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Engineering Nodulation Competitiveness of Rhizobial Bioinoculants in Soils

  • Chapter
Microbes for Legume Improvement

Abstract

In field conditions, inoculated strains of rhizobia are at a survival disadvantage as compared to indigenous strains that are well adapted to local environment. Consequently, nodulation by unwanted strains is a major problem in enhancement of legume growth by rhizobial bio-inoculants. Competitiveness determinants include motility, chemotaxis, cell surface components, ability to use certain substrates, storage polymers, and production of antimicrobial compounds, higher growth rates, and ability to bring about faster infection. More recently, the involvement of other factors such as quorum sensing, the ability to form biofilms, and presence of protein secretion machinery has been shown to be important. Using genomics-based approach, numerous competitiveness genes have been identified. Variation in competitiveness traits among different legume-microsymbionts is becoming apparent. Approaches for the development of competitive bioinoculants by genetic engineering employ the following strategies (a) production of antimetabolites to inhibit nodule occupancy of native rhizobia, (b) interference with the regulation of plant–microbe signaling molecules to ensure efficient nodulation, (c) specific adaptation of the inoculated strain to environmental stresses, and (d) improved nutrition of the inoculant strain for competitive sustenance in soil or rhizosphere including root-derived compounds as well as other soil metabolites such as siderophore iron complexes. Engineering rhizobia for enhanced competitiveness is a challenging aspect of developing effective bioinoculants and ability to utilize heterologous siderophores could provide them with better iron acquisition ability and consequently, rhizosphere stability.

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References

  • Althabegoiti MJ, Lopez-Garcıa SL, Piccinetti C, Mongiardini EJ, Perez-Gimenez J, Quelas JI, Perticari A, Lodeiro AR (2008) Strain selectionfor improvement of Bradyrhizobium japonicum competitiveness for nodulation of soybean. FEMS Microbiol Lett 282:115–123

    Article  PubMed  CAS  Google Scholar 

  • Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C, Capela D, Carrère S, Cruveiller S, Dossat C, Lajus A, Marchetti M, Poinsot V, Rouy Z, Servin B, Saad M, Schenowitz C, Barbe V, Batut J, Médigue C, Masson-Boivin C (2008) Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18:1472–1483

    Article  PubMed  CAS  Google Scholar 

  • Amarger N (2002) Genetically modified bacteria in agriculture. Biochimie 84:1061–1072

    Article  PubMed  CAS  Google Scholar 

  • Ames P, Bergman K (1981) Competitive advantage provided by bacterial motility in the formation of nodules by Rhizobium meliloti. J Bacteriol 148:728–729

    PubMed  CAS  Google Scholar 

  • Ampomah OY, Ayeh EO, Solheim B, Svenning MM (2008a) Host range, symbiotic effectiveness and nodulation competitiveness of some indigenous cowpea bradyrhizobia isolates from the transitional savanna zone of Ghana. Afr J Biotechnol 7:988–996

    CAS  Google Scholar 

  • Ampomah OY, Jensen JB, Bhuvaneswari TV (2008b) Lack of trehalose catabolism in Sinorhizobium species increases their nodulation competitiveness on certain host genotypes. New Phytol 179:495–504

    Article  PubMed  CAS  Google Scholar 

  • Aneja P, Zachertowska A, Charles TC (2005) Comparison of the symbiotic and competition phenotypes of Sinorhizobium meliloti PHB synthesis and degradation pathway mutants. Can J Microbiol 51:599–604

    Article  PubMed  CAS  Google Scholar 

  • Araujo RS, Robleto EA, Handelsman J (1994) A hydrophobic mutant of Rhizobium etli altered in nodulation competitiveness and growth in the rhizosphere. Appl Environ Microbiol 60:1430–1436

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Barbour WM, Hattermann DR, Stacey G (1991) Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl Environ Microbiol 57:2635–2639

    PubMed  CAS  Google Scholar 

  • Barcellos FG, Menna P, Batista JS, Hungria M (2007) Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian savannah soil. Appl Environ Microbiol 73:2635–2643

    Article  PubMed  CAS  Google Scholar 

  • Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770

    Article  CAS  Google Scholar 

  • Battistoni F, Platero R, Noya F, Arias A, Fabiano E (2002) Intracellular Fe content influences nodulation competitiveness of Sinorhizobium meliloti strains as inocula of alfalfa. Soil Biol Biochem 34:593–597

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Benson HP, Boncompagni E, Guerinot ML (2005) An iron uptake operon required for proper nodule development in the Bradyrhizobium japonicum-soybean symbiosis. Mol Plant Microbe Ineract 18:950–959

    Article  CAS  Google Scholar 

  • Bernardelli CE, Luna MF, Galar ML, Boiardi JL (2009) Symbiotic phenotype of a membrane-bound glucose dehydrogenase mutant of Sinorhizobium meliloti. Plant Soil 313:217–225

    Article  CAS  Google Scholar 

  • Bhagwat AA, Tully RE, Keister DL (1991) Isolation and characterization of a competition-defective Bradyrhizobium japonicum mutant. Appl Environ Microbiol 57:3496–3501

    PubMed  CAS  Google Scholar 

  • Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209

    Article  PubMed  CAS  Google Scholar 

  • Bittinger MA, Handelsman J (2000) Identification of genes in the RosR regulon of Rhizobium etli. J Bacteriol 182:1706–1713

    Article  PubMed  CAS  Google Scholar 

  • Bittinger MA, Milner JL, Saville BJ, Handelsman J (1997) rosR, a determinant of nodulation competitiveness in Rhizobium etli. Mol Plant Microbe Interact 10:180–186

    Article  PubMed  CAS  Google Scholar 

  • Bogino P, Banchio E, Bonfiglio C, Giordano W (2008) Competitiveness of a Bradyrhizobium sp. strain in soils containing indigenous Rhizobia. Curr Microbiol 56:66–72

