viciae hydrogenase system for free living microaerobic expression and increased symbiotic hydrogenase activity. Appl Environ Microbiol 68:2461–2467

    Article  PubMed  CAS  Google Scholar 

  • Brito B, Toffanin A, Prieto RI, Imperial J, Ruiz-Argüeso T, Palacios JM (2008) Host-dependent expression of Rhizobium leguminosarum bv. viciae hydrogenase is controlled at transcriptional and post-transcriptional levels in legume nodules. Mol Plant Microbe Interact 21:597–604

    Article  PubMed  CAS  Google Scholar 

  • Broughton WJ, Perret X (1999) Genealogy of legume-Rhizobium symbioses. Curr Opin Plant Biol 2:305–11

    Article  PubMed  CAS  Google Scholar 

  • Callaham D, Torrey J (1981) The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can J Bot 59:1647–1664

    Article  Google Scholar 

  • Campalans A, Kondorosi A, Crespi M (2004) Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 16:1047–1059

    Article  PubMed  CAS  Google Scholar 

  • Cantero L, Palacios JM, Ruiz-Argüeso T, Imperial J (2006) Proteomic analysis of quorum sensing in Rhizobium leguminosarum bv. viciae UPM791. Proteomics 6(Suppl 1):S97–S106

    Article  PubMed  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 

  • Carrion M, Bhat UR, Reuhs B, Carlson RW (1990) Isolation and characterization of the lipopolysaccharides from Bradyrhizobium japonicum. J Bacteriol 172:1725–1731

    PubMed  CAS  Google Scholar 

  • Charon C, Johansson C, Kondorosi E, Kondorosi A, Crespi M (1997) enod40 induces dedifferentiation and division of root cortical cells in legumes. Proc Natl Acad Sci USA 94:8901–8906

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Batley M, Redmond J, Rolfe BG (1985) Alteration of effective nodulation properties of a fast-growing broad host range Rhizobium due to changes in exopolysaccharide synthesis. J Plant Physiol 120:331–349

    Article  CAS  Google Scholar 

  • Cheng Q (2008) Perspectives in biological nitrogen fixation research. J Integr Plant Biol 50:786–798

    Article  PubMed  CAS  Google Scholar 

  • Cheon CI, Hong Z, Verma DP (1994) Nodulin-24 follows a novel pathway for integration into the peribacteroid membrane in soybean root nodules. J Biol Chem 269:6598–6602

    PubMed  CAS  Google Scholar 

  • Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365

    Article  PubMed  CAS  Google Scholar 

  • Corich V, Goormachtig S, Lievens S, Van Montagu M (1998) Holsters M. Patterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata. Plant Mol Biol 37:67–76

    Article  PubMed  CAS  Google Scholar 

  • Crespi MD, Jurkevitch E, Poiret M, d'Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A (1994) enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J 13:5099–5112

    PubMed  CAS  Google Scholar 

  • Crockard A, Bjourson J, Dazzo B, Cooper JE (2002) A white clover nodulin gene, dd23b, encoding a cysteine cluster protein, is expressed in roots during the very early stages of interaction with Rhizobium leguminosarum biovar trifolii and after treatment with chitolipooligosaccharide Nod factors. J Plant Res 115:439–447

    Article  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 

  • Daniels R, Reynaert S, Hoekstra H, Verreth C, Janssens J, Braeken K, Fauvart M, Beullens S, Heusdens C, Lambrichts I, De Vos DE, Vanderleyden J, Vermant J, Michiels J (2006) Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli. Proc Natl Acad Sci USA 103:14965–14970

    Article  PubMed  CAS  Google Scholar 

  • 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 50:511–525

    Article  PubMed  CAS  Google Scholar 

  • Das TK, Lee HC, Duff SM, Hill RD, Peisach J, Rousseau DL, Wittenberg BA, Wittenberg JB (1999) The heme environment in barley hemoglobin. J Biol Chem 274:4207–4212

    Article  PubMed  CAS  Google Scholar 

  • Dazzo F, Truchet G, Sherwood J, Hrabak E, Abe M, Pankratz HS (1984) Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Applied and Environmental Microbiology 48:1140–1150

    PubMed  CAS  Google Scholar 

  • Dazzo FB, Truchet GL, Hollingsworth RI, Hrabak EM, Pankratz HS, Philip-Hollingsworth S, Salzwedel JL, Chapman K, Appenzeller L, Squartini A, Gerhold D, Orgambide G (1991) Rhizobium LPS modulates infection thread development in white clover root hairs. J Bacteriol 173:5371–5384

