Skip to main content

Enhancing Rhizobium–Legume Symbiosis Using Signaling Factors

  • Chapter
Microbes for Legume Improvement

Abstract

Rhizobial symbiosis with leguminous plants affects the supply of organic nitrogen. Soil bacteria comprising members of the genera Rhizobium, Bradyrhizobium, Mesorhizobium, Sinorhizobium, and Azorhizobium, commonly referred to as rhizobia, are taxonomically diverse members of the α and β subclasses of the Proteobacteria. They possess the ability to induce root nodules on legume plants and provide these plants with fixed nitrogen, enabling them to grow in nitrogen-limited soils. Rhizobia colonize root nodules, fix nitrogen inside, transport usable form of N to plants, and concurrently facilitate the growth and grain yields of legumes. Rhizobium–legume symbiosis is a multi-step process requiring the exchange of numerous molecular signals between bacteria and the plant host. Precise fulfilling of all stages of this molecular dialogue is prerequisite to the effective symbiosis, allowing bacteria to invade the host and, conversely, enabling the host to derive benefits from the presence of bacteria. Individual legumes are often nodulated by multiple bacterial strains with varying symbiosis-establishing capabilities. Thus, selection of highly effective strains that successfully compete with less effective ones is required when developing legume inoculants. Various factors that influence symbiotic rhizobial interactions under competitive soil environment, including the exchange of plant and bacterial signaling molecules, such as flavonoids and nodulation factor (Nod factor), in the early stages of symbiosis is highlighted. Beneficial responses of rhizobial inoculants on to legumes, as well as manipulations of symbiotic signaling factors, is likely to increase their potential as biofertilizers for sustainable agriculture to promote growth and nodulation of legume plants.

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

  • Andrade DS, Murphy PJ, Giller KJ (2002) The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Appl Environ Microbiol 68:4025–4034

    Article  PubMed  CAS  Google Scholar 

  • Bailly X, Oliveri I, Brunel B, Cleyet-Marel JC, Bena G (2007) Host-specialization and speciation in the symbiotic nitrogen-fixing Sinorhizobium associated with Medicago. J Bacteriol 189:5223–5236

    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 

  • Beattie GA, Clayton MK, Handelsman J (1989) Quantitative comparison of the laboratory and field competitiveness of Rhizobium leguminosarum biovar phaseoli. Appl Environ Microbiol 55:2755–2761

    PubMed  CAS  Google Scholar 

  • Beattie GA, Handelsman J (1993) Evaluation of a strategy for identifying nodulation competitiveness genes in Rhizobium leguminosarum biovar phaseoli. J Gen Microbiol 139:529–538

    PubMed  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 152:1537–1543

    Article  Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 1:155–194

    Article  CAS  Google Scholar 

  • Brewin NJ (2004) Plant cell wall remodeling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23:293–316

    Article  CAS  Google Scholar 

  • Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27:683–697

    Article  CAS  Google Scholar 

  • Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180

    Article  CAS  Google Scholar 

  • Brom S, de los Santos AG, de Lourdes Girard M, Davilla G, Palacios R, Romero D (1991) High-frequency rearrangements in Rhizobium leguminosarum bv. phaseoli plasmids. J Bacteriol 173:1344–1346

    PubMed  CAS  Google Scholar 

  • Brom S, de los Santos AG, Stepkowsky T, Flores M, Davilla G, Romero D, Palacios R (1992) Different plasmids of Rhizobium leguminosarum bv. phaseoli are required for optimal symbiotic performance. J Bacteriol 174:5183–5189

    PubMed  CAS  Google Scholar 

  • Bromfield ESP, Lewis DM, Barran LR (1985) Cryptic plasmid and rifampin resistance in Rhizobium meliloti influencing nodulation competitiveness. J Bacteriol 164:410–413

    PubMed  CAS  Google Scholar 

  • Broughton WJ, Samrey U, Stanley J (1987) Ecological genetics of Rhizobium meliloti: symbiotic plasmid transfer in the Medicago sativa rhizosphere. FEMS Microbiol Lett 40:251–255

    Article  CAS  Google Scholar 

  • Burgos PA, Castellanos J, Mora Y, Mora J (1999) Field inoculation of common bean (Phaseolus vulgaris L.) with high efficiency Rhizobium strains. In: Martínez E, Hernández G (eds) Highlights of nitrogen fixation research. Kluwer Academic/Plenum Publishers, New York, pp 255–257

    Chapter  Google Scholar 

  • Caetano-Anollés G, Crist-Estes DK, Bauer WD (1988) Chemotaxis of Rhizobium meliloti on the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170:3164–3169

    PubMed  CAS  Google Scholar 

  • Campbell GRO, Reuhs BL, Walker GC (2002) Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc Natl Acad Sci USA 99:3938–3943

    Article  PubMed  CAS  Google Scholar 

  • Cardenas L, Dominguez J, Qiunto C, Lopez-Lara IM, Lugtenberg BJJ, Spaink HP, Rademarker GJ, Haverkamp J, Thomas-Oates JE (1995) Isolation, chemical structures and biological activity of lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol Biol 29:453–464