    Article  PubMed  CAS  Google Scholar 

  • Bosworth AH, Williams MK, Albrecht KA, Kwiatkowski R, Beynon J, Hankinson TR, Ronson CW, Cannon F, Wacek TJ, Triplett EW (1994) Alfalfa yield response to inoculation with recombinant strains of Rhizobium meliloti with an extra copy of dctABD and/or modified nifA expression. Appl Environ Microbiol 60:3815–3832

    PubMed  CAS  Google Scholar 

  • Braeken K, Daniels R, Vos K, Fauvart M, Bachaspatimayum D, Vanderleyden J, Michiels J (2007) Genetic determinants of swarming in Rhizobium etli. Microb Ecol 55:54–64

    Article  PubMed  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 69:155–194

    Article  PubMed  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, Garcia de los Santos A, Cervantes L, Palacios R, Romero D (2000) In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons. Plasmid 44:34–43

    Article  PubMed  CAS  Google Scholar 

  • Bromfield ESP, Barran LR, Wheatcroft R (1995) Relative genetic structure of a population of Rhizobium meliloti isolated directly from soil and from nodules of alfalfa (Medicago sativa) and sweet clover (Melilotus alba). Mol Ecol 4:183–188

    Article  Google Scholar 

  • Caetano-Anolles G, Wall LG, De Micheli AT, Macchi EM, Bauer WD, Favelukes G (1988) Role of motility and chemotaxis in efficiency of nodulation by Rhizobium meliloti. Plant Physiol 86:1228–1235

    Article  PubMed  CAS  Google Scholar 

  • Carlton TM, Sullivan JT, Stuart GS, Hutt K, Lamont IL, Ronson CW (2007) Ferrichrome utilization in a mesorhizobial population: microevolution of a three-locus system. Environ Microbiol 9:2923–2932

    Article  PubMed  CAS  Google Scholar 

  • Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30

    Article  CAS  Google Scholar 

  • Cevallos MA, Encarnacion S, Leija A, Mora Y, Mora J (1996) Genetic and physiological characterization of a Rhizobium etli mutant strain unable to synthesize poly-b-hydroxybutyrate. J Bacteriol 178:1646–1654

    PubMed  CAS  Google Scholar 

  • Chen H, Richardson AE, Gartner E, Djordjevic MA, Roughley RJ, Rolfe BG (1991) Construction of an acid-tolerant Rhizobium leguminosarum bv. trifolii strain with enhanced capacity for nitrogen fixation. Appl Environ Microbiol 57:2005–2011

    PubMed  CAS  Google Scholar 

  • Cheng HP, Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180:5183–5191

    PubMed  CAS  Google Scholar 

  • Chuiko NV, Antonyuk TS, Kurdish IK (2002) The chemotactic response of Bradyrhizobium japonicum to various organic componunds. Microbiology 71:391–396

    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 

  • Crespo-Rivas JC, Margaret I, Hidalgo Á, Buendía-Clavería AM, Ollero FJ, López-Baena FJ, del Socorro MP, Rodríguez-Carvajal MA, Soria-Díaz ME, Reguera M, Lloret J, Sumpton DP, Mosely JA, Thomas-Oates JE, van Brussel AAN, Gil-Serrano A, Vinardell JM, Ruiz-Sainz JE (2009) Sinorhizobium fredii HH103 cgs mutants are unable to nodulate determinate- and indeterminate nodule-forming legumes and overproduce an altered EPS. Mol Plant Microbe Interact 22:575–588

    Article  PubMed  CAS  Google Scholar 

  • Cummings SP, Humphry DR, Santos SR, Andrews M, James EK (2006) The potential and pitfalls of exploiting nitrogen fixing bacteria in agricultural soils as a substitute for inorganic fertilizer. Environ Biotechnol 2:1–10

    Google Scholar 

  • D’Antuono AL, Casabuono A, Couto A, Ugalde RA, Lepek VC (2005) Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis. Mol Plant Microbe Interact 18:446–57

    Article  PubMed  CAS  Google Scholar 

  • D’Antuono AL, Ott T, Krusell L, Voroshilova V, Ugalde RA, Udvardi M, Lepek VC (2008) Defects in rhizobial cyclic glucan and lipopolysaccharide synthesis alter legume gene expression during nodule development. Mol Plant Microbe Interact 21:50–60

    Article  PubMed  CAS  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 

  • D’Haeze W, Leoff C, Freshour G, Noel KD, Carlson RW (2007) Rhizobium etli CE3 bacteroid lipopolysaccharides are structurally similar but not identical to those produced by cultured CE3 bacteria. J Biol Chem 282:17101–13

    Article  PubMed  Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422

    Article  PubMed  CAS  Google Scholar 

  • Dashti N, Zhang F, Hynes R, Smith DL (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixations activity by field grown soybean [Glycine max (L) merr.] under short season conditions. Plant Soil 200:205–213

    Article  CAS  Google Scholar 

  • Davies BW, Walker GC (2007) Identification of novel Sinorhizobium meliloti mutants compromised for oxidative stress protection and symbiosis. J Bacteriol 189:2110–2113

    Article  PubMed  CAS  Google Scholar 

  • Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology – a review. Soil Biol Biochem 36:1275–1288

    Article  CAS  Google Scholar 

  • deLyra MCCP, López-Baena FJ, Madinabeitia N, Vinardell JM, Espuny MR, Cubo MT, Bellogín RA, Ruiz-Sainz JE, Ollero FJ (2006) Inactivation of the Sinorhizobium fredii HH103 rhcJ gene abolishes nodulation outer proteins (Nops) secretion and decreases the symbiotic capacity with soybean. Int Microbiol 9:125–133

    CAS  Google Scholar 

  • Denton MD, Coventry DR, Murphy PJ, Howieson JG, Bellotti WD (2002) Competition between inoculant and naturalised Rhizobium leguminosarum bv. trifolii for nodulation of annual clovers in alkaline soils. Aust J Agric Res 53:1019–1026

    Article  CAS  Google Scholar 

  • Denton MW, Reeve WG, Howieson JC, Coventry DR (2003) Competitive abilities of common field isolates and a comercial strain of Rhizobium leguminosarum bv. trifolii for clover nodule occupancy. Soil Biol Biochem 35:1039–1048