    PubMed  CAS  Google Scholar 

  • Dazzo FB, Orgambide G, Philip-Hollingsworth S, Hollingsworth RI, Ninke K, Salzwedel JL (1996) Modulation of development, growth dynamics, wall crystallinity, and infection thread formation in white clover root hairs by membrane chitolipooligosaccharides from Rhizobium leguminosarum bv. trifolii. J Bacteriol 178:3621–3627

    PubMed  CAS  Google Scholar 

  • De Hoff D, Brill LM, Hirsch AM (2009) Plant lectins: the ties that bind in root symbiosis and plant defense. Mol Genet 282:1–15

    Google Scholar 

  • D'Haeze W, Holsters M (2004) Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol 12:555–561

    Article  PubMed  CAS  Google Scholar 

  • Diebold R, Noel KD (1989) Rhizobium leguminosarum exopolysaccharide mutants: biochemical and genetic analyses and symbiotic behaviour on three hosts. J Bacteriol 171:4821–4827

    PubMed  CAS  Google Scholar 

  • Djordjevic SP, Chen H, Batley M, Redmond JW, Rolfe BG (1987a) Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides. J Bacteriol 169:53–60

    PubMed  CAS  Google Scholar 

  • Djordjevic M, Redmond J, Batley M, Rolfe B (1987b) Clovers secrete specific phenolic-compounds which either stimulate or repress nod gene-expression in Rhizobium trifolii source. EMBO J 6:1173–1179

    PubMed  CAS  Google Scholar 

  • Dos Santos PC, Dean DR, Hu Y, Ribbe MW (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem Rev 104:1159–1173

    Article  PubMed  CAS  Google Scholar 

  • Edwards A, Frederix M, Wisniewski-Dyé 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(9):3059–3067

    Article  PubMed  CAS  Google Scholar 

  • Evans HJ, Harker AR, Papen H, Russell SA, Hanus FJ, Zuber M (1987) Physiology, biochemistry and genetics of the uptake hydrogenase in Rhizobium. Annu Rev Microbiol 41:335–361

    Article  PubMed  CAS  Google Scholar 

  • Fernández D, Toffanin A, Palacios JM, Ruiz-Argüeso T, Imperial J (2005) Hydrogenase genes are uncommon and highly conserved in Rhizobium leguminosarum bv. viciae. FEMS Microbiol Lett 253:83–88

    Article  PubMed  CAS  Google Scholar 

  • Flemetakis E, Kavroulakis N, Quaedvlieg NE, Spaink HP, Dimou M, Roussis A, Katinakis P (2000) Lotus japonicus contains two distinct ENOD40 genes that are expressed in symbiotic, nonsymbiotic, and embryonic tissues. Mol Plant Microbe Interact 13:987–994

    Article  PubMed  CAS  Google Scholar 

  • Forsberg LS, Carlson RW (1998) The structures of the lipopolysaccharides from Rhizobium etli strains CE358 and CE359 - the complete structure of the core region of R. etli lipopolysaccharides. J Biol Chem 273:2747–2757

    Article  PubMed  CAS  Google Scholar 

  • Forsberg LS, Reuhs B (1997) Structural characterization of the K antigens from Rhizobium fredii USDA257: evidence for a common structural motif, with strain-specific variation, in the capsular polysaccharides of Rhizobium spp. J Bacteriol 179:5366–5371

    PubMed  CAS  Google Scholar 

  • Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 270:1365–1380

    Article  PubMed  CAS  Google Scholar 

  • Gage DJ (2002) Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184:7042–7046

    Article  PubMed  CAS  Google Scholar 

  • Garrocho-Villegas V, Gopalasubramaniam SK, Arredondo-Peter R (2007) Plant hemoglobins: what we know six decades after their discovery. Gene 398:78–85

    Article  PubMed  CAS  Google Scholar 

  • Gibson QH, Wittenberg JB, Wittenberg BA, Bogusz D, Appleby CA (1989) The kinetics of ligand binding to plant hemoglobins J Biol Chem 264:100–107

