Skip to main content

Nitrogen Fixing Symbiosis in a Sustainable Agriculture

  • Chapter
  • First Online:
Plant, Soil and Microbes

Abstract

In most agricultural systems, the primary source of biologically fixed N2 takes place through the symbiotic interactions of legumes and rhizobia bacteria. As a collective name, rhizobia cover several genera in the alpha- and beta-Proteobacteria. As a rule, all species of rhizobia form nodules with a range of hosts, determined by their nodulation genes. Nodulation and N2 fixation in these symbioses need that host and microorganisms are compatible, and also that the soil environment is appropriate for the exchange of signals that precede infection. Thus, soil abiotic factors, such as pH, temperature, salinity, and heavy metals, are also critical in the ecology of rhizobia. Besides nitrogen fixation, rhizobia may also benefit plants by other processes, being naturally associated with nonlegume plants and affecting positively their growth through one or several mechanisms independent of symbiotic nitrogen fixation. In this chapter, the focal point is related with some aspects of the Rhizobium-legume symbiosis taking into account that the improvement in molecular biology methods contributed significantly to a major advance in the knowledge of rhizobial diversity. We highlight the importance of certain abiotic stress conditions and the emerging knowledge of the potential of rhizobia as plant growth-promoting bacteria. Special emphasis is given to legumes in natural and sown pasture, namely a particular case on the Mediterranean area exemplifying a long-term sustainable agrosilvopastoral ecosystem.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akhtar MS, Shakeel U, Siddiqui ZA (2010) Biocontrol of Fusarium wilt by Bacillus pumilus, Pseudomonas alcaligenes and Rhizobium sp. on lentil. Turk J Biol 34:1–7

    Google Scholar 

  • Akhtar MS, Siddiqui ZA (2008) Biocontrol of a root-rot disease complex of chickpea by Glomus intraradices, Rhizobium sp. and Pseudomonas striata. Crop Prot 27:410–417

    Article  Google Scholar 

  • Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alikhani HA, Saleh-Rastin N, Antoun H (2006) Phosphate solubilization activity of rhizobia native to Iranian soils. Plant Soil 287:35–41

    Article  CAS  Google Scholar 

  • Andrade DS, Murphy PJ, Giller KE (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67

    Article  CAS  Google Scholar 

  • Antoun H, Prévost D (2006) Ecology of plant growth promoting rhizobacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 1–38

    Chapter  Google Scholar 

  • Arayankoon T, Schomberg HH, Weaver RW (1990) Nodulation and N2 fixation of guar at high root temperature. Plant Soil 126:209–213

    Article  Google Scholar 

  • Ardley JK, Parker MA, de Meyer SE, Trengove RD, O’Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Willems A, Howieson JG (2012) Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are alphaproteobacterial root-nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol 62:2579–2588

    Article  CAS  PubMed  Google Scholar 

  • Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore-producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677

    Google Scholar 

  • Arrese-Igor C, González EM, Marino D, Ladrera R, Larrainzar E, Gil-Quintana E (2011) Physiological response of legumes nodules to drought. Plant Stress 5:24–31

    Google Scholar 

  • Ayalew AM (2011) Factors affecting adaptation of improved haricot bean varieties and associated agronomic practices in Dale woreda, Snnprs. M.Sc. thesis. Hawassa University, Hawassa, Ethiopia

    Google Scholar 

  • Bala A, Murphy P, Giller KE (2002) Occurrence and genetic diversity of rhizobia nodulating Sesbania sesban in African soils. Soil Biol Biochem 34:1759–1768

    Article  CAS  Google Scholar 

  • Bala A, Murphy PJ, Giller KE (2003) Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Mol Ecol 12:917–930

    Article  CAS  PubMed  Google Scholar 

  • Baldock JA, Ballard RA (2004) Fixed nitrogen in sustainable farming systems: a symposium examining factors influencing the extent of biological nitrogen fixation and its role in southern Australian agricultural systems. Setting the scene. Soil Biol Biochem 36:1191–1193

    Article  CAS  Google Scholar 

  • Barcellos FG, Menna P, da Silva 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardain SD, Huang H-C, Pinto J, Amundsen EJ, Erickson RS (2004) Biological control of Phytium damping-off of pea and sugar beet by Rhizobium leguminosarum bv. viciae. Can J Bot 82:291–296

    Article  Google Scholar 

  • Bautista VV, Monsalud RG, Yokota A (2010) Devosia yakushimensis sp. nov., isolated from root nodules of Pueraria lobata (Willd.) Ohwi. Int J Syst Evol Microbiol 60:627–632

    Article  CAS  PubMed  Google Scholar 

  • Bell CJ, Dixon RA, Farmer AD, Flores R, Inman J, Gonzales RA, Harrison MJ, Paiva NL, Scott AD, Weller JW, May GD (2001) The Medicago genome initiative: a model legume database. Nucleic Acids Res 29:114–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell W, Edwards DG, Asher CJ (1989) External calcium requirements for growth and nodulation of six tropical food legumes grown in flowing solution culture. Aust J Agric Res 40:85–96

    Article  Google Scholar 

  • Beynon JL, Josey DP (1980) Demonstration of heterogeneity in a natural population of Rhizobium phaseoli using variation in intrinsic antibiotic resistance. J Gen Microbiol 118:437–442

    Google Scholar 

  • Bhagwat AA, Apte SK (1989) Comparative analysis of proteins induced by heat shock, salinity and osmotic stress in the nitrogen-fixing Cyanobacterium anabaena-sp strain L-31. J Bacteriol 171:5187–5189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bohlool BB, Schmidt EL (1980) The immunofluorescence approach in microbial ecology. In: Alexander M (ed) Advances in microbial ecology. Springer, Berlin, pp 203–241

    Chapter  Google Scholar 

  • Bordeleau LM, Prevost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125

    Article  CAS  Google Scholar 

  • Boundy-Mills KL, Kosslack RM, Tully RE, Pueppke SG, Lohrke SM, Sadowsky MJ (1994) Induction of the Rhizobium fredii nod box-independent nodulation gene nolJ requires a functional nodD1 gene. Mol Plant Microbe Interact 7:305–308

    Article  CAS  Google Scholar 

  • Brígido C, Alexandre A, Oliveira S (2012) Transcriptional analysis of major chaperone genes in salt-tolerant and salt-sensitive mesorhizobia. Microbiol Res 167:623–629