    Article  CAS  Google Scholar 

  • Djordjevic MA, Chen HC, Natera S, Noorden GV, Menzel CST, Renard C, Geiger O, Weiller GF (2003) A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation. Mol Plant Microbe Interact 16:508–524

    Article  PubMed  CAS  Google Scholar 

  • Domínguez-Ferreras A, Soto MJ, Pérez-Arnedo R, Olivares J, Sanjuán J (2009) Importance of trehalose biosynthesis for Sinorhizobium meliloti osmotolerance and nodulation of alfalfa roots. J Bacteriol 191:7490–7499

    Article  PubMed  CAS  Google Scholar 

  • Dowling DN, Broughton WJ (1986) Competition for nodulation of legumes. Annu Rev Microbiol 40:131–157

    Article  PubMed  CAS  Google Scholar 

  • Dowling DN, Samrey U, Stanley J, Broughton WJ (1987) Cloning of Rhizobium leguminosarum genes for competitive nodulation blocking on peas. J Bacteriol 169:1345–1348

    PubMed  CAS  Google Scholar 

  • Dunlap J, Minami E, Bhagwat AA, Keister DL, Stacey G (1996) Nodule development induced by mutants of Bradyrhizobium japonicum defective in cyclic B-glucan synthesis. Mol Plant Microbe Interact 9:546–555

    Article  PubMed  CAS  Google Scholar 

  • Duodu S, Bhuvaneswari TV, Stokkermans TJW, Peters NK (1999) A positive role for rhizobitoxine in rhizobium–legume symbiosis. Mol Plant Microbe Interact 12:1082–1089

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Elliott GN, Chou JH, Chen WM, Bloemberg GV, Bontemps C, Martínez-Romero E, Velázquez E, Young JPW, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions Environ. Microbiology 11:762–778

    Google Scholar 

  • Entcheva P, Phillips DA, Streit WR (2002) Functional analysis of Sinorhizobium meliloti genes involved in biotin synthesis and transport. Appl Environ Microbiol 68:2843–2848

    Article  PubMed  CAS  Google Scholar 

  • Faraldo-Gomez JD, Sansom MSP (2003) Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4:105–116

    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 

  • Fry J, Wood M, Poole PS (2001) Investigation of myo-inositol catabolism in Rhizobium leguminosarum bv. viciae and its effect on nodulation competitiveness. Mol Plant Microbe Interact 14:1016–1025

    Article  PubMed  CAS  Google Scholar 

  • Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM (2006) Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 56:195–206

    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 

  • Galbraith MP, Feng SZ, Borneman J, Triplett EW, de Bruijn FJ, Rossbach S (1998) A functional myoinositol catabolism pathway is essential for rhizopine utilization by Sinorhizobium meliloti. Microbiology 144:2915–2924

    Article  PubMed  CAS  Google Scholar 

  • Garg N, Geetanjali (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. Agron Sustain Dev 5:519–531

    Google Scholar 

  • Geetha R, Desai AJ, Archana G (2009) Effect of the expression of Escherichia coli fhuA gene in Rhizobium sp. IC3123 and ST1 in planta: its role in increased nodule occupancy and function in pigeon pea. Appl Soil Ecol 43:185–190

    Article  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 

  • 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, Hernandez-Gonzalez I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramırez MA, Jimenez-Jacinto V, Collado-Vides J, Davila 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 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    Article  PubMed  CAS  Google Scholar 

  • Gordon DM, Ryder MH, Heinrich K, Murphy PJ (1996) An experimental test of the rhizopine concept in Rhizobium meliloti. Appl Environ Microbiol 62:3991–3996

    PubMed  CAS  Google Scholar 

  • Griffitts JS, Carlyon RE, Erickson JH, Moulton JL, Barnett MJ, Toman CJ, Long SR (2008) A Sinorhizobium meliloti osmosensory two-component system required for cyclic glucan export and symbiosis. Mol Microbiol 69:479–490

    Article  PubMed  CAS  Google Scholar 

  • Guillen-Navarro K, Araız G, Garcıa-de los Santos A, Mora Y, Dunn MF (2005) The Rhizobium etli bioMNY operon is involved in biotin transport. FEMS Microbiol Lett 250:209–219

    Article  PubMed  CAS  Google Scholar 

  • Guntli D, Heeb M, Moenne-Loccoz Y, Defago G (1999) Contribution of calystegine catabolic plasmid to competitive colonization of the rhizosphere of calystegine-producing plants by Sinorhizobium meliloti Rm41. Mol Ecol 8:855–863

    Article  CAS  Google Scholar 

  • Hartmann A, Giraud JJ, Catroux G (1998) Genotypic diversity of Sinorhizobium (formerly Rhizobium) meliloti strains isolated directly from a soil and from nodules of alfalfa (Medicago sativa) grown in the same soil. FEMS Microbiol Ecol 25:107–116

    CAS  Google Scholar 

  • Heinrich K, Gordon DM, Ryder MH, Murphy PJ (1999) A rhizopine strain of Sinorhizobium meliloti remains at a competitive nodulation advantage after an extended period in the soil. Soil Biol Biochem 31:1063–1065

    Article  CAS  Google Scholar 

  • Hirsch PR (2004) Release of transgenic bacterial inoculants – rhizobia as a case study. Plant Soil 266:1–10

    Article  CAS  Google Scholar 

  • Howieson JG, O’Hara GW, Carr SJ (2000) Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crops Res 65:107–122

    Article  Google Scholar 

  • Hubber A, Vergunst AC, Sullivan JT, Hooykaas PJJ, Ronson CW (2004) Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol Microbiol 54:561–574

    Article  PubMed  CAS  Google Scholar 

  • Hynes MF, McGregor NF (1990) Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 4:567–574

    Article  PubMed  CAS  Google Scholar 

  • Janczarek M, Skorupska A (2007) The Rhizobium leguminosarum bv. trifolii RosR: transcriptional regulator involved in exopolysaccharide production. Mol Plant Microbe Interact 20:867–881