    CAS  Google Scholar 

  • Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Ann Rev Genet 42:413–441

    Article  PubMed  CAS  Google Scholar 

  • Girard G, Roussis A, Gultyaev AP, Pleij CW, Spaink HP (2003) Structural motifs in the RNA encoded by the early nodulation gene enod40 of soybean. Nucleic Acids Res 31:5003–5015

    Article  PubMed  CAS  Google Scholar 

  • Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Verméglio A, Médigue C, Sadowsky M (2007) Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • González JE, Marketon MM (2003) Quorum sensing in nitrogen-fixing rhizobia. Microbiol Mol Biol Rev 67:574–592

    Article  PubMed  CAS  Google Scholar 

  • Gray XJ, Zhan H, Levery SB, Battisti L, Rolfe BG, Leigh JA (1991) Heterologous exopolysaccharide production in Rhizobium sp. strain NGR234 and consequences for nodule development. J Bacteriol 173:3066–3077

    PubMed  CAS  Google Scholar 

  • Gronlund M, Roussis A, Flemetakis E, Quaedvlieg NE, Schlaman HR, Umehara Y, Katinakis P, Stougaard J, Spaink HP (2005) Analysis of promoter activity of the early nodulin Enod40 in Lotus japonicus. Mol Plant Microbe Interact 18:414–427

    Article  PubMed  CAS  Google Scholar 

  • Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15:981–991

    Article  PubMed  CAS  Google Scholar 

  • Gulash M, Ames P, Larosiliere RC, Bergman K (1984) Rhizobia are attracted to localized sites on legume roots. Appl Environ Microbiol 48:149–152

    PubMed  CAS  Google Scholar 

  • Hamblin J, Kent SP (1973) Possible role of phytohemagglutinin in Phaseolus vulgaris L. Nat New Biol 245:28–30

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto Y, Kondo T, Kageyama Y (2008) Lilliputians get into the limelight: novel class of small peptide genes in morphogenesis. Dev Growth Differ 50(Suppl 1):S269–276

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo E, Leyva A, Ruiz-Argüeso T (1990) Nucleotide sequence of the hydrogenase structural genes from Rhizobium leguminosarum. Plant Mol Biol 15:367–370

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM (1999) Role of lectins (and rhizobial exopolysaccharides) in legume nodulation. Curr Opin Plant Biol 2:320–326

    Article  PubMed  CAS  Google Scholar 

  • Horvath B, Heidstra R, Lados M, Moerman M, Spaink HP, Promé J-C, van Kammen A, Bisseling T (1993) Lipooligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J 4:727–733

    Article  PubMed  CAS  Google Scholar 

  • Howard JB, Rees DC (2006) Nitrogen Fixation Special Feature: How many metals does it take to fix N2? A mechanistic overview of biological nitrogen fixation. Proc Natl Acad Sci 103:17088–17093

    Article  PubMed  CAS  Google Scholar 

  • Hoy JA, Hargrove MS (2008) The structure and function of plant hemoglobins. Plant Physiol Biochem 46:371–379

    Article  PubMed  CAS  Google Scholar 

  • Hoy JA, Robinson JT, Kakar S, Smagghe BJ, Hargrove MS (2007) Plant hemoglobins: a molecular fossil record for the evolution of oxygen transport. J Mol Biol 371:168–179

    Article  PubMed  CAS  Google Scholar 

  • Hubbell D (1981) Legume infection by Rhizobium: a conceptual approach. BioScience 31:832–837

    Article  Google Scholar 

  • Hubbell DH, Morales VM, Umali-García M (1978) Pectolytic enzymes in Rhizobium. Appl Environ Microbiol 35:210–213

    PubMed  CAS  Google Scholar 

  • Hungria M, Joseph CM, Phillips DA (1991) Rhizobium nod gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol 97:759–764

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen-Lyon K, Jensen EO, Jorgensen JE, Marcker KA, Peacock WJ, Dennis ES (1995) Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell 7:213–223

    PubMed  CAS  Google Scholar 

  • Jeffreys AJ (1982) Evolution of globin genes. In: Dover GA, Flavell RB (eds) Genome Evolution. Academic Press, New York, pp 157–176

    Google Scholar 

  • Jensen EO, Paludan K, Hyldig-Nielsen JJ, Jorgensen P, Marcker KA (1981) The structure of a chromosomal leghaemoglobin gene from soybean. Nature 291:677–679