    Article  PubMed  CAS  Google Scholar 

  • Brockwell J, Pilka A, Holliday RA (1991) Soil pH is the major determinant of the numbers of naturally-occurring Rhizobium meliloti in non-cultivated soils in New South Wales. Aust J Exp Agric 31:211–219

    Article  Google Scholar 

  • Bromfield ESP, Behara AMP, Singh RS, Barran LR (1998) Genetic variation in local populations of Sinorhizobium meliloti. Soil Biol Biochem 30:1707–1716

    Article  CAS  Google Scholar 

  • Bromfield ESP, Sinha IB, Wolynetz MS (1986) Influence of location, host cultivar, and inoculation on the composition of naturalized populations in Rhizobium meliloti in Medicago sativa nodules. Appl Environ Microbiol 51:1077–1084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182:5641–5652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruins MR, Kapll S, Oetme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207

    Article  CAS  PubMed  Google Scholar 

  • Burns RC, Hardy RWF (1975) Nitrogen fixation in bacteria and higher plants, vol 21, Molecular biology, biochemistry and biophysics. Springer, Berlin

    Google Scholar 

  • Caballero-Mellado J, Martínez-Romero E (1999) Soil fertilization limits the genetic diversity of Rhizobium in bean nodules. Symbiosis 26:111–121

    Google Scholar 

  • Camacho M, Santamaria C, Temprano F, Rodriguez-Navarro DN, Daza A, Espuny R, Bellogín R, Ollero FJ, de Lyra MCCP, Buendía-Clavería A, Zhou J, Li FD, Mateos C, Velázquez E, Vinardell JM, Ruiz-Sainz JE (2002) Soils of the Chinese Hubei province show a very high diversity of Sinorhizobium fredii in strains. Syst Appl Microbiol 25:592–602

    Article  CAS  PubMed  Google Scholar 

  • Carbonell AA, Aarabi MA, DeLaune RD, Gambrell RP, Patrick WH Jr (1998) Arsenic in wetland vegetation: availability, phytotoxicity, uptake and effects on plant growth and nutrition. Sci Total Environ 217:189–199

    Article  CAS  Google Scholar 

  • Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, Lopez R, Chamber MA, Palomares AJ (2005) Isolation and characterisation of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcollar pyrite mine. Soil Biol Biochem 37:1131–1140

    Article  CAS  Google Scholar 

  • Castanheira N, Dourado AC, Alves PI, Cortés-Pallero AM, Delgado-Rodríguez AI, Prazeres A, Borges N, Sánchez C, Barreto Crespo MT, Fareleira P (2014) Annual ryegrass-associated bacteria with potential for plant growth promotion. Microbiol Res 169:768–779

    Article  CAS  PubMed  Google Scholar 

  • Castro IV, Ferreira E, McGrath SP (2003) Survival and plasmid stability of rhizobia introduced into a contaminated soil. Soil Biol Biochem 35:49–54

    Article  CAS  Google Scholar 

  • Castro IV, Ferreira EM (2006) Contaminación y fertilización: metales pesados y lodos de depuradoras. In: Bedmar EJ, González J, Lluch C, Rodelas B (eds) Fijación de nitrógeno: Fundamentos y Aplicaciones. Sociedad Española de Fijación de Nitrógeno (SEFIN), Granada, pp 291–303

    Google Scholar 

  • Castro IV, Ferreira EM (2010) Nitrogen fixing symbioses adapted to contaminated soils. In: Araújo ASF, Figueiredo MVB (eds) Microbial ecology of tropical soils. Nova, New York, pp 1–18

    Google Scholar 

  • Castro IV, Ferreira EM, McGrath SP (1997) Effectiveness and genetic diversity of Rhizobium leguminosarum bv. trifolii isolates in Portuguese soils polluted by industrial effluents. Soil Biol Biochem 29:1209–1213

    Article  CAS  Google Scholar 

  • Castro IV, Sá-Pereira P, Simões F, Matos JA, Ruiz O, Ferreira E (2008) Lotus/Rhizobium symbiosis in contaminated soils. Importance and use for bioremediation. Lotus Newslett 38:44–45

    Google Scholar 

  • Castro IV, Sequeira OA (1989) Detecção rápida de estirpes de Rhizobium leguminosarum biovar trifolii por um processo modificado do teste imunoenzimático (ELISA). Agron Lusit 44:79–88

    Google Scholar 

  • Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184:311–321

    Article  CAS  Google Scholar 

  • Chabot R, Beauchamp CJ, Kloepper JW, Antoun H (1998) Effect of phosphorus on root colonization and growth promotion of maize by bioluminescent mutants of phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Soil Biol Biochem 30:1615–1618

    Article  Google Scholar 

  • Chaintreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, de Lajudie P, Dreyfus B (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66:5437–5447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz J Microbiol 38:124–130

    Article  Google Scholar 

  • Chen H, Richardson AE, Rolfe BG (1993) Studies on the physiological and genetic basis of acid tolerance in Rhizobium leguminosarum bv. trifolii. Appl Environ Microbiol 59:1798–1804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WM, Laevens S, Lee TM, Coenye T, de Vos P, Mergeay M (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  CAS  PubMed  Google Scholar 

  • Cordovilla MP, Ligero F, Lluch C (1995) Influence of host genotypes on growth, symbiotic performance and nitrogen assimilation in faba bean (Vicia faba L.) under salt stress. Plant Soil 172:289–297

    Article  CAS  Google Scholar 

  • Costechareyre D, Rhouma A, Lavire C, Portier P, Chapulliot D, Bertolla F, Boubaker A, Dessaux Y, Nesme X (2010) Rapid and efficient identification of Agrobacterium species by recA allele analysis: Agrobacterium recA diversity. Microb Ecol 60:862–872

    Article  CAS  PubMed  Google Scholar 

  • Coventry DR, Evans J (1989) Symbiotic nitrogen fixation and soil acidity. In: Robson AD (ed) Soil acidity and plant growth. Academic, Sydney, pp 103–137

    Google Scholar 

  • Crespi M, Gálvez S (2000) Molecular mechanisms in root nodule development. J Plant Growth Regul 19:155–166

    CAS  PubMed  Google Scholar 

  • Crespo DG (2006) The role of pasture improvement on the rehabilitation of the montado/dehesa system and in developing its traditional products. In: Ramalho Ribeiro JMC, Horta AEM, Mosconi C, Rosati A (eds) Animal products from the Mediterranean area. EAAP publication N° 119. Wageningen Academic Publishers, Wageningen, pp 185–197