    Article  PubMed  CAS  Google Scholar 

  • Janczarek M, Jaroszuk-Ścise J, Skorupska A (2009) Multiple copies of rosR and pssA genes enhance exopolysaccharide production, symbiotic competitiveness and clover nodulation in Rhizobium leguminosarum bv. trifolii. Antonie Van Leeuwenhoek 96:471–486

    Article  PubMed  CAS  Google Scholar 

  • Jensen JB, Ampomah OY, Darrah R, Peters NK, Bhuvaneswari TV (2005) Role of trehalose transport and utilization in Sinorhizobium meliloti-alfalfa interactions. Mol Plant Microbe Interact 18:694–702

    Article  PubMed  CAS  Google Scholar 

  • Jiang G, Krishnan AH, Kim YW, Wacek TJ, Krishnan HB (2001) A functional myo-inositol dehydrogenase gene is required for efficient nitrogen fixation and competitiveness of Sinorhizobium fredii USDA191 to nodulate soybean (Glycine max [L.] Merr.). Appl Environ Microbiol 183:2595–2604

    CAS  Google Scholar 

  • Jiménez-Zurdo JI, van Dillewijn P, Soto MJ, de Felipe MR, Olivares J, Toro N (1995) Characterization of a Rhizobium meliloti proline dehydrogenase mutant altered in nodulation efficiency and competitiveness on alfalfa roots. Mol Plant Microbe Interact 8:492–498

    Article  PubMed  Google Scholar 

  • Jiménez-Zurdo JI, García-Rodríguez FM, Toro N (1997) The Rhizobium meliloti putA gene: its role in the establishment of the symbiotic interaction with alfalfa. Mol Microbiol 23:85–93

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci USA 105:704–709

    Article  PubMed  CAS  Google Scholar 

  • Joshi FR, Archana G, Desai AJ (2006) Siderophore cross-utilization amongst rhizospheric bacteria and role of their differential affinities for Fe3+ on growth stimulation under iron limited conditions. Curr Microbiol 53:141–147

    Article  PubMed  CAS  Google Scholar 

  • Joshi FR, Chaudhari A, Joglekar P, Archana G, Desai AJ (2008a) Effect of expression of Bradyrhizobium japonicum 61A152 fegA gene in Mesorhizobium sp, on its competitive survival and nodule occupancy on Arachis hypogea. Appl Soil Ecol 40:338–347

    Article  Google Scholar 

  • Joshi FR, Kholiya S, Archana G, Desai AJ (2008b) Siderophore cross-utilization amongst nodule isolates of the cowpea miscellany group and its effect on plant growth in the presence of antagonistic organisms. Microbiol Res 163:564–570

    Article  PubMed  Google Scholar 

  • Joshi FR, Desai DK, Archana G, Desai AJ (2009) Enhanced survival and nodule occupancy of pigeon pea nodulating Rhizobium sp.ST1 expressing fegA Gene of Bradyrhizobium japonicum 61A152 OnLine. J Biol Sci 9:40–51

    CAS  Google Scholar 

  • Kadouri D, Jurkevitch E, Castro-Sowinski YOS (2005) Ecological and agricultural significance of bacterial polyhydroxyalkanoates. Crit Rev Microbiol 31:55–67

    Article  PubMed  CAS  Google Scholar 

  • Kannenberg EL, Carlson RW (2001) Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol 39:379–391

    Article  PubMed  CAS  Google Scholar 

  • Keller M, Roxlau A, Weng WM, Schmidt M, Quandt J, Niehaus K, Jording D, Arnold W, Puhler A (1995) Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan. Mol Plant Microbe Interact 8:267–277

    Article  PubMed  CAS  Google Scholar 

  • Khan A, Geetha R, Akolkar A, Pandya A, Archana G, Desai AJ (2006) Differential cross-utilization of heterologous siderophores by nodule bacteria of Cajanus cajan and its, possible role in growth under iron-limited conditions. Appl Soil Ecol 34:19–26

    Article  Google Scholar 

  • Knee EM, Gong F, Gao M, Teplitski M, Jones AR, 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 

  • Kunin V, Goldovsky L, Darzentas N, Ouzounis CA (2005) The net of life: reconstructing the microbial phylogenetic network. Genome Res 15:954–959

    Article  PubMed  CAS  Google Scholar 

  • Lagares A, Caetano-Anollés G, Niehaus K, Lorenzen J, Ljunggren HD, Pühler A, Favelukes G (1992) A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. J Bacteriol 174:5941–5952

    PubMed  CAS  Google Scholar 

  • Lakshman K, Shamala TR (2003) Enhanced biosynthesis of polyhydroxyalkanoates in a mutant strain of Rhizobium meliloti. Biotechnol Lett 25:115–119

    Article  PubMed  CAS  Google Scholar 

  • Lamrabet Y, Bellogin RA, Cubo T, Espuny R, Gil A, Krishnan HB, Megias M, Ollero FJ, Pueppke SG, Ruiz-Sainz JE, Spaink HP, Tejero-Mateo P, Thomas-Oates J, Vinardell JM (1999) Mutation in GDP-fucose synthesis genes of Sinorhizobium fredii alters Nod factors and significantly decreases competitiveness to nodulate soybeans. Mol Plant Microbe Interact 12:207–217

    Article  PubMed  CAS  Google Scholar 

  • Law IJ, Botha WF, Majaule UC, Phalane FL (2007) Symbiotic and genomic diversity of ‘cowpea’ bradyrhizobia from soils in Botswana and South Africa. Biol Fertil Soils 43:653–663

    Article  Google Scholar 

  • Leigh JA, Signer ER, Walker GC (1985) Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci USA 82:6231–6235

    Article  PubMed  CAS  Google Scholar 

  • Lepek V, D’Antuono A (2005) Bacterial surface polysaccharides and their role in legume–rhizobium symbiosis. Lotus Newsl 35:93–105

    Google Scholar 

  • Leung K, Yap K, Dashti N, Bottomley PJ (1994) Serological and ecological characteristics of a nodule-dominant serotype from an indigenous soil population of Rhizobium leguminosarum bv. trifolii. Appl Environ Microbiol 60:408–415