    Article  PubMed  CAS  Google Scholar 

  • Castillo M, Flores M, Mavingui P, Martinez-Romero E, Palacios R, Hernandez G (1999) Increase in alfafa nodulation, nitrogen fixation, and plant growth by specific DNA amplification in Sinorhizobium meliloti. Appl Environ Microbiol 65:2716–2722

    PubMed  CAS  Google Scholar 

  • Chen H-C, Feng J, Hou B-H, Li F-Q, Li Q, Hong G-F (2005) Modulating DNA bending affects NodD-mediated transcriptional control in Rhizobium leguminosarum. Nucleic Acid Res 33:2540–2548

    Article  PubMed  CAS  Google Scholar 

  • Chen WM, Laevens S, Lee TM, Coenye T, de Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735

    Article  PubMed  CAS  Google Scholar 

  • Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res 41:1–62

    Article  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 

  • Cren M, Kondorosi A, Kondorosi E (1995) NolR controls expression of the Rhizobium meliloti nodulation genes involved in the core Nod factor synthesis. Mol Microbiol 15:733–747

    Article  PubMed  CAS  Google Scholar 

  • D’Haeze W, Holsters M (2002) Nod factor structures, responses and perception during initiation of nodule development. Glycobiol 12:79–105

    Article  Google Scholar 

  • De Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, Schiavo FL, Terzi M, Bisseling T, Van Kammen A, De Vries SC (1993) Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5:615–620

    PubMed  Google Scholar 

  • De Weert S, Dekkers LC, Kuiper I, Bolemberg GV, Lugtenberg BJJ (2004) Generation of enhanced competitive root-tip-colonizing Pseudomonas bacteria through accelerated evolution. J Bacteriol 186:3153–3159

    Article  PubMed  CAS  Google Scholar 

  • Deavours BE, Liu CJ, Naoumkina MA, Tang YH, Farag MA, Sumner LW, Noel JP, Dixon RA (2006) Functional analysis of members of the isoflavone and isoflavanone O-methyltransferase enzyme families from the model legume Medicago truncatula. Plant Mol Biol 62:715–733

    Article  PubMed  CAS  Google Scholar 

  • Debellé F, Rosenberg C, Vasse J, Maillet F, Martinez E, Dénarié J, Truchet G (1986) Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. J Bacteriol 168:1075–1086

    PubMed  Google Scholar 

  • Dénarié J, Cullimore J (1993) Lipo-oligosaccharide nodulation factors: New class of signaling molecules mediating recognition and morphogenesis. Cell 74:951–954

    Article  PubMed  Google Scholar 

  • Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-oligosaccharide nodulation factors: signalling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

    Article  PubMed  Google Scholar 

  • Depret G, Laguerre G (2008) Plant phenology and genetic variability in root and nodule development strongly influence genetic structuring of Rhizobium leguminosarum biovar viciae populations nodulating pea. New Phytol 179:224–235

    Article  PubMed  Google Scholar 

  • Dharmatilake AJ, Bauer WD (1992) Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Appl Environ Microbiol 58:1153–1158

    PubMed  CAS  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    PubMed  CAS  Google Scholar 

  • Dombrecht B, Tesfay MZ, Verreth C, Heusdens C, Napoles MC, Vanderleyden J, Michiels J (2002) The Rhizobium etli gene iscN is highly expressed in bacteroids and required for nitrogen fixation. Mol Gen Genomics 267:820–828

    Article  CAS  Google Scholar 

  • Doyle JJ (1998) Phylogenetic perspectives of nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3:473–478

    Article  Google Scholar 

  • Duodu S, Brophy C, Connolly J, Svenning MM (2009) Competitiveness of native Rhizobium leguminosarum bv. trifolii strain for nodule occupancy is manifested during infection. Plant Soil 318:117–126

    Article  CAS  Google Scholar 

  • Dyachok JV, Tobin AE, Price NPJ, von Arnold S (2000) Rhizobial Nod factors stimulate somatic embryo development in Picea abies. Plant Cell Rep 19:290–297

    Article  CAS  Google Scholar 

  • Fagerli IL, Svenning MM (2005) Arctic and subarctic soil populations of Rhizobium leguminosarum biovar trifolii nodulating three different clover species: characterization by diversity of chromosomal and symbiosis loci. Plant Soil 275:371–381

    Article  CAS  Google Scholar 

  • Faure D, Vereecke D, Leveau JHJ (2009) Molecular communication in rhizosphere. Plant Soil 321:279–303

    Article  CAS  Google Scholar 

  • Fedorova M, van de Mortel J, Matsumoto PA, Cho J, Town CD, VandenBosch KA, Gantt JS, Vance CP (2002) Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol 130:519–537