    Google Scholar 

  • Cunningham SD, Munns DN (1984) The correlation between extracellular polysaccharide production and acid tolerance in Rhizobium. Soil Sci Soc Am J 48:1273–1276

    Article  CAS  Google Scholar 

  • Dakora FD, Matiru V, King M, Phillips DA (2002) Plant growth promotion in legumes and cereals by lumichrome, a rhizobial signal metabolite. In: Finan TM, O’Brian MR, Layzell DB, Vessey K, Newton WE (eds) Nitrogen fixation: Global perspectives. CABI Publishing, Wallingford, pp 321–322

    Google Scholar 

  • Date RA, Halliday J (1979) Selecting Rhizobium for acid, infertile soils of the tropics. Nature 277:62–64

    Article  Google Scholar 

  • de Lucena DKC, Pühler A, Weidner S (2010) The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiol 10:265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Delgado MJ, Garrido JM, Ligero F, Lluch C (1993) Nitrogen fixation and carbon metabolism by nodules and bacteroids of pea plants under sodium chloride. Physiol Plant 89:824–829

    Article  CAS  Google Scholar 

  • Delgado MJ, Ligero F, Lluch C (1994) Effects of salt stress on growth and nitrogen fixation by pea, faba-bean, common bean and soybean plants. Soil Biol Biochem 26:371–376

    Article  CAS  Google Scholar 

  • Demir Y, Kocacaliskan I (2002) Effect of NaCl and proline on bean seedlings culture in vitro. Biol Plantarum 45:597–599

    Article  CAS  Google Scholar 

  • Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:R775–R785

    Article  CAS  PubMed  Google Scholar 

  • Depret G, Houot S, Allard MR, Breuil MC, Nouaim R, Laguerre G (2004) Long-term effects of crop management on Rhizobium leguminosarum biovar viciae populations. FEMS Microbiol Ecol 51:87–97

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Ravina M, Baath M, Frostegard A (1994) Multiple heavy metal tolerance of soil bacterial communities and its measurement by thymidine incorporation technique. Appl Environ Microbiol 60:2238–2247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dilworth MJ, Carson KC, Giles RGF, Byrne LT, Glenn AR (1998) Rhizobium leguminosarum bv. viciae produces a novel cyclic trihydroxamate siderophore, vicibactin. Microbiology 144:781–791

    Article  CAS  Google Scholar 

  • Dilworth MJ, Glenn AR (1999) Problems of adverse pH and bacterial strategies to combat it. Novartis Found Symp 221:4–14

    CAS  PubMed  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Dong Z, Shi L, Wang Y, Chen L, Cai Z, Wang Y, Jin J, Li X (2013) Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int J Mol Sci 14:2717–2738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dourado AC, Alves PIL, Tenreiro T, Ferreira EM, Tenreiro R, Fareleira P, Crespo TB (2009) Identification of Sinorhizobium (Ensifer) medicae based on a specific genomic sequence unveiled by M13-PCR fingerprinting. Int Microbiol 12:215–225

    CAS  PubMed  Google Scholar 

  • Eaglesham A, Seaman B, Ahmad H, Hassouna S, Ayanaba A, Mulongoy K (1991) High temperature tolerant “cowpea” rhizobia. In: Gibson AH, Newton WE (eds) Current perspectives in nitrogen fixation. Australian Academy of Science, Canberra, p 356

    Google Scholar 

  • Elsheikh EAE, Wood M (1990) Effect of salinity on growth, nodulation and nitrogen yield of chickpea (Cicer arietinum L.). J Exp Bot 41:1263–1269

    Article  CAS  Google Scholar 

  • Elsheikh EAE, Wood M (1995) Nodulation and N2 fixation in soybean inoculated with salt-tolerant rhizobia or salt-sensitive bradyrhizobia in saline soil. Soil Biol Biochem 27:657–661

    Article  CAS  Google Scholar 

  • FAO (2011) Current world fertilizer trends and outlook to 2015. Rome, Italy. ftp://ftp.fao.org/ag/agp/docs/cwfto15.pdf. Assessed 11 May 2015

  • Fentahun M, Akhtar MS, Muleta D, Limmese F (2013) Isolation and characterization of nitrogen deficit Rhizobium isolates and their effect on growth of haricot bean. Afr J Agric Res 46:5942–5952

    Google Scholar 

  • Ferreira E, Marques JF (1992) Selection of Portuguese Rhizobium leguminosarum bv. trifolii strains for production of legume inoculants. I. Screening for effectiveness in laboratory conditions. Plant Soil 147:151–158

    Article  Google Scholar 

  • Ferreira E, Simões N, Castro IV, Carneiro L (2010) Relationships of selected soil parameters and natural pastures yield in the montado ecosystem of the Mediterranean area using multivariate analysis. Silva Lusitana 18:151–166

    Google Scholar 

  • Ferreira EM, Castro IV (2011) Fijación biológica de nitrógeno y productividade de pastos naturales en sistemas agrícolas del mediterráneo. In: Megías M, Rivilla R, Soto MJ, Delgado MJ, González E, Mateos PF, León M, Rodelas B, Bedmar EJ (eds) Fundamentos y aplicaciones agroambientales de las interacciones beneficiosas plantas-microorganismos. Sociedad Española de Fijación de Nitrógeno (SEFIN), Granada, pp 403–416

    Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flores-Félix JD, Carro L, Velázquez E, Valverde A, Cerda-Castillo E, García-Fraile P, Rivas R (2013) Phyllobacterium endophyticum sp. nov., isolated from nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 63:821–826

    Article  PubMed  CAS  Google Scholar 

  • Fred EB, Baldwin IL, McCoy E (1932) Root-nodule bacteria and leguminous plants. University of Wisconsin, Madison

    Google Scholar 

  • Garau G, Reeve WG, Brau L (2005) The symbiotic requirements of different Medicago spp. suggest the evolution of Sinorhizobium meliloti and S. medicae with hosts differentially adapted to soil pH. Plant Soil 176:263–277

    Article  CAS  Google Scholar 

  • García-Fraile P, Carro L, Robledo M, Ramírez-Bahena M-H, Flores-Félix J-D, Fernández MT, Mateos PF, Rivas R, Igual JM, Martínez-Molina E, Peix A, Velázquez E (2012) Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One 7:e38122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Georgiev GI, Atkins CA (1993) Effects of salinity on N2 fixation, nitrogen metabolism and export and diffusive conductance of cowpea root nodules. Symbiosis 15:239–255