    Article  Google Scholar 

  • Jiménez-Zurdo JI, Mateos PF, Dazzo FB, Martínez-Molina E (1996a) Influence of the symbiotic plasmid (pSym) on cellulase production by Rhizobium leguminosarum bv. trifolii ANU843. Soil Biol Biochem 28:131–133

    Article  Google Scholar 

  • Jiménez-Zurdo JI, Mateos PF, Dazzo FB, Martínez-Molina E (1996b) Cell-bound cellulase and polygalacturonase production by Rhizobium and Bradyrhizobium species. Soil Biol Biochem 28:917–921

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kijne JW, Bauchrowitz MA, Díaz CL (1997) Root lectins and rhizobia. Plant Physiol 115:869–873

    PubMed  CAS  Google Scholar 

  • Kim CH, Tully RE, Keister DL (1989) Exopolysaccharide-deficient mutants of Rhizobium fredii HH303 which are symbiotically effective. Appl Environ Microbiol 55:1852–1859

    PubMed  CAS  Google Scholar 

  • Kobayashi H, Naciri-Graven Y, Broughton WJ, Perret X (2004) Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol Microbiol 51:335–347

    Article  PubMed  CAS  Google Scholar 

  • Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238:106–119

    PubMed  CAS  Google Scholar 

  • Kouchi H, Takane K, So RB, Ladha JK, Reddy PM (1999) Rice ENOD40: isolation and expression analysis in rice and transgenic soybean root nodules. Plant J 18:121–129

    Article  PubMed  CAS  Google Scholar 

  • Kubo H (1939) Über hämoprotein aus den wurzelknöllchen von leguminosen. Acta Phytochim (Tokyo) 11:195–200

    CAS  Google Scholar 

  • Kumagai H, Kinoshita E, Ridge RW, Kouchi H (2006) RNAi knock-down of ENOD40s leads to significant suppression of nodule formation in Lotus japonicus. Plant Cell Physiol 47:1102–1111

    Article  PubMed  CAS  Google Scholar 

  • Kundu S, Trent JT III, Hargrove MS (2003) Plants, humans and hemoglobins. Trends Plant Sci 8:387–393

    Article  PubMed  CAS  Google Scholar 

  • Lang K, Lindemann A, Hauser F, Göttfert M (2008) The genistein stimulon of Bradyrhizobium japonicum. Mol Genet Genomics 279:203–211

    Article  PubMed  CAS  Google Scholar 

  • Laporte P, Merchan F, Amor BB, Wirth S, Crespi M (2007) Riboregulators in plant development. Biochem Soc Trans 35:1638–1642

    Article  PubMed  CAS  Google Scholar 

  • Lerouge P, Roché P, Faucher C, Maillet F, Truchet G, Promé J-C, Dénarié J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784

    Article  PubMed  CAS  Google Scholar 

  • Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2 + and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  PubMed  CAS  Google Scholar 

  • Leyva A, Palacios JM, Ruiz-Argüeso T (1987) Cloning and characterization of hydrogen uptake genes from Rhizobium leguminosarum. Appl Environ Microbiol 53:2539–2543

    PubMed  CAS  Google Scholar 

  • Leyva A, Palacios JM, Murillo J, Ruiz-Argüeso T (1990) Genetic organization of the hydrogen uptake (hup) cluster from Rhizobium leguminosarum. J Bacteriol 172:1647–1655

    PubMed  CAS  Google Scholar 

  • Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633

    Article  PubMed  CAS  Google Scholar 

  • Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102:10375–10380

    Article  PubMed  CAS  Google Scholar 

  • Lioi L, Galasso I, Santantonio M, Lanave C, Bollini R, Sparvoli F (2006) Lectin gene sequences and species relationships among cultivated legumes. Genet Resour Crop Evol 53:1615–1623

    Article  CAS  Google Scholar 

  • 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 37:81–97

    Article  PubMed  CAS  Google Scholar 

  • Ljunggren H, Fahraeus G (1961) The role of polygalacturonase in root-hair invasion by nodule bacteria. J Gen Microbiol 26:521–528

    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 

  • López M, Carbonero V, Cabrera E, Ruiz-Argüeso T (1983) Effect of host on the expression of the H2-uptake hydrogenase of Rhizobium in legume nodules. Plant Sci Lett 29:191–199

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Molina E, Morales VM, Hubbell DH (1979) Hydrolytic enzyme production by Rhizobium. Appl Environ Microbiol 38:1186–1188