    PubMed  CAS  Google Scholar 

  • Ligero F, Lluch C, Olivares J (1986) Evolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti. Plant Physiol 125:361–365

    Article  CAS  Google Scholar 

  • Lodwig EM, Leonard M, Marroqui S, Wheeler TR, Findlay K, Downie JA, Poole PS (2005) Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids. Mol Plant Microbe Interact 18:67–74

    Article  PubMed  CAS  Google Scholar 

  • Lohar DP, Sharopova N, Endre G, Penuela S, Samac D, Town C, Silverstein KA, Vanden Bosch KA (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 140:221–234

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Garcia SL, Vazquez TE, Favelukes G, Lodeiro AR (2002) Rhizobial position as a main determinant in the problem of competition for nodulation in soybean. Environ Microbiol 4:216–224

    Article  PubMed  Google Scholar 

  • López-García SL, Perticari A, Piccinetti C, Ventimiglia L, Arias N, De Battista JJ, Althabegoiti MJ, Mongiardini EJ, Pérez-Giménez J, Quelas JI, Lodeiro AR (2009) In-furrow inoculation and selection for higher motility enhances the efficacy of Bradyrhizobium japonicum nodulation. Agron J 101:357–363

    Article  CAS  Google Scholar 

  • Ma W, Guinel FC, Glick BR (2003a) Rhizobium leguminosarum bv. viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69:4396–4402

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003b) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Antonie Leeuwenhoek 83:285–291

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Charles TC, Glick BR (2004) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891–5897

    Article  PubMed  CAS  Google Scholar 

  • Machado D, Krishnan HB (2003) nodD alleles of Sinorhizobium fredii USDA191 differentially influence soybean nodulation, nodC expression, and production of exopolysaccharides. Curr Microbiol 47:134–137

    Article  PubMed  CAS  Google Scholar 

  • MacLean AM, Finan TM, Sadowsky MJ (2007) Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 144:615–622

    Article  PubMed  CAS  Google Scholar 

  • Malmcrona-Friberg K, Goodman A, Kjelleberg S (1990) Chemotactic responses of marine Vibrio sp. strain S14 (CCUG 15956) to low-molecular weight substances under starvation and recovery conditions. Appl Environ Microbiol 56:3699–3704

    PubMed  CAS  Google Scholar 

  • Marroquì S, Zorreguieta A, Santamarìa C, Temprano F, Soberòn M, Megìas M, Downie AJ (2001) Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. J Bacteriol 183:854–864

    Article  PubMed  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 

  • Mathis R, Gijsegem FV, Rycke RD, D'Haeze W, Maelsaeke EV, Anthonio E, Montagu MV, Holsters M, Vereecke D (2005) Lipopolysaccharides as a communication signal for progression of legume endosymbiosis. Proc Natl Acad Sci USA 102:2655–2660

    Article  PubMed  CAS  Google Scholar 

  • McIntyre HJ, Davies H, Hore TA, Miller SH, Dufour J-P, Ronson CW (2007) Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl Environ Microbiol 73:3984–3992

    Article  PubMed  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 

  • Mongiardini EJ, Pérez-Giménez J, Althabegoiti MJ, Covelli J, Quelas JI, López-García SL, Lodeiro AR (2009) Overproduction of the rhizobial adhesin RapA1 increases competitiveness for nodulation. Soil Biol Biochem 41:2017–2020

    Article  CAS  Google Scholar 

  • Mrabet M, Mnasri B, Romdhane SB, Laguerre G, Aouani ME, Mhamdi R (2006) Agrobacterium strains isolated from root nodules of common bean specifically reduce nodulation by Rhizobium gallicum. FEMS Microbiol Ecol 56:304–309

    Article  PubMed  CAS  Google Scholar 

  • Murphy PJ, Wexler M, Ggzemski W, Rao JP, Gordon D (1995) Rhizopines: their role in symbiosis and competition. Soil Biol Biochem 27:525–529

    Article  CAS  Google Scholar 

  • Nandasena KG, O'Hara GW, Tiwari RP, Sezmis E, Howieson JG (2007) In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 9:2496–2511

    Article  PubMed  CAS  Google Scholar 

  • Nirmala J, Gaur YD, Lawrence PK (2001) Isolation and characterization of a bacteriocin produced by Cicer-Rhizobium World. J Microbiol Biotechnol 17:795–799

    Article  CAS  Google Scholar 

  • Nogales J, Campos R, BenAbdelkhalek H, Olivares J, Lluch C, Sanjuan J (2002) Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol Plant Microbe Interact 15:225–232

    Article  PubMed  CAS  Google Scholar 

  • Nukui N, Ezura H, Yuhashi K, Yasuta T, Minamisawa K (2000) Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant Cell Physiol 41:893–897

    Article  PubMed  CAS  Google Scholar 

  • Okazaki S, Yuhashi K, Minamisawa K (2003) Quantitative and time course evaluation of nodulation competitiveness of rhizobitoxine-producing Bradyrhizobium elkanii. FEMS Microbiol Ecol 45:155–160

    Article  PubMed  CAS  Google Scholar 

  • Okazaki S, Nukui N, Sugawara M, Minamisawa K (2004) Rhizobial strategies to enhance symbiotic interactions: rhizobitoxine and 1-aminocyclopropane-1-carboxylate deaminase. Microbes Environ 19:99–111

    Article  Google Scholar 

  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd GED, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835–1849

    PubMed  CAS  Google Scholar 

  • Onishchuk OP, Kurchak ON, Sharypova LA, Provorov NA, Simarov BV (2001) Analysis of different types of competitive capacity in the Alfalfa Rhizobia (Sinorhizobium meliloti) Tn5 mutants. Russ J Genet 37:1266–1271

    Article  CAS  Google Scholar 

  • Oono R, Denison RF, Kiers ET (2009) Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytol 183:967–979

    Article  PubMed  Google Scholar 

  • Oresnik IJ, Pacarynuk LA, O’Brien SAP, Yost CK, Hynes MF (1998) Plasmid-encoded catabolic genes in Rhizobium leguminosarum bv. trifolii: evidence for a plant-inducible rhamnose locus involved in competition for nodulation. Mol Plant Microbe Interact 12:1175–1185