    Google Scholar 

  • Gibson AH, Curnow BC, Bergerssen FJ, Brockwell J, Robinson AC (1975) Studies of field populations of Rhizobium: effectiveness of strains of Rhizobium trifolii associated with Trifolium subterraneum L. in south-eastern Australia. Soil Biol Biochem 7:95–102

    Article  Google Scholar 

  • Giller KE, Nussbaum R, Chaudri AM, McGrath SP (1993) Rhizobium meliloti is less sensitive to heavy-metal contamination in soil than R. leguminosarum bv. trifolii or R. loti. Soil Biol Biochem 25:273–278

    Article  CAS  Google Scholar 

  • Giller KE, Wilson K (1991) Nitrogen fixation in tropical cropping systems. CAB International, Wallingford

    Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    Article  CAS  PubMed  Google Scholar 

  • Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium nodulation under adverse soil conditions. Can J Microbiol 38:475–484

    Article  CAS  Google Scholar 

  • Graham PH (2008) Ecology of the root-nodule bacteria of legumes. In: James EK, Sprent JI, Newton WE, Dilworth MJ (eds) Nitrogen-fixing leguminous symbiosis. Springer, The Netherlands, pp 23–58

    Google Scholar 

  • Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martinez E (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for pH tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207

    Article  CAS  Google Scholar 

  • Graham PH, Sadowsky MJ, Keyser HH, Barnet M, Bradley RS, Cooper JE, De Ley DJ, Jarvi BDW, Roslycky EB, Strijdom BW, Young JPW (1991) Proposed minimal standards for the description of new genera and species of root- and stem-nodulating bacteria. Int J Syst Bacteriol 41:582–587

    Article  Google Scholar 

  • Graham PH, Vance CP (2000) Nitrogen fixation in perspective, an overview of research and extension needs. Field Crops Res 65:93–106

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu CT, Wang ET, Sui XH, Chen WF, Chen WX (2007) Diversity and geographical distribution of rhizobia associated with Lespedeza spp. in temperate and subtropical regions of China. Arch Microbiol 188:355–365

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91:117–126

    Article  PubMed  Google Scholar 

  • Hafeez FY, Safdar ME, Chaudhry AU, Malik KA (2004) Rhizobial inoculation improves seedling emergence, nutrient uptake and growth of cotton. Aust J Exp Agric 44:617–622

    Article  Google Scholar 

  • Han TX, Wang ET, Han LL, Chen WF, Sui XH, Chen WX (2008) Molecular diversity and phylogeny of rhizobia associated with wild legumes native to Xinjiang, China. Syst Appl Microbiol 58:1693–1699

    CAS  Google Scholar 

  • Haque SE, Ghaffar A (1993) Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J Phytopathol 138:157–163

    Article  Google Scholar 

  • Hardy RWF (1993) Biological nitrogen fertilization: Present and future applications in agriculture and environmental challenges. In: Srivastava JP, Aldermans H (eds) Proceeding of 13th agricultural sector symposium. The World Bank, Washington, DC, pp 109–117

    Google Scholar 

  • Harrison SP, Mytton LR, Skot L, Dye M, Cresswell A (1992) Characterization of Rhizobium isolates by amplification of DNA polymorphisms using random primers. Can J Microbiol 38:1009–1015

    Article  CAS  PubMed  Google Scholar 

  • Hartel PG, Alexander M (1984) Temperature and desiccation tolerance of cowpea rhizobia. Can J Microbiol 30:820–823

    Article  Google Scholar 

  • Harwood R (1990) A history of sustainable agriculture. In: Edwards CA, Lal R, Madden P, Miller RH, House G (eds) Sustainable agriculture systems. Soil and Water Conservation Society, Ankeny, pp 4–19

    Google Scholar 

  • Hernández-Armenta R, Wien H, Eagleshman ARJ (1989) Carbohydrate partitioning and nodule functioning in common bean after heat stress. Crop Sci 29:1292–1297

    Article  Google Scholar 

  • Herridge D, Gemell G, Hartley E (2002) Legume inoculants and quality control. In: Herridge D (ed) Inoculants and nitrogen fixation legumes in Vietnam. ACIAR Proceedings, Canberra, pp 105–115

    Google Scholar 

  • Hider RC (1984) Siderophore mediated absorption of iron. Struct Bond 58:25–87

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hirsch PR, Van Montagu M, Johnston AWB, Brewin NJ, Schell J (1980) Physical identification of bacteriocinogenic nodulation and other plasmids in strains of Rhizobium leguminosarum. J Gen Microbiol 120:403–412

    Google Scholar 

  • Howieson JG, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia–some contemporary thoughts. Soil Biol Biochem 36:1261–1273

    Article  CAS  Google Scholar 

  • Humphry DR, Andrews M, Santos SR, James EK, Vinogradova LV, Perin L, Reis VM, Cummings SP (2007) Phylogenetic assignment and mechanism of action of a crop growth promoting Rhizobium radiobacter strain used as a biofertilizer on graminaceous crops in Russia. Antonie Van Leeuwenhoek 91:105–113

    Article  PubMed  Google Scholar 

  • Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris (L.). Plant Soil 149:95–102

    Article  CAS  Google Scholar 

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with emphasis on Brazil. Field Crops Res 65:151–164

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Imran A, Hafeez FY, Frühling A, Schumann P, Malik KA, Stackebrandt E (2010) Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. Int J Syst Evol Microbiol 60:1548–1553

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo PMD, Guimarães AA, Florentino LA, Silva KB, Nóbrega RSA, Moreira FMS (2013) Symbiotic nitrogen-fixing bacterial populations trapped from soils under agroforestry systems in the Western Amazon. Sci Agric 70:397–404

    CAS  Google Scholar 

  • Jarvis BDW, Tighe SW (1994) Rapid identification of Rhizobium species based on cellular fatty acid analysis. Plant Soil 161:31–41

    Article  CAS  Google Scholar 

  • Joffre R, Vacher J, Llanos C, Long G (1988) The dehesa: an agrosilvopastoral system of the Mediterranean region with special reference to the Sierra Morena area of Spain. Agroforest Syst 6:71–96

    Article  Google Scholar 

  • Jourand P, Giraud E, Béna G, Sy A, Willems A, Gillis M, Dreyfus B, De Lajudie P (2004) Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int J Syst Evol Microbiol 54:2269–2273