    PubMed  Google Scholar 

  • Mateos PF, Jiménez-Zurdo JI, Chen J, Squartini A, Haack S, Martínez-Molina E, Hubbell DH, Dazzo F (1992) Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 58:1816–1822

    PubMed  CAS  Google Scholar 

  • Mateos PF, Baker DL, Philiphollingsworth S, Squartini A, Peruffo ADB, Nuti MP, Dazzo F (1995) Direct in-situ identification of cellulose microfibrils associated with Rhizobium leguminosarum biovar trifolii attached to the root epidermis of white clover. Can J Microbiol 41:202–207

    Article  CAS  Google Scholar 

  • Mateos PF, Baker D, Petersen M, Velázquez E, Jiménez-Zurdo JI, Martínez-Molina E, Squartini A, Orgambide G, Hubbell D, Dazzo FB (2001) Erosion of root epidermal cell walls by Rhizobium polysaccharide-degrading enzymes as related to primary host infection in the Rhizobium-legume symbiosis. Can J Microbiol 47:475–487

    PubMed  CAS  Google Scholar 

  • Mathesius U (2009) Comparative proteomic studies of root-microbe interactions. J Proteomics 72:353–366

    Article  PubMed  CAS  Google Scholar 

  • Matvienko M, van de Sande K, Yang WC, van Kammen A, Bisseling T, Franssen H (1994) Comparison of soybean and pea ENOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Mol Biol 26:487–493

    Article  PubMed  CAS  Google Scholar 

  • Maxwell CA, Hartwig UA, Joseph CM, Phillips DA (1989) A chalcone and 2 related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol 91:842–847

    Article  PubMed  CAS  Google Scholar 

  • McAnulla C, Edwards A, Sanchez-Contreras M, Sawers RG, Downie JA (2007) Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar viciae. Microbiology 153:2074–2082

    Article  PubMed  CAS  Google Scholar 

  • McCoy E (1932) Infection by Bact. radicicola in relation to the microchemistry of the host's cell walls. Proc Royal Society B 110:514–533

    Article  CAS  Google Scholar 

  • Miller LD, Yost CK, Hynes MF, Alexandre G (2007) The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol Microbiol 63:348–362

    Article  PubMed  CAS  Google Scholar 

  • Morales V, Martínez-Molina E, Hubbell D (1984) Cellulase production by Rhizobium. Plant Soil 80:407–415

    Article  CAS  Google Scholar 

  • Muñoz JA, Coronado C, Pérez-Hormaeche J, Kondorosi A, Ratet P, Palomares AJ (1998) MsPG3, a Medicago sativa polygalacturonase gene expressed during the alfalfa-Rhizobium meliloti interaction. Proc Natl Acad Sci USA 95:9687–9692

    Article  PubMed  Google Scholar 

  • Napoli C, Dazzo F, Hubbell D (1975) Production of cellulose microfibrils by Rhizobium. Appl Microbiol 30:123–131

    PubMed  CAS  Google Scholar 

  • Niwa S, Kawaguchi M, Imazumi-Anraku H, Chechetka SA, Ishizaka M, Ikuta A, Kouchi H (2001) Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. Mol Plant Microbe Interact 14:848–856

    Article  PubMed  CAS  Google Scholar 

  • Novák K, Chovanec P, Skrdleta V, Kropácová M, Lisá L, Nemcová M (2002) Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.). J Exp Bot 53:1735–1745

    Article  PubMed  CAS  Google Scholar 

  • Nutman P, Doncaster C, Dart P (1973) Infection of clover by root-nodule bacteria. British Film Institute, London, UK

    Google Scholar 

  • Ott T, van Dongen JT, Günther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535

    Article  PubMed  CAS  Google Scholar 

  • Palacios JM, Manyani H, Martínez M, Ureta AC, Brito B, Básscones E, Rey L, Imperial J, Ruiz-Argüeso T (2005) Genetics and biotechnology of the H2-uptake [NiFe] hydrogenase from Rhizobium leguminosarum bv. viciae, a legume endosymbiotic bacterium. Biochem Soc Trans 33:94–96

    Article  PubMed  CAS  Google Scholar 

  • Papadopoulou K, Roussis A, Katinakis P (1996) Phaseolus ENOD40 is involved in symbiotic and non-symbiotic organogenetic processes: expression during nodule and lateral root development. Plant Mol Biol 30:403–417