    Article  PubMed  CAS  Google Scholar 

  • Feng J, Li Q, Hu HL, Chen XC, Hong GF (2003) Inactivation of the nod box distal half-site allows tetrameric NodD to activate nodA transcription in an inducer-independent manner. Nucleic Acids Res 31:3143–3156

    Article  PubMed  CAS  Google Scholar 

  • Firmin JL, Wilson KE, Rossen L, Johnston AWB (1986) Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324:90–92

    Article  CAS  Google Scholar 

  • Fisher HM (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386

    Google Scholar 

  • Fisher RF, Egelhoff TT, Mulligan JT, Long SR (1988) Specific binding of Rhizobium meliloti extracts containing nodD to DNA sequences upstream of inducible nodulation genes. Genes Dev 2:282–293

    Article  PubMed  CAS  Google Scholar 

  • Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59

    Article  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 

  • Frugier F, Kosuta S, Murray JD, Crespi M, Szczygłowski K (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci 13:115–120

    Article  PubMed  CAS  Google Scholar 

  • Fujishige NA, Lum MR, de Hoff PL, Whitelegge JP, Faull KF, Hirsch AM (2008) Rhizobium common nod genes are required for biofilm formation. Mol Microbiol 67:504–515

    Article  PubMed  CAS  Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  PubMed  CAS  Google Scholar 

  • Gagnon H, Ibrahim RK (1998) Aldonic acids: a novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti. Mol Plant-Microbe Interact 11:988–998

    Article  CAS  Google Scholar 

  • Galibert F, Finan TM, Long SR, Pühler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dréano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thébault P, Vandenbol M, Vorhölter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    Article  PubMed  CAS  Google Scholar 

  • Gaworzewska ET, Carlile MJ (1982) Positive chemotaxis of Rhizobium leguminosarum and other bacteria towards root exudates from legumes and other plants. J Gen Microbiol 128:1179–1188

    CAS  Google Scholar 

  • Gemel LG, Roughley RJ (1993) Field evaluation in acid soils of strains of Rhizobium leguminosarum bv. trifolii selected for their tolerance or sensitivity to acid soil factors in agar medium. Soil Biol Biochem 25:1447–1452

    Article  Google Scholar 

  • Geurts R, Fedorova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8:346–352

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Giller KE, Cadisch G (1995) Future benefits from biological nitrogen fixation: an ecological approach to agriculture. Plant Soil 174:255–277

    Article  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, Vermeglio A, Medigue C, Sadovsky M (2007) Legume symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • Goldmann A, Boivin C, Fleury V, Message B, Lecoeur L, Maille M, Tepfer D (1991) Betaine use by rhizosphere bacteria: genes essential for trigonelline, stachydrine and carnitine catabolism in Rhizobium meliloti are located on pSym in the symbiotic region. Mol Plant-Microbe Interact 4:571–578

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez V, Santamaria RI, Bustos P, Hernández-González I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramírez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103:3834–3839

    Article  PubMed  Google Scholar 

  • Gőttfert M, Grob P, Hennecke H (1990) Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc Natl Acad Sci USA 87:2680–2684

    Article  PubMed  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: importance and constraints to greater utilization. Plant Physiol 131:872–877

    Article  PubMed  CAS  Google Scholar 

  • Guo X, Flores M, Mavingui P, Fuentes SI, Hernandez G, Davila G, Palacios R (2003) Natural genomics design in Sinorhizobium meliloti: novel genomic architectures. Genome Res 8:1810–1817

    Google Scholar 

  • Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microbe Interact 22:763–772

    Article  PubMed  CAS  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    Article  PubMed  CAS  Google Scholar 

  • Harborne JB, Williams CA (2001) Anthocyanins and other flavonoids. Nat Prod Rep 18:310–333

    Article  PubMed  CAS  Google Scholar 

  • Hartwig UA, Maxwell CA, Joseph CM, Phillips DA (1990) Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes. J Bacteriol 172:2769–2773

    PubMed  CAS  Google Scholar 

  • Heidstra R, Bisseling T (1996) Nod factor-induced host responses and mechanisms of Nod factor perception. New Phytol 133:25–43

    Article  CAS  Google Scholar 

  • Herridge D, Gemell G, Hartley E (2002) Legume inoculants and quality control. In: Herridge D (ed) Inoculants and nitrogen fixation of legumes in Vietnam, ACIAR Proceedings 109e. PK Editorial Service, Australia, Brisbane

    Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hogg B, Davies AE, Wilson KE, Bisseling T, Downie JA (2002) Competitive nodulation blocking of cv. Afghanistan pea is related to high level of nodulation factors made by some strains of Rhizobium leguminosarum bv. viciae. Mol Plant-Microbe Interact 15:60–68

    Article  PubMed  CAS  Google Scholar 

  • Hong GF, Burn JE, Johnston AWB (1987) Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucleic Acids Res 15:9677–9690