    Article  CAS  PubMed  Google Scholar 

  • Judicial Commission (2008) Opinion 84 – The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘Sinorhizobium adhaerens’ is not validly published. Int J Syst Evol Microbiol 58:1973

    Article  Google Scholar 

  • Karanja NK, Wood M (1988) Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya. Tolerance of high temperature and antibiotic resistance. Plant Soil 112:15–22

    Article  CAS  Google Scholar 

  • Kawasaki S, Murakami Y (2000) Genome analysis of Lotus japonicus. J Plant Res 113:497–506

    Article  Google Scholar 

  • Keane PJ, Kerr A, New RB (1970) Crown gall of stone fruit. II. Identification and nomenclature of Agrobacterium isolates. Aust J Biol Sci 23:585–595

    Google Scholar 

  • Khan M, Scullion J (1999) Microbial activity in grassland soil amended with sewage sludge containing varying rates and combinations of Cu Ni and Zn. Biol Fert Soils 30:202–209

    Article  CAS  Google Scholar 

  • Kipe-Nolt JA, Giller KE (1993) A field evaluation using 15N isotope dilution method of lines of Phaseolus vulgaris bred for increased nitrogen fixation. Plant Soil 152:107–114

    Article  Google Scholar 

  • Kure CF, Abeln ECA, Holst-Jensen A, Skaar I (2002) Differentiation of Penicillium commune and Penicillium palitans isolates from cheese and indoor environments of cheese factories using M13 fingerprinting. Food Microbiol 19:151–157

    Article  CAS  Google Scholar 

  • Laguerre G, Mazurie SI, Amarger N (1992) Plasmid profiles and restriction length polymorphism of Rhizobium leguminosarum bv. viciae in field populations. FEMS Microbiol Ecol 101:17–26

    Article  CAS  Google Scholar 

  • Lakzian A, Murphy P, Turner A, Beynon JL, Giller KE (2002) Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance. Soil Biol Biochem 34:519–529

    Article  CAS  Google Scholar 

  • Lasat MM (2000) Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. J Hazard Subst Res 2:1–21

    Google Scholar 

  • Lauchli A (1984) Salt exclusion: an adaptation of legumes for crops and pastures under saline conditions. In: Staples RC, Toenniessen GH (eds) Salinity tolerance in plants: strategies for crop improvement. Wiley, New York, pp 171–188

    Google Scholar 

  • Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J, Choi J, Kang C, Qiu J, Stacey G (2013) Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–1387

    Article  CAS  PubMed  Google Scholar 

  • Lie TA (1981) Environmental physiology of the legume-Rhizobium symbiosis. In: Broughton WJ (ed) Nitrogen fixation, vol I. Clarendon, Oxford, pp 104–134

    Google Scholar 

  • Lin DX, Wang ET, Tang H, Han TX, He YR, Guan SH, Chen WX (2008) Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int J Syst Evol Microbiol 58:1409–1413

    Article  CAS  PubMed  Google Scholar 

  • Lindström K, Young JPW (2011) International Committee on Systematics of Prokaryotes, Subcommittee on the taxonomy of Agrobacterium and Rhizobium. Int J Syst Evol Microbiol 61:3089–3093

    Article  PubMed  Google Scholar 

  • Long SR (2001) Genes and signals in the Rhizobium-legume symbiosis. Plant Physiol 125:69–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorite J, Castro IV, Muñoz S, Sanjuán J (2012) Phylogenetic relationship of Lotus uliginosus symbionts with bradyrhizobia nodulating genistoid legumes. FEMS Microbiol Ecol 79:454–464

    Article  CAS  PubMed  Google Scholar 

  • Lupwayi NZ, Clayton GW, Hanson KG, Rice WA, Biederbeck VO (2004) Endophytic rhizobia in barley, wheat and canola roots. Can J Plant Sci 84:37–45

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahieu S, Frérot H, Vidal C, Galiana A, Heulin K, Maure L, Brunel B, Lefèbvre C, Escarré J, Cleyet-Marel JC (2011) Anthyllis vulneraria/Mesorhizobium metallidurans, an efficient symbiotic nitrogen fixing association able to grow in mine tailings highly contaminated by Zn, Pb and Cd. Plant Soil 342:405–417

    Article  CAS  Google Scholar 

  • Man CX, Wang H, Chen WF, Sui XH, Wang ET, Chen WX (2008) Diverse rhizobia associated with soybean grown in the subtropical and tropical regions of China. Plant Soil 310:77–87

    Article  CAS  Google Scholar 

  • Martinez-Romero E, Caballero-Mellado J (1996) Rhizobium phylogenies and bacterial genetic diversity. Crit Rev Plant Sci 15:113–140

    Article  CAS  Google Scholar 

  • Martinez-Romero E, Caballero-Mellado J, Gándara B, Rogel MA, López Merino A, Wang ET, Fuentes-Ramirez LE, Toledo I, Hernández-Lucas I, Martinez-Romero J (2000) Ecological, phylogenetic and taxonomic remarks on diazotrophs and related genera. In: Pedrosa FO, Hungria M, Yates G, Newton WE (eds) Nitrogen fixation: from molecules to crop productivity. Springer, The Netherlands, pp 155–160

    Google Scholar 

  • Materon LA (1988) Maximizing biological nitrogen fixation by forage and pasture legumes in semi-arid areas. In: Beck DP, Materon LA (eds) Nitrogen fixation by legumes in Mediterranean agriculture. ICARDA, Martinus Nijhoff Publishers, Dordrecht, pp 33–40

    Chapter  Google Scholar 

  • Matiru VN, Dakora FD (2005) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol 166:439–444

    Article  CAS  PubMed  Google Scholar 

  • Matiru VN, Jaffer MA, Dakora FD (2005) Rhizobial infection of African landraces of sorghum (Sorghum bicolor L.) and finger millet (Eleusine coracana L.) promotes plant growth and alters tissue nutrient concentration under axenic conditions. Symbiosis 40:7–15

    CAS  Google Scholar 

  • Maynaud G, Willems A, Soussou S, Vidal C, Mauré L, Moulin L, Cleyet-Marel JC, Brunel B (2012) Molecular and phenotypic characterization of strains nodulating Anthyllis vulneraria in mine tailings, and proposal of Aminobacter anthyllidis sp. nov., the first definition of Aminobacter as legume-nodulating bacteria. Syst Appl Microbiol 35:65–72