    Article  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 65:2833–2940

    PubMed  CAS  Google Scholar 

  • Pandya S, Iyer P, Gaitonde V, Parekh T, Desai A (1999) Chemotaxis of Rhizobium sp. S2 towards Cajanus cajan root exudate its major components. Curr Microbiol 4:205–209

    Article  Google Scholar 

  • Parniske M, Kosch K, Werner D, Müller P (1993) ExoB mutants of Bradyrhizobium japonicum with reduced competitiveness for nodulation of Glycine max. Mol Plant Microbe Interact 6:99–106

    Article  CAS  Google Scholar 

  • Patankar AV, Gonzalez JE (2009) An Orphan LuxR Homolog of Sinorhizobium meliloti affects stress adaptation and competition for nodulation. Appl Environ Microbiol 75:946–955

    Article  PubMed  CAS  Google Scholar 

  • Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527–530

    Article  PubMed  CAS  Google Scholar 

  • Peralta H, Mora Y, Salazar E, Encarnacion S, Palacios R, Mora J (2004) Engineering the nifH promoter region and abolishing Poly-β-Hydroxybutyrate accumulation in Rhizobium etli enhance nitrogen fixation in symbiosis with Phaseolus vulgaris. Appl Environ Microbiol 70:3272–3281

    Article  PubMed  CAS  Google Scholar 

  • Perez-Giménez J, Mongiardini EJ, Althabegoiti MJ, Covelli J, Quelas JI, Lopez-Garcıa SL, Lodeiro AR (2009) Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int J Microbiol. doi:10.1155/2009/719367

    PubMed  Google Scholar 

  • Phillips DA, Sande ES, Vriezen AC, de Bruijn FJ, Le Rudulier D, Joseph CM (1998) A new genetic locus in Sinorhizobium meliloti is involved in stachydrine utilization. Appl Environ Microbiol 64:3954–3960

    PubMed  CAS  Google Scholar 

  • Pobigaylo N, Wetter D, Szymczak S, Schiller U, Kurtz S, Meyer F, Nattkemper TW, Becker A (2006) Construction of a large signature-tagged Mini-Tn5 transposon library and its application to mutagenesis of Sinorhizobium meliloti. Appl Environ Microbiol 72:4329–4337

    Article  PubMed  CAS  Google Scholar 

  • Pobigaylo N, Szymczak S, Nattkemper TW, Becker A (2008) Identification of genes relevant to symbiosis and competitiveness in Sinorhizobium meliloti using signature-tagged mutants. Mol Plant Microbe Interact 21:219–231

    Article  PubMed  CAS  Google Scholar 

  • Povolo S, Casella S (2004) Poly-3-hydroxybutyrate has an important role for the survival of Rhizobium tropici under starvation. Ann Microbiol 54:307–316

    CAS  Google Scholar 

  • Povolo S, Casella S (2009) Effect of poly-3-hydroxybutyrate synthase mutation on the metabolism of Ensifer (formerly Sinorhizobium) meliloti. J Basic Microbiol 49:178–186

    Article  PubMed  CAS  Google Scholar 

  • Powell PE, Cline GR, Reid CPP, Szaniszlo PJ (1980) Occurrence of hydroxamate siderophore iron chelators in soil. Nature 287:833–834

    Article  CAS  Google Scholar 

  • Poysti NJ, Loewen EDM, Wang Z, Oresnik IJ (2007) Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism. Microbiology 153:727–736

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rajendran G, Mistry S, Desai AJ, Archana G (2007) Functional expression of Escherichia coli fhuA gene in Rhizobium spp. of Cajanus cajan provides growth advantage in presence of Fe+3: ferrichrome as iron source. Arch Microbiol 187:257–264

    Article  PubMed  CAS  Google Scholar 

  • Ratcliff BC, Denison RF (2009) Rhizobitoxine producers gain more poly-3-hydroxybutyrate in symbiosis than do competing rhizobia, but reduce plant growth. ISME J 3:870–872

    Article  PubMed  CAS  Google Scholar 

  • Ratcliff WC, Kadam SV, Denison RF (2008) Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiol Ecol 65:391–399

    Article  PubMed  CAS  Google Scholar 

  • Riccillo PM, Muglia CI, de Bruijn FJ, Roe AJ, Booth IR, Aguilar MO (2000) Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J Bacteriol 182:1748–1753

    Article  PubMed  CAS  Google Scholar 

  • Rinaudi L, Fujishige NA, Hirsch AM, Banchio E, Zorreguieta A, Giordano W (2006) Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. Res Microbiol 157:867–875

    Article  PubMed  CAS  Google Scholar 

  • Robleto EA, Scupham AJ, Triplett EW (1997) Trifolitoxin production in Rhizobium etli strain CE3 increases competitiveness for rhizosphere growth and root nodulation of Phaseolus vulgaris in soil. Mol Plant Microbe Interact 10:228–233

    Article  Google Scholar 

  • Robleto EA, Borneman J, Triplett EW (1998) Effects of bacterial antibiotic production on rhizosphere microbial communities from a culture independent perspective. Appl Environ Microbiol 64:5020–5022

    PubMed  CAS  Google Scholar 

  • Rojas-Jiménez K, Sohlenkamp C, Geiger O, Werner D, Martínez-Romero E, Vinuesa P (2005) A putative ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Mol Plant Microbe Interact 18:1175–1185

    Article  PubMed  CAS  Google Scholar 

  • Roy H (2009) Tuning the properties of the bacterial membrane with aminoacylated phosphatidylglycerol. IUBMB Life 61:940–953

    Article  PubMed  CAS  Google Scholar 

  • Saikia SP, Jain V (2007) Biological nitrogen fixation with non-legumes: an achievable target or a dogma? Curr Sci 92:317–322

    CAS  Google Scholar 

  • Sanchez C, Iannino F, Deakin WJ, Ugalde RA, Lepek VC (2009) Characterization of the Mesorhizobium loti MAFF303099 type-three protein secretion system. Mol Plant Microbe Interact 22:519–528