    Article  PubMed  CAS  Google Scholar 

  • Horvath B, Kondorosi E, John M, Schmidt J, Török I, Györgypal Z, Barabas I, Wieneke U, Schell J, Kondorosi A (1986) Organization, structure and symbiotic function of Rhizobium meliloti nodulation genes determining host specificity for alfalfa. Cell 46:335–343

    Article  PubMed  CAS  Google Scholar 

  • Hotter GS, Scott DB (1991) Exopolysaccharide mutants of Rhizobium loti are fully effective on a determinate nodulating host but are ineffective on an indeterminate nodulating host. J Bacteriol 173:851–859

    PubMed  CAS  Google Scholar 

  • Hungria M, Phillips DA (1993) Effects of a seed color mutation on rhizobial nod-gene-inducing flavonoids and nodulation in common bean. Mol Plant-Microbe Interact 6:418–422

    Article  CAS  Google Scholar 

  • Hungria M, Stacey G (1997) Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture. Soil Biol Biochem 29:819–830

    Article  CAS  Google Scholar 

  • Hynes MF, O’Connel MP (1990) Host plant effect on competition among strains of Rhizobium leguminosarum. Can J Microbiol 36:864–869

    Article  Google Scholar 

  • Jacobs TW, Egelhoff TT, Long SR (1985) Physical and genetic map of a Rhizobium meliloti nodulation gene region and nucleotide sequence of nodC. J Bacteriol 162:469–476

    PubMed  CAS  Google Scholar 

  • Jaeger CH, Lindow SE, Miller W, Clark E, Firestone MK (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl Environ Microbiol 65:2685–2690

    PubMed  CAS  Google Scholar 

  • Jensen ES, Sorensen LH (1987) Survival of Rhizobium leguminosarum is soil after addition as inoculant. FEMS Microbiol Ecol 45:221–226

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kaminski PA, Batut J, Boistard P (1998) A survey of symbiotic nitrogen fixation by rhizobia. In: Spaink HP, Kondorosi A, Hooykaas PJ (eds) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Kluver Academic Publisher, Dordrecht, The Netherland, pp 426–490

    Google Scholar 

  • Kannenberg EL, Perzl M, Hartner T (1995) The occurrence of hopanoid lipids in Bradyrhizobium bacteria. FEMS Microbiol Lett 127:255–262

    Article  CAS  Google Scholar 

  • Kapulnik Y, Joseph CM, Phillips DA (1987) Flavone limitation to root nodulation and symbiotic nitrogen fixation in alfalfa. Plant Physiol 84:1193–1196

    Article  PubMed  CAS  Google Scholar 

  • Knee EM, Gong FC, Gao M, Teplitski M, Jones AM, Foxworthy A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol plant-Microbe Interact 14:775–784

    Article  PubMed  CAS  Google Scholar 

  • Knight CD, Rossen L, Robertson JG, Wells B, Downie JA (1986) Nodulation inhibition by Rhizobium leguminosarum multicopy nodABC genes and analysis of early stages of plant infection. J Bacteriol 166:552–558

    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 

  • Kondorosi E, Gyuris J, Schmidt J, John E, Hofmann DB, Schell J, Kondorosi A (1989) Positive and negative control of nod gene expression in Rhizobium meliloti is reqiured for optimal nodulation. EMBO J 8:1331–1340

    PubMed  CAS  Google Scholar 

  • Kondorosi E, Pierre M, Cren M, Haumann U, Buire M, Hoffmann B, Schell J, Kondorosi A (1991) Identification of NolR, a negative transacting factor controlling the nod regulon in Rhizobium meliloti. J Mol Biol 222:885–896

    Article  PubMed  CAS  Google Scholar 

  • Kosslak RM, Bookland R, Berkei J, Paaren HE, Applebaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci USA 84:7428–7432

    Article  PubMed  CAS  Google Scholar 

  • Kosslak RM, Joshi RS, Bowen BA, Paaren HE, Applebaum ER (1990) Strain-specific inhibition of nod gene induction in Bradyrhizobium japonicum by flavonoid compounds. Appl Environ Microbiol 56:1333–1341

    PubMed  CAS  Google Scholar 

  • Król J, Mazur A, Marczak M, Skorupska A (2007) Syntenic arrangements of the surface polysaccharide biosynthesis genes in Rhizobium leguminosarum. Genomics 89:237–247

    Article  PubMed  CAS  Google Scholar 

  • Laguerre G, Courde L, Nouaim R, Lamy I, Revellin C, Breuil MC, Chaussod R (2006) Response of rhizobial populations to moderate copper stress applied to an agricultural soil. Microbiol Ecol 52:426–435

    Article  CAS  Google Scholar 

  • Laguerre G, Louvrier P, Allard MR, Amarger N (2003) Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulating of host legumes. Appl Environ Microbiol 69:2276–2283

    Article  PubMed  CAS  Google Scholar 

  • Leibovitch S, Migner P, Smith DL (2001) Evaluation of the effect of SoyaSignal technology on soybean yield [Glycine max (L.) Merr.] under field conditions over 6 years in Eastern Canada and the Northern United States. J Agron Crop Sci 187:281–292