    Article  CAS  PubMed  Google Scholar 

  • McInnes A, Haq K (2003) Contributions of rhizobia to soil nitrogen fertility. In: Abbott LK, Murphy DV (eds) Soil biological fertility: a key to sustainable land use in agriculture. Kluwer Academic Publishers, Dordrecht, The Netherland, pp 99–108

    Google Scholar 

  • McInroy JA, Kloepper JW (1995) Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 173:337–342

    Article  CAS  Google Scholar 

  • Mehboob I, Naveed M, Zahir ZA (2009) Rhizobial associations with non-legumes: mechanisms and applications. Crit Rev Plant Sci 28:432–456

    Article  CAS  Google Scholar 

  • Mellor HY, Glen AR, Arwas R, Dilworth MJ (1987) Symbiotic and competitive properties of motility mutants of Rhizobium trifolii TA1. Arch Microbiol 148:34–39

    Article  CAS  Google Scholar 

  • Miransari M, Smith D (2009) Rhizobial lipo-chitooligosaccharides and gibberellins enhance barley (Hordeum vulgare L.) seed germination. Biotechnology 8:270–275

    Article  CAS  Google Scholar 

  • Mishra RPN, Singh RK, Jaiswal HK, Kumar V, Maurya S (2006) Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Curr Microbiol 52:383–389

    Article  CAS  PubMed  Google Scholar 

  • Moawad H, Beck D (1991) Some characteristics of Rhizobium leguminosarum isolates from uninoculated field-grown lentil. Soil Biol Biochem 23:917–925

    Article  Google Scholar 

  • Moulin L, Béna G, Boivin-Masson C, Stepkowski T (2004) Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732

    Article  CAS  PubMed  Google Scholar 

  • Mpepereki S, Wollum AG, Makonese F (1996) Diversity in symbiotic specificity of cowpea rhizobia indigenous to Zimbabwean soils. Plant Soil 186:167–171

    Article  CAS  Google Scholar 

  • Muglia CI, Grasso DH, Aguilar OM (2007) Rhizobium tropici response to acidity involves activation of glutathione synthesis. Microbiology 153:1286–1296

    Article  CAS  PubMed  Google Scholar 

  • Munns DN (1986) Acid soils tolerance in legumes and rhizobia. Adv Plant Nutr 2:63–91

    CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nascimento FX, Rossi MJ, Soares CR, McConkey BJ, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS One 9:e99168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neilands JB (1981) Iron absorption and transport in microorganisms. Annu Rev Nutr 1:27–46

    Article  CAS  PubMed  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  CAS  PubMed  Google Scholar 

  • Noel KD, Brill WJ (1980) Diversity and dynamics of indigenous Rhizobium japonicum populations. Appl Environ Microbiol 40:931–938

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42:279–283

    Article  CAS  PubMed  Google Scholar 

  • Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Nutman PS, Ross GJS (1970) Rhizobium in soils of the Rothamsted and Woburn farms. In: Rothamsted Experimental Station Report for 1969, Part 2:148–167

    Google Scholar 

  • Olea L, San Miguel-Ayanz A (2006) The Spanish dehesa. A traditional Mediterranean silvopastoral system linking production and nature conservation. In: Lloveras J, González-Rodríguez A, Vázquez-Yañez O, Piñeiro J, Santamaría O, Olea L, Poblaciones MJ (eds), Sustainable grassland productivity: Proceedings of the 21st General Meeting of the European Grassland Federation, Badajoz, pp 3–15

    Google Scholar 

  • Oliveira A, Pampulha ME (2006) Effects of long-term heavy metal contamination on soil microbial characteristics. J Biosci Bioeng 102:157–161

    Article  CAS  PubMed  Google Scholar 

  • Oliveira A, Pampulha ME, Neto MM, Almeida AC (2008) Enumeration and characterization of arsenic-tolerant diazotrophic bacteria in a long-term heavy metal contaminated soil. Water Air Soil Pollut 200:237–243

    Article  CAS  Google Scholar 

  • Pajuelo E, Dary M, Palomares AJ, Rodriguez-Llorente ID, Carrasco JA, Chamber MA (2008) Biorhizoremediation of heavy metals toxicity using Rhizobium-legume symbioses. In: Dakora F, Chimphango SBM, Valentine AJ, Elmerich C, Newton WE (eds) Biological nitrogen fixation: towards poverty alleviation through sustainable agriculture. Springer, The Netherlands, pp 101–104

    Chapter  Google Scholar 

  • Pajuelo E, Rodríguez-Llorente ID, Lafuente A, Caviedes MA (2011) Legume-Rhizobium symbioses as a tool for bioremediation of heavy metal polluted soils. In: Khan MS, Zaidi A, Goel R, Musarrat J (eds) Biomanagement of metal-contaminated soils, vol 20, Environmental pollution. Springer, The Netherlands, pp 95–123

    Chapter  Google Scholar 

  • Pastor J, Hernández AJ, Prieto N, Fernández-Pascual M (2003) Accumulating behaviour of Lupinus albus L. growing in a normal and a decalcified calcic luvisol polluted with Zn. J Plant Physiol 160:1455–1463

    Article  Google Scholar 

  • Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martínez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33:103–110

    Article  CAS  Google Scholar 

  • Peng S, Biswas JC, Ladha JK, Gyaneshwar P, Chen Y (2002) Influence of rhizobial inoculation on photosynthesis and grain yield of rice. Agron J 94:925–929

    Article  Google Scholar 

  • Peoples MB, Bowman AM, Gault RR, Herridge DF, McCallum MH, McKormick KM, Norton RM, Rochester IJ, Scammel GJ, Schwenke GD (2001) Factors regulating the contributions of fixed nitrogen by pasture and crop legumes to different farming systems of eastern Australia. Plant Soil 228:29–41

    Article  CAS  Google Scholar 

  • Pereira SIA, Castro IV, Figueira E (2007) Are Rhizobium and soil enzyme activities good indicators of heavy metal soil contamination. In: Kurladze GV (ed) Environmental microbiology research trends. Nova, Lancaster, pp 237–256

    Google Scholar 

  • Pérez-Montaño F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips DA, Joseph CM, Yang G-P, Martínez-Romero E, Sanborn JR, Volpin H (1999) Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth. Proc Natl Acad Sci U S A 96:12275–12280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piha MI, Munns DN (1987) Sensitivity of the common bean (Phaseolus vulgaris L.) symbiosis to high soil temperature. Plant Soil 98:183–194