    Article  PubMed  CAS  Google Scholar 

  • Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427

    Article  PubMed  CAS  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(18):5067–5076

    Article  PubMed  CAS  Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Article  PubMed  CAS  Google Scholar 

  • Pesce A, Couture M, Dewilde S, Guertin M, Yamauchi K, Ascenzi P, Moens L, Bolognesi M (2000) A novel two-over-two alpha-helical sandwich fold is characteristic of the truncated hemoglobin family. EMBO J 19:2424–2434

    Article  PubMed  CAS  Google Scholar 

  • Podkowinski J, Zmienko A, Florek B, Wojciechowski P, Rybarczyk A, Wrzesinski J, Ciesiolka J, Blazewicz J, Kondorosi A, Crespi M, Legocki A (2009) Translational and structural analysis of the shortest legume ENOD40 gene in Lupinus luteus. Acta Biochim Pol 56:89–102

    PubMed  CAS  Google Scholar 

  • Recourt K, Schripsema J, Kijne JW, Vanbrussel AAN (1991) Lugtenberg BJJ. Inoculation of Vicia sativa subsp nigra roots with Rhizobium leguminosarum biovar viciae results in release of nod gene activating flavanones and chalcones Plant Mol Biol 16:841–852

    CAS  Google Scholar 

  • Rees DC, Howard JB (2000) Nitrogenase: standing at the crossroads. Curr Opin Chem Biol 4:559–566

    Article  PubMed  CAS  Google Scholar 

  • Renier A, Jourand P, Rapior S, Poinsot V, Sy A, Dreyfus B, Moulin L (2008) Symbiotic properties of Methylobacterium nodulans ORS 2060(T): A classic process for an atypical symbiont. Soil Biol Biochem 40:4104–1412

    Article  CAS  Google Scholar 

  • Reuhs BL, Carlson RW, Kim JS (1993) Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-D-manno-2-octulosonic acid-containing polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli. J Bacteriol 175:3570–3580

    PubMed  CAS  Google Scholar 

  • Reuhs BL, Williams MNV, Kim JS, Carlson RW, Cote F (1995) Suppression of the Fix-phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K-polysaccharide. J Bacteriol 177:4289–4296

    PubMed  CAS  Google Scholar 

  • Rey L, Murillo J, Hernando Y, Hidalgo E, Cabrera E, Imperial J, Ruiz-Argüeso T (1993) Molecular analysis of a microaerobically induced operon required for hydrogenase synthesis in Rhizobium leguminosarum bv. viciae. Mol Microbiol 8:471–481

    Article  PubMed  CAS  Google Scholar 

  • Robledo M, Jiménez-Zurdo JI, Velázquez E, Trujillo ME, Zurdo-Piñeiro JL, Ramírez-Bahena MH, Ramos B, Díaz-Mínguez JM, Dazzo F, Martínez-Molina E, Mateos PF (2008) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. Proc Natl Acad Sci USA 105:7064–7069

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Llorente ID, Pérez-Hormaeche J, Dary M, Caviedes MA, Kondorosi A, Ratet P, Palomares AJ (2003) Expression of MsPG3-GFP fusions in Medicago truncatula ‘hairy roots' reveals preferential tip localization of the protein in root hairs. Eur J Biochem 270:261–269

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Llorente ID, Pérez-Hormaeche J, El Mounadi K, Dary M, Caviedes MA, Cosson V, Kondorosi A, Ratet P, Palomares AJ (2004) From pollen tubes to infection threads: recruitment of Medicago floral pectic genes for symbiosis. Plant J 39:587–598

    Article  PubMed  CAS  Google Scholar 

  • Rohrig H, Schmidt J, Miklashevichs E, Schell J, John M (2002) Soybean ENOD40 encodes two peptides that bind to sucrose synthase. Proc Natl Acad Sci USA 99:1915–1920

    Article  PubMed  CAS  Google Scholar 

  • Ross EJH, Lira-Ruan V, Arredondo-Peter R, Klucas RV, Sarath G (2002) Recent insights into plant hemoglobins. Rev Plant Biochem Biotechnol 1:173–189

    Google Scholar 

  • Ruiz-Argüeso T, Imperial J, Palacios JM (2000) Uptake hydrogenases in root nodule bacteria. In: Triplett E.W (ed) Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific Press, Wymondham, pp 489–507