    Article  CAS  Google Scholar 

  • Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, 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 

  • Lodwig E, Poole P (2003) Metabolism of Rhizobium bacteroids. CRC Crit Rev Plant Sci 22:37–78

    Article  CAS  Google Scholar 

  • Lohar DP, Schaff JE, Laskey G, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J 38:203–214

    Article  PubMed  CAS  Google Scholar 

  • Louvrier P, Laguerre G, Amarger N (1996) Distribution of symbiotic genotypes in Rhizobium leguminosarum biovar viciae populations isolated directly from soils. Appl Environ Microbiol 62:4202–4205

    PubMed  CAS  Google Scholar 

  • Lupwayi NZ, Haque I, Holl FB (1997) Effectiveness, competitiveness and persistence of inoculant Rhizobium in perennial African clovers in a highland. Vertisol J Agric Sci 129:429–437

    Article  Google Scholar 

  • Mabood F, Jung WJ, Smith DL (2008) Signals in the underground: microbial signaling and plant productivity. In: Nautiyal CS, Dion PE, Chopra VL (eds) Molecular mechanisms of plant and microbe coexistence. Springer-Verlag, Berlin, Heidelberg, pp 291–318

    Chapter  Google Scholar 

  • Mabood F, Smith DL (2005) Pre-incubation of Bradyrhizobium japonicum with jasmonates accelerates nodulation and nitrogen fixation in soybean (Glycine max) at optimal and suboptimal root zone temperatures. Physiol Plant 125:311–323

    Article  CAS  Google Scholar 

  • Mabood F, Souleimanov A, Khan W, Smith DL (2006) Jasmonates induce Nod factor production by Bradyrhizobium japonicum. Plant Physiol Biochem 44:759–765

    Article  PubMed  CAS  Google Scholar 

  • Macchiavelli RE, Brelles-Mariño G (2004) Nod factor-treated Medicago truncatula roots and seeds show an increased number of nodules when inoculated with a limiting population of Sinorhizobium meliloti. J Exp Bot 55:2635–2640

    Article  PubMed  CAS  Google Scholar 

  • Maier RJ, Triplett EW (1996) Toward more productive, efficient, and competitive nitrogen-fixing symbiotic bacteria. Crit Rev Plant Sci 15:191–234

    Google Scholar 

  • Maj D, Wielbo J, Marek-Kozaczuk M, Skorupska A (2009) Pretreatment of clover seeds with Nod factors improves growth and nodulation of Trifolium pratense. J Chem Ecol 35:479–487

    Article  PubMed  CAS  Google Scholar 

  • Maj D, Wielbo J, Marek-Kozaczuk M, Skorupska A (2010) Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiol Res 165:50–60

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Abarca F, Herrera-Cervera JA, Bueno P, Sanjuan J, Bisseling T, Olivares J (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol Plant Microbe Interact 11:153–155

    Article  CAS  Google Scholar 

  • Martínez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252:11–23

    Article  Google Scholar 

  • Martínez-Romero E (2009) Coevolution in Rhizobium-legume symbiosis? DNA Cell Biol 28:361–370

    Article  PubMed  CAS  Google Scholar 

  • Martyniuk S, Oroń J, Martyniuk M (2005) Diversity and numbers of root-nodule bacteria (rhizobia) in Polish soils. Acta Soc Bot Polon 74:83–86

    Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466

    Article  PubMed  CAS  Google Scholar 

  • Mathesius U, Schlaman HR, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34

    Article  PubMed  CAS  Google Scholar 

  • Mercado-Blanco J, Toro N (1996) Plasmids in rhizobia: the role of nonsymbiotic plasmids. Mol Plant-Microbe Interact 9:535–545

    Article  CAS  Google Scholar 

  • Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy-Hubler F, Galibert F, Kondorosi A, Kondorosi E (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci USA 103:5230–5235

    Article  PubMed  CAS  Google Scholar 

  • Mimmack ML, Hong GF, Johnston AWB (1994) Sequence and regulation of psrA, a gene on the Sym plasmid of Rhizobium leguminosarum biovar phaseoli which inhibits transcription of the psi genes. Microbiology 140:455–461

    Article  PubMed  CAS  Google Scholar 

  • Minic Z, Brown S, De Kouchkovsky Y, Schultze M, Staehelin C (1998) Purification and characterization of a novel chitinase-lysozyme, of another chitinase, both hydrolysing Rhizobium meliloti Nod factors, and of a pathogenesis-related protein from Medicago sativa roots. Biochem J 332:329–335

    PubMed  CAS  Google Scholar 

  • Mitra RM, Long SR (2004) Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis. Plant Physiol 134:595–604

    Article  PubMed  CAS  Google Scholar 

  • Miwa H, Sun J, Oldroyd G, Downie JA (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883–894