    Article  Google Scholar 

  • Rashid MH, Krehenbrink M, Akhtar MS (2015) Nitrogen-fixing plant-microbe symbioses. In: Lichtfouse E (ed) Sustainable agriculture reviews, vol 15. Springer International Publishing, Switzerland, pp 193–234

    Google Scholar 

  • Reeve W, Brau L, Castelli J, Garau G, Sohlenkamp C, Geiger O, Dilworth M, Glenn A, Howieson J, Tiwari R (2006) The Sinorhizobium medicae WSM419 IpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions. Microbiology 152:3049–3059

    Article  CAS  PubMed  Google Scholar 

  • Reeve WG, Tiwari RP, Kale NB, Dilworth MJ, Glenn AR (2002) ActP controls copper homeostasis in Rhizobium leguminosarum bv. viciae and Sinorhizobium meliloti preventing low pH induced copper toxicity. Mol Microbiol 43:981–991

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rice WA, Penney DC, Nyborg M (1977) Effects of soil acidity on rhizobia numbers, nodulation and nitrogen fixation by alfalfa and red clover. Can J Soil Sci 57:197–203

    Article  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (1989) Acid-tolerance and symbiotic effectiveness of Rhizobium trifolii associated with a Trifolium subterraneum L. based pasture growing in an acid soil. Soil Biol Biochem 21:87–95

    Article  Google Scholar 

  • Rivas R, Garcia-Fraile P, Velazquez E (2009) Taxonomy of bacteria nodulating legumes. Microbiol Insights 2:51–69

    Google Scholar 

  • Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martínez-Molina E, Gillis M, Velázquez E (2003) Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 26:47–53

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues S, Ferreira E, Figueira E, Castro IV (2010) Genetic diversity of rhizobia nodulating alfalfa. In: Becana M (ed) Biological nitrogen fixation and plant-associated microorganisms. Sociedad Española de Fijación de Nitrógeno, Zaragoza, pp 49–50

    Google Scholar 

  • Ruiz-Díez B, Quiñones AM, Fajardo S, López MA, Higueras P, Fernández-Pascual M (2012) Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl Microbiol Biotechnol 96:543–554

    Article  PubMed  CAS  Google Scholar 

  • Sadowsky MJ (2005) Soil stress factors influencing symbiotic nitrogen fixation. In: Werner D, Newton WE (eds) Nitrogen fixation research in agriculture, forestry, ecology, and the environment. Springer, The Netherlands, pp 89–102

    Chapter  Google Scholar 

  • Sadowsky MJ, Graham PH (1998) Soil biology of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas P (eds) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Springer, The Netherlands, pp 155–172

    Google Scholar 

  • Sanchez M, Ramírez-Bahena MH, Peix A, Lorite MJ, Sanjuán J, Velázquez E, Monza J (2014) Phyllobacterium loti sp. nov. isolated from nodules of Lotus corniculatus. Int J Syst Evol Microbiol 64:781–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos-Villalobos S, Folter S, Délano-Frier JP, Gómez-Lim MA, Guzmán-Ortiz DA, Peña-Cabriales JJ (2013) Growth promotion and flowering induction in mango (Mangifera indica L. cv “Ataulfo”) trees by Burkholderia and Rhizobium inoculation: morphometric, biochemical, and molecular events. J Plant Growth Regul 32:615–627

    Article  CAS  Google Scholar 

  • Sá-Pereira P, Rodrigues M, Castro IV, Simões F (2007) Identification of an arsenic resistance mechanism in strains of Rhizobium. World J Microbiol Biotechnol 23:1351–1356

    Article  CAS  Google Scholar 

  • Sá-Pereira P, Rodrigues M, Simões F, Domingues L, Castro IV (2009) Bacterial activity in heavy metals polluted soils: metal efflux systems in native rhizobial strains. Geomicrobiol J 26:281–288

    Article  CAS  Google Scholar 

  • Saxena MC (1988) Food legumes in the Mediterranean type of environment and ICARDA’s efforts in improving their productivity. In: Beck DP, Materon LA (eds) Nitrogen fixation by legumes in Mediterranean agriculture. ICARDA, Martinus Nijhoff Publishers, Dordrecht, pp 11–23

    Chapter  Google Scholar 

  • Sequeira EM (2008) Pasture and fodder crop as part of high natural value farm systems at Mediterranean dryland agro-ecosystems. Options Méditerranéennes Series A 79:17–22

    Google Scholar 

  • Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JPW, Chen WM (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 62:2272–2278

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui ZA (2006) PGPR: prospective biocontrol agents of plant pathogens. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 111–142

    Chapter  Google Scholar 

  • Silver S (1998) Genes for all metals - a bacterial view of the Periodic Table. The 1996 Thom Award Lecture. J Ind Microbiol Biotechnol 20:1–12

    Article  CAS  PubMed  Google Scholar 

  • Simon Z, Mtei K, Gessesse A, Ndakidemi PA (2014) Isolation and characterization of nitrogen fixing rhizobia from cultivated and uncultivated soils of northern Tanzania. Am J Plant Sci 5:4050–4067

    Article  CAS  Google Scholar 

  • Singleton PW, Bohlool BB, Nakao PL (1992) Legume rhizobia inoculation in the tropics: myths and realities. In: Lal R, Sanchez PA (eds), Myths and science of soils in the tropics. Special Publication No. 29. Soil Science Society of America, Madison, pp 135–155

    Google Scholar 

  • Smil V (1999) Nitrogen in crop production: an account of global flows. Glob Biogeochem Cycles 13:647–662

    Article  CAS  Google Scholar 

  • Smith DL, Prithiviraj B, Zhang F (2002) Rhizobial signals and control of plant growth. In: Finan TM, O’Brian MR, Layzell DB, Vessey K, Newton WE (eds) Nitrogen fixation: global perspectives. CABI Publishing, Wallingford, pp 327–330

    Google Scholar 

  • Spaepen S, Vanderleyden J (2010) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a001438

    Google Scholar 

  • Spaink HP, Wijffelman CA, Pees E, Okker RJH, Lugtenberg BJJ (1987) Rhizobium nodulation gene nodD as a determinant of host specificity. Nature 328:337–340

    Article  CAS  Google Scholar 

  • Sprent JI (1994) Evolution and diversity in the legume-Rhizobium symbiosis: Chaos theory. Plant Soil 161:1–10