    Article  PubMed  CAS  Google Scholar 

  • Sarma AD, Emerich (2005) Global protein expression pattern of Bradyrhizobium japonicum bacteroids: a prelude to functional proteomics. Proteomics 5:4170–4184

    Article  PubMed  CAS  Google Scholar 

  • Savka MA, Dessaux Y, Oger P, Rossbach S (2002) Engineering bacterial competitiveness and persistence in the phytosphere. Mol Plant Microbe Interact 15:866–874

    Article  PubMed  CAS  Google Scholar 

  • Scheidle H, Gross A, Niehaus K (2005) The lipid A substructure of the Sinorhizobium meliloti lipopolysaccharides is sufficient to suppress the oxidative burst in host plants. New Phytol 165:559–565

    Article  PubMed  CAS  Google Scholar 

  • Scupham AJ, Bosworth AH, Ellis WR, Wacek TJ, Albrecht KA, Triplett EW (1996) Inoculation with Sinorhizobium meliloti RMBPC-2 increases alfalfa yield compared with inoculation with a nonengineered wild-type strain. Appl Environ Microbiol 62:4260–4262

    PubMed  CAS  Google Scholar 

  • Seneviratne G, Jayasinghearachchi HS (2003) Mycelial colonization by bradyrhizobia and azorhizobia. J Biosci 28:243–247

    Article  PubMed  Google Scholar 

  • Sessitsch A, Hardarson G, de Vos WM, Wilson KJ (1998) Use of marker genes in competition studies of Rhizobium. Plant Soil 204:35–45

    Article  CAS  Google Scholar 

  • Sessitsch A, Howieson JG, Perret X, Antoun H, Martínez-Romero E (2002) Advances in rhizobium research. Crit Rev Plant Sci 21:323–378

    Article  CAS  Google Scholar 

  • Shimoda Y, Mitsui H, Kamimatsuse H, Minamisawa K, Nishiyama E, Ohtsubo Y, Nagata Y, Tsuda M, Shinpo S, Watanabe A, Kohara M, Yamada M, Nakamura Y, Tabata S, Sato S (2008) Construction of signature-tagged mutant library in Mesorhizobium loti as a powerful tool for functional genomics. DNA Res 15:297–308

    Article  PubMed  CAS  Google Scholar 

  • Simms EL, Bever JD (1998) Evolutionary dynamics of rhizopine within spatially structured rhizobium populations. Proc R Soc Lond B 265:1713–1719

    Article  Google Scholar 

  • Simms EL, Taylor DL, Povich J, Shefferson RP, Sachs JL, Urbina M, Tausczik Y (2006) An empirical test of partner choice mechanisms in a wild legume–rhizobium interaction. Proc R Soc Lond B 273:77–81

    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. doi:10.1186/1475-2859-5-7

    Article  PubMed  CAS  Google Scholar 

  • Slattery JF, Pearce DJ, Slattery WJ (2004) Effects of resident rhizobial communities and soil type on the effective nodulation of pulse legumes. Soil Biol Biochem 36:1339–1346

    Article  CAS  Google Scholar 

  • Sohlenkamp C, Galindo-Lagunas KA, Guan Z, Vinuesa P, Robinson S, Thomas-Oates J et al (2007) The lipid lysyl-phosphatidylglycerol is present in membranes of Rhizobium tropici CIAT899 and confers increased resistance to polymyxin B under acidic growth conditions. Mol Plant Microbe Interact 20:1421–1430

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sprent JI (2008) 60 Ma of legume nodulation. What’s new? What’s changing? J Exp Bot 59:1081–1084

    Article  PubMed  CAS  Google Scholar 

  • Spriggs AC, Dakora FD (2009) Assessing the suitability of antibiotic resistance markers and the indirect ELISA technique for studying the competitive ability of selected Cyclopia Vent. rhizobia under glasshouse and field conditions in South Africa. BMC Microbiol 9:142

    Article  PubMed  CAS  Google Scholar 

  • Sridevi M, Mallaiah KV (2008) Production of bacteriocins by root nodule bacteria. Int J Agric Res 3:161–165

    Article  CAS  Google Scholar 

  • Steele TT, Fowler CW, Griffitts JS (2009) Control of gluconate utilization in Sinorhizobium meliloti. J Bacteriol 191:1355–1358

    Article  PubMed  CAS  Google Scholar 

  • Stiens M, Schneiker S, Keller M, Kuhn S, Puhler A, Schluter A (2006) Sequence analysis of the 144-Kilobase accessory plasmid pSmeSM11a, isolated from a dominant Sinorhizobium meliloti strain identified during a long-term field release experiment. Appl Environ Microbiol 72:3662–3672

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Streit WR, Joseph CM, Phillips DA (1996) Biotin and other water-soluble vitamins are key growth factors for alfalfa rhizosphere colonization by Rhizobium meliloti, 1021. Mol Plant Microbe Interact 5:331–338

    Google Scholar 

  • Streit WR, Schmitz RA, Perret X, Staehelin C, Deakin WJ, Raasch C, Liesegang H, Broughton WJ (2004) An evolutionary hot spot: the pNGR234b replicon of Rhizobium sp. strain NGR234. J Bacteriol 186:535–542

    Article  PubMed  CAS  Google Scholar 

  • Strijdom BW (1998) South African studies on biological nitrogen fixing systems and the exploitation of the nodule bacterium legume symbiosis. S Afr J Sci 94:11–23

    CAS  Google Scholar 

  • Suárez R, Wong A, Ramírez M, Barraza A, del Carmen OM, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in Rhizobia. Mol Plant Microbe Interact 21:958–966

    Article  PubMed  CAS  Google Scholar 

  • Sugawara M, Okazaki S, Nukui N, Ezura H, Mitsui H, Minamisawa K (2006) Rhizobitoxine modulates plant–microbe interactions by ethylene inhibition. Biotechnol Adv 24:382–388

    Article  PubMed  CAS  Google Scholar 

  • Theunis M, Kobayashi H, Broughton WJ, Prinsen E (2004) Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Mol Plant Microbe Interact 17:1153–1161