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Murphy PJ, Heycke N, Banfalvi Z, Tate ME, de Brujin F, Kondorosi A, Tempe J, Schell J (1987) Genes for the catabolism and synthesis of an opine-like compound in Rhizobium meliloti are closely linked on the Sym plasmid. Proc Natl Acad Sci USA 84:493–497

    Article  PubMed  CAS  Google Scholar 

  • Mutch LA, Young JPW (2004) Diversity and specifity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol Ecol 13:2435–2444

    Article  PubMed  CAS  Google Scholar 

  • Newton WE (2007) Physiology, biochemistry and molecular biology of nitrogen fixation. In: Ferguson BH, SJ NWE (eds) Biology of nitrogen cycle. Elsevier, Amsterdam, pp 109–130

    Chapter  Google Scholar 

  • Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd GED, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 9:351–357

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ovtsyna AO, Schultze M, Tikhonovich IA, Spaink HP, Kondorosi E, Kondorosi A, Staehelin C (2000) Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates. Mol Plant Microbe Interact 13:799–807

    Article  PubMed  CAS  Google Scholar 

  • Palacios R, Newton WE (2005) Genomes and genomics of nitrogen-fixing organisms. Springer, Dordrecht

    Book  Google Scholar 

  • Palmer KM, Young JPW (2000) Higher diversity of Rhizobium leguminosarum biovar viciae populations in arable soils than in grass soils. Appl Environ Microbiol 66:2445–2450

    Article  PubMed  CAS  Google Scholar 

  • Patriarca EJ, Tate R, Iaccarino M (2002) Key role of bacterial NH +4 metabolism in Rhizobium-plant symbiosis. Microbiol Mol Biol Rev 66:203–222

    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 

  • Peoples MB, Herridge DF, Ladha JK (1995a) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:3–28

    Article  CAS  Google Scholar 

  • Peoples MB, Ladha JK, Herridge DF (1995b) Enhancing legume N2 fixation through plant and soil management. Plant Soil 174:83–101

    Article  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 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980

    Article  PubMed  CAS  Google Scholar 

  • Peters NK, Long SR (1988) Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol 88:396–400

    Article  PubMed  CAS  Google Scholar 

  • Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894

    Article  PubMed  CAS  Google Scholar 

  • Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1531

    Article  PubMed  CAS  Google Scholar 

  • Phillips DA, Kapulnik Y (1995) Plant isoflavonoids, pathogens and symbionts. Trends Microbiol 3:58–63

    Article  PubMed  CAS  Google Scholar 

  • Poustini K, Mabood F, Smith DL (2007) Preincubation of Rhizobium leguminosarum bv. phaseoli with jasmonate and genistein signal molecules increases bean (Phaseolus vulgaris L.) nodulation, nitrogen fixation and biomass production. J Agric Sci Technol 9:107–117

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Prithiviraj B, Zhou X, Souleimanov A, Kahn WM, Smith DL (2003) A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants. Planta 21:437–445

    Google Scholar 

  • Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant-Microbe Interact 12:293–318

    Article  PubMed  CAS  Google Scholar 

  • Rangin C, Brunel B, Cleyet-Marel JC, Perrineau MM, Bena G (2008) Effect of Medicago truncatula genetic diversity, rhizobial competition and strain effectiveness on the diversity of a natural Sinorhizobium species community. Appl Environ Microbiol 74:5653–5661

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rivas R, Velazquez E, Willems A, Vizcaino N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. Appl Environ Microbiol 68:5217–5222

    Article  PubMed  CAS  Google Scholar 

  • Robertson BK, Dreyfus B, Alexander M (1995) Ecology of stem-nodulating Rhizobium and Azorhizobium in four vegetation zones of Senegal. Microb Ecol 29:71–81

    Article  Google Scholar 

  • Robleto EA, Kmiecik K, Oplinger ES, Nienhuis J, Triplett EW (1998) Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Appl Environ Microbiol 64:2630–2633

    PubMed  CAS  Google Scholar 

  • Rosas S, Soria R, Correa N, Abdala G (1998) Jasmonic acid stimulates the expression of nod genes in Rhizobium. Plant Mol Biol 38:1161–1168

    Article  PubMed  CAS  Google Scholar 

  • Rossbach S, Kulpa DA, Rossbach U, de Bruijn FJ (1994) Molecular and genetic characterization of the rhizopine catabolism (mocABRC) genes of Rhizobium meliloti L5-30. Mol Gen Genet 245:11–24

    Article  PubMed  CAS  Google Scholar 

  • Ruvkun GB, Ausubel FM (1980) Interspecies homology of nitrogenase genes. Proc Natl Acad Sci USA 77:191–195

    Article  PubMed  CAS  Google Scholar 

  • Sanjuan J, Grob P, Gőttfert M, Hennecke H, Stacey G (1994) NodW is essential for full expression of the common nodulation genes in Bradyrhizobium japonicum. Mol Plant-Microbe Interact 7:364–369

    Article  CAS  Google Scholar 

  • Schlaman HRM, Horvath B, Vijgenboom E, Okker RJH, Lugtenberg BJJ (1991) Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J Bacteriol 173:4277–4287