    Article  Google Scholar 

  • Sprent JI (1995) Legume trees and shrubs in the tropics: N2 fixation in perspective. Soil Biol Biochem 27:401–407

    Article  CAS  Google Scholar 

  • Sridevi M, Mallaiah KV (2009) Phosphate solubilisation by Rhizobium strains. Indian J Microbiol 49:98–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein M, Bromfield ESP, Dye M (1982) An assessment of a method based on intrinsic antibiotic resistance for identifying Rhizobium strains. Ann Appl Biol 101:261–267

    Article  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willem 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Talbi C, Sánchez C, Hidalgo-Garcia A, González EM, Arrese-Igor C, Girard L, Bedmar EJ, Delgado MJ (2012) Enhanced expression of Rhizobium etli cbb3 oxidase improves drought tolerance of common bean symbiotic nitrogen fixation. J Exp Bot 63:5035–5043

    Article  CAS  PubMed  Google Scholar 

  • Tenkorang F, Lowenberg-Deboer J (2008) Forecasting long-term global fertilizer demand. FAO, Rome, Italy

    Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian CF, Wang ET, Han TX, Sui XH, Chen WX (2007) Genetic diversity of rhizobia associated with Vicia faba in three ecological regions of China. Arch Microbiol 188:273–282

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Trujillo ME, Willems A, Abril A, Planchuelo A-M, Rivas R, Ludeña D, Mateos PF, Martínez-Molina E, Velázquez E (2005) Nodulation of Lupinus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trujillo RG, Mata C (2001) The dehesa: an extensive livestock system in the Iberian Peninsula. In: Hovi M, Trujillo RG (eds) Diversity of livestock systems and definition of animal welfare. Proceedings of the Second NAHWOA Workshop, Córdoba, pp 50–61

    Google Scholar 

  • Valls M, Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338

    Article  CAS  PubMed  Google Scholar 

  • Valverde A, Velázquez E, Fernández-Santos F, Vizcaíno N, Rivas R, Gillis M, 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  CAS  PubMed  Google Scholar 

  • Valverde A, Velázquez E, Gutiérrez 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  CAS  PubMed  Google Scholar 

  • van Berkum P, Eardly D (1998) Molecular evolutionary systematics of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas P (eds) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Springer, The Netherlands, pp 1–24

    Google Scholar 

  • Vandamme P, Goris J, Chen WM, de Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov. nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512

    Article  PubMed  Google Scholar 

  • Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vargas LK, Lisboa BB, Giongo A, Beneduzi A, Passaglia LMP (2010) Potential of rhizobia as plant growth-promoting rhizobacteria. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer, Wien, pp 137–155

    Chapter  Google Scholar 

  • Vargas LK, Lisboa BB, Schlindwein G, Granada CE, Giongo A, Beneduzi A, Passaglia LMP (2009) Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in Rio Grande do Sul state. R Bras Ci Solo 33:1227–1235

    Article  Google Scholar 

  • Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  • Vincent JM (1981) The genus Rhizobium. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The Prokaryotes. A handbook on habitats, isolation and identification of bacteria. Springer, Berlin, pp 818–841

    Google Scholar 

  • Vinuesa P (2013) ICSP Subcommittee on the taxonomy of Rhizobium and Agrobacterium – diversity, phylogeny and systematics. http://edzna.ccg.unam.mx/rhizobial-taxonomy/node/4. Accessed 14 May 2015

  • Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martinez-Romero E, Werner D (2003) Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAt 899 involved in acid tolerance and nodulation competitiveness. Mol Plant Microbe Interact 16:159–168

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Man CX, Wang ET, Chen WX (2009) Diversity of rhizobia and interactions among the host legumes and rhizobial genotypes in an agricultural-forestry ecosystem. Plant Soil 314:169–182

    Article  CAS  Google Scholar 

  • Webster G, Gough C, Vasse J, Batchelor CA, O’Callaghan KJ, Kothari SL, Davey MR, Dénarié J, Cocking EC (1997) Interactions of rhizobia with rice and wheat. Plant Soil 194:115–122

    Article  CAS  Google Scholar 

  • Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

  • Xie Z-P, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vögeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519–1525

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang HC, Cheng J, Finan TM, Rosen BP, Bhattacharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187:6991–6997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yanni YG, Rizk RY, Abb El-Fattah FK, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Garcia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust J Plant Physiol 28:845–870

    CAS  Google Scholar 

  • Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114

    Article  CAS  Google Scholar 

  • Yates RJ, Howieson JG, Reeve WG, O’Hara GW (2011) A re-appraisal of the biology and terminology describing rhizobial strain success in nodule occupancy of legumes in agriculture. Plant Soil 348:255–267

    Article  CAS  Google Scholar 

  • Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51:89–103

    Article  CAS  PubMed  Google Scholar 

  • Young JPW, Wexler M (1988) Sym plasmid and chromosomal genotypes are correlated in field populations of Rhizobium leguminosarum. J Gen Microbiol 134:2731–2739

    CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zahran HH, Rasanen LA, Karsisto M, Lindstrom K (1994) Alteration of lipopolysaccharide and protein profiles in SDS-PAGE of rhizobia by osmotic and heat stress. World J Microbiol Biotechnol 10:100–105

    Article  CAS  PubMed  Google Scholar 

  • Zhang HH, Charles TC, Driscoll BT, Prithiviraj B, Smith DL (2002) Low temperature-tolerant Bradyrhizobium japonicum strains allowing improved soybean yield in short-season areas. Agron J 94:870–875

    Google Scholar 

  • Zornoza P, Vázquez S, Esteban E, Fernández-Pascual M, Carpena R (2002) Cd-stress in nodulated white lupin: strategies to avoid toxicity. Plant Physiol Biochem 40:1003–1009

    Article  CAS  Google Scholar 

  • Zucuk C, Kivanc M (2008) Preliminary characterization of Rhizobium strains isolated from chickpea nodules. Afr J Biotechnol 7:772–775

    Google Scholar 

  • Zurdo-Piñeiro JL, Rivas R, Trujillo ME, Vizcaíno N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martínez-Molina E, Velázquez 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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Isabel Videira e Castro .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

e Castro, I.V., Fareleira, P., Ferreira, E. (2016). Nitrogen Fixing Symbiosis in a Sustainable Agriculture. In: Hakeem, K., Akhtar, M., Abdullah, S. (eds) Plant, Soil and Microbes. Springer, Cham. https://doi.org/10.1007/978-3-319-27455-3_4

Download citation

Publish with us

Policies and ethics