    Google Scholar 

  • Ruiz-Argüeso T, Maier RJ, Evans HJ (1979) Hydrogen Evolution from Alfalfa and Clover Nodules and Hydrogen Uptake by Free-Living Rhizobium meliloti. Appl Environ Microbiol 37:582–587

    PubMed  Google Scholar 

  • Sánchez-Contreras M, Bauer WD, Gao M, Robinson JB, Allan Downie J (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc Lond B Biol Sci 362:1149–1163

    Article  PubMed  CAS  Google Scholar 

  • Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quéré A, Wollherr A, Heinemeyer I, Morgenstern B, Pommerening-Röser A, Flores M, Palacios R, Brenner S, Gottschalk G, Schmitz RA, Broughton WJ, Perret X, Strittmatter AW, Streit WR (2009) Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75:4035–4045

    Article  PubMed  CAS  Google Scholar 

  • Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57

    Article  PubMed  CAS  Google Scholar 

  • Simpson FB, Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–1097

    Article  PubMed  CAS  Google Scholar 

  • Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 16:5–7

    Google Scholar 

  • Smit G, Swart S, Lugtenberg BJ, Kijne JW (1992) Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 6:2897–2903

    Article  PubMed  CAS  Google Scholar 

  • Soto MJ, Domínguez-Ferreras A, Pérez-Mendoza D, Sanjuán J, Olivares J (2009) Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell Microbiol 11:381–388

    Article  PubMed  CAS  Google Scholar 

  • Sousa C, Johansson C, Charon C, Manyani H, Sautter C, Kondorosi A, Crespi M (2001) Translational and structural requirements of the early nodulin gene enod40, a short-open reading frame-containing RNA, for elicitation of a cell-specific growth response in the alfalfa root cortex. Mol Cell Biol 21:354–366

    Article  PubMed  CAS  Google Scholar 

  • Spaink HP, Sheeley DM, van Brussel AAN, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJJ (1991) A novel highly saturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354:125–130

    Article  PubMed  CAS  Google Scholar 

  • Sreevidya VS, Hernandez-Oane RJ, So RB, Sullia SB, Stacey G, Ladha JK, Reddy PM (2005) Expression of the legume symbiotic lectin genes psl and gs52 promotes rhizobial colonization of roots in rice. Plant Sci 169:726–736

    Article  CAS  Google Scholar 

  • Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121

    Article  PubMed  CAS  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273

    Article  PubMed  CAS  Google Scholar 

  • Suominen L, Luukkainen R, Roos C, Lindström K (2003) Activation of the nodA promoter by the nodD genes of Rhizobium galegae induced by synthetic flavonoids or Galega orientalis root exudate. FEMS Microbiol Lett 219:225–232

    Article  PubMed  CAS  Google Scholar 

  • Taurian T, Morón B, Soria-Díaz ME, Angelini JG, Tejero-Mateo P, Gil-Serrano A, Megías M, Fabra A (2008) Signal molecules in the peanut-bradyrhizobia interaction. Arch Microbiol 189:345–356

    Article  PubMed  CAS  Google Scholar 

  • Taylor ER, Nie XZ, MacGregor AW, Hill RD (1994) A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol 24:853–862

    Article  PubMed  CAS  Google Scholar 

  • Tjepkema JD (1983) Hemoglobins in the nitrogen-fixing root nodules of actinorhizal plants. Can J Bot 61:2924–2929

    Article  CAS  Google Scholar 

  • Trevaskis B, Watts RA, Andersson CR, Llewellyn DJ, Hargrove MS, Olson JS, Dennis ES, Peacock WJ (1997) Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc Natl Acad Sci USA 94:12230–12234

    Article  PubMed  CAS  Google Scholar 

  • Ureta AC, Imperial J, Ruiz-Argüeso T, Palacios JM (2005) Rhizobium leguminosarum biovar viciae symbiotic hydrogenase activity and processing are limited by the level of nickel in agricultural soils. Appl Environ Microbiol 71:7603–7606

    Article  PubMed  CAS  Google Scholar 

  • Van Damme EJM, Barre A, Rougé P, Peumans WJ (2004) Cytoplasmic/nuclear plant lectins: a new story. Trends Plant Sci 9:484–489