    PubMed  CAS  Google Scholar 

  • Schlaman HRM, Phillips DA, Kondorosi E (1998) Genetic organization and transcriptional regulation of rhizobial nodulation genes. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 361–368

    Google Scholar 

  • Schmidt J, Röhrig H, John M, Wieneke U, Stacey G, Koncz C, Schell J (1993) Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J 4:651–658

    Article  CAS  Google Scholar 

  • Schwedock J, Long SR (1989) Nucleotide sequence and protein products of two new nodulation genes of Rhizobium meliloti, nodP and nodQ. Mol Plant-Microbe Interact 2:181–194

    Article  PubMed  CAS  Google Scholar 

  • Sharma SB, Signer ER (1990) Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev 4:344–356

    Article  PubMed  CAS  Google Scholar 

  • Silva C, Kan FL, Martinez-Romero E (2007) Population genetic structure of Sinorhizobium meliloti and S. medicae isolated from nodules Medicago spp. in Mexico. FEMS Microbiol Ecol 60:477–489

    Article  PubMed  CAS  Google Scholar 

  • Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixation mutualisms of legume and rhizobia. Integ Comp Biol 42:369–380

    Article  Google Scholar 

  • Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 5(7):1–19

    Google Scholar 

  • Slattery JF, Pearce DJ (2002) Development of elite inoculant strains of Rhizobium in southeastern. In: Herridge D (ed) Inoculants and nitrogen fixation of legumes in Vietnam, Proceedings of a workshop proceedings, ACIAR proceedings 109:86–94

    Google Scholar 

  • Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Critic Rev Microbiol 30:205–240

    Article  CAS  Google Scholar 

  • Souleimanov A, Prithiviraj B, Smith DL (2002) The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn. J Exp Bot 53:1929–1934

    Article  PubMed  CAS  Google Scholar 

  • Souza V, Nguyen TT, Hudson RR, Pinero D, Lenski RE (1992) Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proc Natl Acad Sci USA 89:8389–8393

    Article  PubMed  CAS  Google Scholar 

  • Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol 54:257–288

    Article  PubMed  CAS  Google Scholar 

  • Spaink HP, Bloemberg GV, van Brussel AAN, Lugtenberg BJJ, van der Drift KMGM, Haverkamp J, Thomas-Oates JE (1995) Host specificity of Rhizobium leguminosarum is determined by the hydrophobicity of highly unsaturated fatty acyl moieties of the nodulation factors. Mol Plant-Microbe Interact 8:155–164

    Article  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 unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354:125–130

    Article  PubMed  CAS  Google Scholar 

  • Stokkermans TJ, Ikeshita S, Cohn J, Carlson RW, Stacey G, Ogawa T, Peters NK (1995) Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordial on Glycine soja. Plant Physiol 108:1587–1595

    Article  PubMed  CAS  Google Scholar 

  • Streeter JG (1994) Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Can J Microbiol 40:513–522

    Article  Google Scholar 

  • Streit WR, Joseph CM, Philips DA (1996) Biotin and other water-soluble vitamins are key growth factors for alfalfa root colonization by Rhizobium meliloti 1021. Mol Plant-Microbe Interact 9:330–338

    Article  PubMed  CAS  Google Scholar 

  • Stuurman N, Bras CP, Schlaman HRM, Wijfjes AHM, Bloemberg G, Spaink HP (2000) Use of green fluorescent protein color variants expressed on stable broad-host-range vectors to visualize rhizobia interacting with plants. Mol Plant-Microbe Interact 13:1163–1169

    Article  PubMed  CAS  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci 12:282–285

    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 

  • Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation and nodulation. Plant J 46:961–970

    Article  PubMed  CAS  Google Scholar 

  • Svenning MM, Gudmundsson J, Fagerli IL, Leinonen P (2001) Competition for nodule occupancy between introduced strains of Rhizobium leguminosarum bv. trifolii and its influence on plant production. Ann Bot 88:781–787

    Article  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact 13:637–648

    Article  PubMed  CAS  Google Scholar 

  • Timmers AC, Soupène E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G (2000) Saprophytic intracellular rhizobia in alfalfa nodules. Mol Plant-Microbe Interact 13:1204–121

    Article  PubMed  CAS  Google Scholar 

  • Valverde A, Velázquez E, Fernández-Santos F, Vizcaíno N, Rivas R, Mateos PF, Martínez-Molina E, Igual JM, Willems A (2005) Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989

    Article  PubMed  CAS  Google Scholar 

  • Valverde A, Velázquez E, Gutirrez C, Cervantes E, Ventosa A, Igual JM (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979–1983

    Article  PubMed  CAS  Google Scholar 

  • van Dillewijn P, Soto MJ, Villadas P, Toro N (2001) Construction and environmental release of a Sinorhizobium meliloti strain genetically modified to be more competitive for alfalfa nodulation. Appl Environ Microbiol 67:3860–3865