    Article  PubMed  CAS  Google Scholar 

  • Thies JE, Singleton PW, Bohlool BB (1991) Influence of the size of indigenous rhizobial populations on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Appl Environ Microbiol 57:19–28

    PubMed  CAS  Google Scholar 

  • Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2007) Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 22:120–126

    Article  PubMed  Google Scholar 

  • Tikhonovich IA, Provorov NA (2007) Cooperation of plants and microorganisms: getting closer to the genetic construction of sustainable agro-systems. Biotechnol J 2:833–848

    Article  PubMed  CAS  Google Scholar 

  • Toro N (1996) Nodulation competitiveness in the Rhizobium–legume symbiosis. World J Microbiol Biotechnol 12:157–162

    Article  Google Scholar 

  • Trainer M, Charles T (2006) The role of PHB metabolism in the symbiosis of rhizobia with legumes. Appl Microbiol Biotechnol 71:377–386

    Article  PubMed  CAS  Google Scholar 

  • Triplett EW, Barta TM (1987) Trifolitoxin production and nodulation are necessary for the expression of superior nodulation competitiveness by Rhizobium leguminosarum bv. trifolii strain T24 on clover. Plant Physiol 85:335–342

    Article  PubMed  CAS  Google Scholar 

  • Triplett EW, Sadowsky MJ (1992) Genetics of competition for nodulation of legumes. Annu Rev Microbiol 46:399–428

    Article  PubMed  CAS  Google Scholar 

  • Van Berkum P, Eardly BD (1998) Molecular evolutionary systematics of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae, molecular biology of model plant-associated bacteria. Kluwer Academic Publishers, Dordrecht, pp 1–24

    Google Scholar 

  • Van Dillewijn P, Soto MJ, Villadas PJ, 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 

  • Vasse J, Billy F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J 4:555–566

    Article  Google Scholar 

  • Velasquez E, Mateos PF, Velasco N, Santos F, Burgos PA, Villadas P, Toro N, Martinez-Molina E (1999) Symbiotic characteristics and selection of autochthonous strains of Sinorhizobium meliloti populations in different soils. Soil Biol Biochem 31:1039–1047

    Article  Google Scholar 

  • Vences-Guzmán MA, Geiger O, Sohlenkamp C (2008) Sinorhizobium meliloti mutants deficient in phosphatidylserine decarboxylase accumulate phosphatidylserine and are strongly affected during symbiosis with alfalfa. J Bacteriol 190:6846–6856

    Article  PubMed  CAS  Google Scholar 

  • Venter AP, Twelker S, Oresnik IJ, Hynes MF (2001) Analysis of the genetic region encoding a novel rhizobiocin from Rhizobium leguminosarum bv. viciae strain 306 Can. J Microbiol 47:495–502

    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 16:159–68

    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 

  • Wadisirisuk P, Danso SKA, Hardarson G, Bowen GD (1989) Influence of Bradyrhizobium japonicum location and movement on nodulation and nitrogen fixation in soyabean. Appl Environ Microbiol 55:1711–1716

    PubMed  CAS  Google Scholar 

  • Wang C, Saldanha M, Sheng X, Shelswell KJ, Walsh KT, Sobral BWS, Charles TC (2007) Roles of poly-3-hydroxybutyrate (PHB) and glycogen in symbiosis of Sinorhizobium meliloti with Medicago sp. Microbiology 153:388–398

    Article  PubMed  CAS  Google Scholar 

  • Wei X, Bauer WD (1998) Starvation induced changes in motility, chemotaxis, and flagellation of Rhizobium meliloti. Appl Environ Microbiol 64:1708–1714

    PubMed  CAS  Google Scholar 

  • Wexler M, Gordon D, Murphy PJ (1995) The distribution of inositol rhizopine genes in Rhizobium populations. Soil Biol Biochem 27:531–537

    Article  CAS  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 

  • Williams A, Wilkinson A, Krehenbrink M, Russo DM, Zorreguieta A, Downie JA (2008) Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. J Bacteriol 190:4706–4715

    Article  PubMed  CAS  Google Scholar 

  • Willis LB, Walker GC (1998) The phbC (poly-hydroxybutyrate synthase) gene of Rhizobium (Sinorhizobium) meliloti and characterization of phbC mutants. Can J Microbiol 44:554–569

    PubMed  CAS  Google Scholar 

  • Wrangstadh M, Szewzyk U, O’stling J, Kjelleberg S (1990) Starvation specific formation of a peripheral exopolysaccharide by a marine Pseudomonas sp, strain S9. Appl Environ Microbiol 56:2065–2072

    PubMed  CAS  Google Scholar 

  • Xie B, Chen D, Cheng G, Ying Z, Xie F, Li Y, Zhou J (2009) Effects of the purL gene expression level on the competitive nodulation ability of Sinorhizobium fredii. Curr Microbiol 59:193–198

    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 

  • Yost CK, Rath AM, Noel TC, Hynes MF (2006) Characterization of genes involved in erythritol catabolism in Rhizobium leguminosarum bv. viciae. Microbiology 152:2061–2074

    Article  PubMed  CAS  Google Scholar 

  • You Z, Gao X, Ho MM, Borthakur D (1998) A stomatin-like protein encoded by the slp gene of Rhizobium etli is required for nodulation competitiveness on the common bean. Microbiology 144:2619–2627

    Article  PubMed  CAS  Google Scholar 

  • Yuhashi KI, Ichikawa N, Ezura H, Akao S, Minakawa Y, Nukui N, Yasuta T, Minamisawa K (2000) Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Appl Environ Microbiol 66:2658–2663

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

I would like to thank students from our group whose work has been cited in this chapter. I also express gratitude to Retd. Prof. A. J. Desai, M. S. University of Baroda and funding agencies DBT, India and UGC, India for financial support of the work carried out in our laboratory.

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Correspondence to Gattupalli Archana .

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Archana, G. (2010). Engineering Nodulation Competitiveness of Rhizobial Bioinoculants in Soils. 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_8

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