    Article  PubMed  CAS  Google Scholar 

  • van Rhijn P, Fujishige NA, Lim P-O, Hirsch AM (2001) Sugar-binding activity of pea (Pisum sativum) lectin is essential for heterologous infection of transgenic alfalfa (Medicago sativa L.) plants by Rhizobium leguminosarum biovar viciae. Plant Physiol 125:133–144

    Article  Google Scholar 

  • Van Soom C, Browaeys J, Verreth C, Vanderleyden J (1993) Nucleotide sequence analysis of four genes, hupC, hupD, hupF and hupG, downstream of the hydrogenase structural genes in Bradyrhizobium japonicum. J Mol Biol 234:508–512

    Article  PubMed  Google Scholar 

  • Vance CP, Heichel G (1991) Carbon in N2 fixation: limitation and exquisite adaptation. Ann Rev Plant Physiol 42:373–392

    CAS  Google Scholar 

  • Varkonyi-Gasic E, White DW (2002) The white clover enod40 gene family. Expression patterns of two types of genes indicate a role in vascular function. Plant Physiol 129:1107–1118, Erratum in: Plant Physiol 2002 130:514

    Article  PubMed  CAS  Google Scholar 

  • Vijn I, Yang WC, Pallisgård N, Ostergaard Jensen E, van Kammen A, Bisseling T (1995) VsENOD5, VsENOD12 and VsENOD40 expression during Rhizobium-induced nodule formation on Vicia sativa roots. Plant Mol Biol 28:1111–1119

    Article  PubMed  CAS  Google Scholar 

  • Virtanen AI, Laine TR (1946) brown and green pigments in leguminous root nodules. Nature 1157:25–26

    Article  Google Scholar 

  • Vleghels I, Hontelez J, Ribeiro A, Fransz P, Bisseling T, Franssen H (2003) Expression of ENOD40 during tomato plant development. Planta 218:42–49

    Article  PubMed  CAS  Google Scholar 

  • Wan X, Hontelez J, Lillo A, Guarnerio C, van de Peut D, Fedorova E, Bisseling T, Franssen H (2007) Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development. J Exp Bot 58:2033–2041

    Article  PubMed  CAS  Google Scholar 

  • 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 182:520–525

    Article  PubMed  CAS  Google Scholar 

  • Watts RA, Hunt PW, Hvitved AN, Hargrove MS, Peacock WJ, Dennis ES (2001) A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proc Natl Acad Sci USA 98:10119–10124

    Article  PubMed  CAS  Google Scholar 

  • Wei M, Yokoyama T, Minamisawa K, Mitsui H, Itakura M, Kaneko T, Tabata S, Saeki K, Omori H, Tajima S, Uchiumi T, Abe M, Ohwada T (2008) Soybean seed extracts preferentially express genomic loci of Bradyrhizobium japonicum in the initial interaction with soybean, Glycine max (L.) Merr. DNA Res 15:201–214

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

    Article  PubMed  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 

  • Wittenberg JB, Bergersen FJ, Appleby CA, Turner GL (1974) Facilitated oxygen diffusion: the role of leghemoglobin in nitrogen fixation by bacteroids isolated from soybean root nodules. J Biol Chem 249:4057–4066

    PubMed  CAS  Google Scholar 

  • Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277:871–874

    Article  PubMed  CAS  Google Scholar 

  • Yan XR, Chen WF, Fu JF, Lu YL, Xue CY, Sui XH, Li Y, Wang ET, Chen WX (2007) Mesorhizobium spp. are the main microsymbionts of Caragana spp. grown in Liaoning Province of China. FEMS Microbiol Lett 271:265–273

    Article  PubMed  CAS  Google Scholar 

  • Yeh KC, Peck MC, Long SR (2002) Luteolin and GroESL modulate in vitro activity of NodD. J Bacteriol 184:525–530

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank our numerous collaborators and students involved in this research over the years. Funding was provided by Ministerio de Ciencia e Innovación and Junta de Castilla y León from Spain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alvaro Peix .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag/Wien

About this chapter

Cite this chapter

Peix, A., Velázquez, E., Silva, L.R., Mateos, P.F. (2010). Key Molecules Involved in Beneficial Infection Process in Rhizobia–Legume Symbiosis. In: Khan, M.S., Musarrat, J., Zaidi, A. (eds) Microbes for Legume Improvement. Springer, Vienna. https://doi.org/10.1007/978-3-211-99753-6_3

Download citation

Publish with us

Policies and ethics