    Article  PubMed  Google Scholar 

  • Vance C (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  PubMed  CAS  Google Scholar 

  • Vasse J, de Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306

    PubMed  CAS  Google Scholar 

  • Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martínez-Romero E, Werner D (2003) Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol Plant-Microbe Interact 16:159–168

    Article  PubMed  CAS  Google Scholar 

  • Vlassak KM, Vanderleyden J (1997) Factors influencing nodule occupancy by inoculant rhizobia. Crit Rev Plant Sci 16:163–229

    Google Scholar 

  • Wasson AP, Pellerone FI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18:1617–1629

    Article  PubMed  CAS  Google Scholar 

  • Wernegreen JJ, Harding EE, Riley MA (1997) Rhizobium gone native: unexpected plasmid stability of indigenous Rhizobium leguminosarum. Proc Natl Acad Sci USA 94:5483–5488

    Article  PubMed  CAS  Google Scholar 

  • Wernegreen JJ, Riley MA (1999) Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages. Mol Biol Evol 16:98–113

    Article  PubMed  CAS  Google Scholar 

  • White J, Prell J, James EK, Poole P (2007) Nutrient sharing between symbionts. Plant Physiol 144:604–614

    Article  PubMed  CAS  Google Scholar 

  • Wielbo J, Golus J, Marek-Kozaczuk M, Skorupska A (2009) Symbiosis stage-associated alterations in quorum sensing autoinducer molecules biosynthesis in Sinorhizobium meliloti. Plant Soil. doi:10.1007/s11104-009-0166-z

    Google Scholar 

  • Wielbo J, Marek-Kozaczuk M, Kubik-Komar A, Skorupska A (2007) Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness. Can J Microbiol 53:957–967

    Article  PubMed  CAS  Google Scholar 

  • Wielbo J, Marek-Kozaczuk M, Mazur A, Kubik-Komar A, Skorupska A (2010) Genetic and metabolic divergence within a Rhizobium leguminosarum bv. trifolii population recovered from clover nodules. Appl Environ Microbiol doi:10.1128/AEM.00667-10

    PubMed  Google Scholar 

  • Wielbo J, Mazur A, Król J, Marczak M, Kutkowska J, Skorupska A (2004a) Complexity of phenotypes and symbiotic behaviour of Rhizobium leguminosarum biovar trifolii exopolysaccharide mutants. Arch Microbiol 182:331–336

    Article  PubMed  CAS  Google Scholar 

  • Wielbo J, Mazur A, Król J, Marczak M, Skorupska A (2004b) Environmental modulation of the pssTNOP gene expression in Rhizobium leguminosarum bv. trifolii. Can J Microbiol 50:201–211

    Article  PubMed  CAS  Google Scholar 

  • Yahyaoui FE, Küster H, Amor BB, Hohnjec N, Pühler A, Becker A, Gouzy J, Vernié T, Gough C, Niebel A, Godiard L, Gamas P (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136:3159–3176

    Article  PubMed  Google Scholar 

  • Young JP, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34

    Article  PubMed  CAS  Google Scholar 

  • Yuen JPY, Cassini ST, De Oliveira TT, Nagem TJ, Stacey G (1995) Xanthone induction of nod gene expression in Bradyrhizobium japonicum. Symbiosis 19:131–140

    CAS  Google Scholar 

  • Zhang F, Smith DL (1995) Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures. Plant Physiol 108:961–968

    Article  PubMed  CAS  Google Scholar 

  • Zhang F, Smith DL (1996) Inoculation of soybean (Glycine max (L.) Merr.) with genistein-preincubated Bradyrhizobium japonicum or genistein directly applied into soil increases soybean protein and dry matter yield under short season conditions. Plant Soil 179:233–241

    Article  CAS  Google Scholar 

  • Zhang F, Smith DL (2002) Interorganismal signaling in suboptimum environments: the legume–rhizobia symbiosis. Adv Agron 76:125–61

    Article  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 

  • Zuanazzi JAS, Clergeot PH, Quirion JC, Husson HP, Kondorosi A, Ratet P (1998) Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Mol Plant-Microbe Interact 11:784–794

    Article  CAS  Google Scholar 

  • Zurdo-Piñeiro JL, Rivas R, Trujillo ME, Vizcaino N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martínez-Molina E, Velásquez E (2007) Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int J Syst Evol Microbiol 57:784–788

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The research reported in this study was funded in part by a grant of Ministry of Sciences and Higher Education nr N N304 026734. The authors are grateful to Joanna Golus, Jolanta Kutkowska, and Jan Kuske for kindly providing the photographs presented in Fig. 2.1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Skorupska .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag/Wien

About this chapter

Cite this chapter

Skorupska, A., Wielbo, J., Kidaj, D., Marek-Kozaczuk, M. (2010). Enhancing Rhizobium–Legume Symbiosis Using Signaling Factors. 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_2

Download citation

Publish with us

Policies and ethics