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Endophytic Bacteria and Their Role in Legumes Growth Promotion

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Bacteria in Agrobiology: Plant Probiotics

Abstract

The rhizosphere and the phylloplane of plants are habitats for large number of microorganisms. The study of plant-associated bacteria is important not only for understanding their role in these interactions but also for biotechnological application in areas as the plant growth promotion. Legume plants are able to form nitrogen-fixing nodules by symbiotic association with soil bacteria collectively known as rhizobia. Even when the term “root nodule bacteria” has been exclusively applied to rhizobia, nonsymbiotic endophytic bacteria from several genera have been isolated from legume nodules, and this is the main topic of this chapter. Endophytes are defined as those microorganisms isolated and detected inside the tissues by microscopic methods, which maintain their ability to infect plants, being rhizobia the most studied group. Endophytic bacteria can positively influence plant growth through different mechanisms, such as fixation of atmospheric nitrogen, solubilization of phosphates, and protection against pathogens, among others. Therefore, a wide number of studies have been and still are focused in plant-growth-promoting bacteria as potential supplements of fertilizers, herbicides, fungicides, etc. For endophytes to exert beneficial effects on plant growth, they should be in an intimate relationship with the host plant. The signaling cascade involved in legume–rhizobia interaction that leads to nodule development as well as recent knowledge about the taxonomy of this bacterial group are also described.

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References

  • Abeles FB, Morgan PW, Salveit ME Jr (1992) Ethylene in plant biology, 2nd edn. Academic, San Diego, CA

    Google Scholar 

  • Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer use efficiency. Appl Microbiol Biotechnol 85:1–12

    Article  PubMed  CAS  Google Scholar 

  • Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886

    Article  PubMed  CAS  Google Scholar 

  • Aeron A, Maheshwari DK (2011) Diversity of root nodulating bacteria in Clitoria ternatea L. Ph.D. thesis, Gurukula Kangri University, Haridwar

    Google Scholar 

  • Amann G, Stetter KO, Llobet-Brossa E, Amann R, Anton J (2000) Direct proof for the presence and expression of two 5% different 16S rRNA genes in individual cells of Haloarcula marismortui. Extremophiles 4:373–376

    Article  PubMed  CAS  Google Scholar 

  • Andrews J, Harris R (2000) The ecology and biogeography of microorganisms on plant surface. Annu Rev Phytopathol 38:145–180

    Article  PubMed  Google Scholar 

  • Anè JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lèvy J, Debellè F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, D’enariè J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  CAS  Google Scholar 

  • Arora NK, Kim MJ, Kang SC, Maheshwari DK (2007) Role of chitinase and β-1,3-glucanase activity produced by a fluorescent pseudomonad and in vitro inhibition of Phytophthora capsici and Rhizoctonia solani. Can J Microbiol 53:207–212

    Article  PubMed  CAS  Google Scholar 

  • Arrighi JF, Barre A, Amor BB, Bersoult A, Campos Soriano L, Mirabella R, de Carvalho-Niebel F, Journet E-P, Ghérardi M, Huguet T, Geurts R, Dénearié J, Rougé P, Gough C (2006) The Medicago truncatula LysM motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265–279

    Article  PubMed  CAS  Google Scholar 

  • Arya R, Maheshwari DK (2009) Isolation of stress tolerating rhizobia and their biocontrol potential against wilt of Cajanus cajan L. Ph.D. thesis, Gurukula Kangri University, Haridwar

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Azevedo JL, Maccheroni W, Pereira JR Jr, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:15–16

    Google Scholar 

  • Bai Y, D’Aoust F, Smith DL, Driscoll BT (2002) Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can J Microbiol 48:230–238

    Article  PubMed  CAS  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32

    Article  PubMed  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:33–66

    Article  CAS  Google Scholar 

  • Baldwin IL, Fred EB (1929) Nomenclature of root nodule bacteria of the Leguminosae. J Bacteriol 17:141–150

    PubMed  CAS  Google Scholar 

  • Barlog P, Grzebisz W (2004) Effect of timing and nitrogen fertilizer application on winter oilseed rape (Brassica napus L.) II Nitrogen uptake dynamics and fertilizer efficiency. J Agron Crop Sci 190:314–323

    Article  Google Scholar 

  • Bashan Y, Holguin G (1998) Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol Biochem 30:1225–1230

    Article  CAS  Google Scholar 

  • Benhizia Y, Benhizia H, Benguedouar A, Muresu R, Giacomini A, Squartini A (2004) Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27:462–468

    Article  PubMed  CAS  Google Scholar 

  • Bishop PE, Premakumar R (1992) Alternative nitrogen fixation systems. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 736–762

    Google Scholar 

  • Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, Batagov AO, Sandal N, Mortensen A, Schauser L, Ellis N, Tikhonovich IA, Stougaard J (2003) The SYM35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol 131:1009–1017

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Burris RH, Roberts GP (1993) Biological nitrogen fixation. Annu Rev Nutr 13:317–335

    Article  PubMed  CAS  Google Scholar 

  • Capoen W, Goormachtig S, De Rycke R, Schroeyers K, Holsters M (2005) SymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci USA 102:10369–10374

    Article  PubMed  CAS  Google Scholar 

  • Castro S, Permigiani M, Vinocur M, Fabra A (1999) Nodulation in peanut (Arachis hypogaea L.) roots in the presence of native and inoculated rhizobia strain. Appl Soil Ecol 13:39–44

    Article  Google Scholar 

  • Cerda Castillo E (2008) Aislamiento de Micromonospora de nódulos de leguminosas tropicales y análisis de su interés como promotor del crecimiento vegetal. Ph.D. thesis, Universidad de Salamanca

    Google Scholar 

  • Chandler M (1978) Some observations of infection of Arachis hypogaea L. by Rhizobium. J Exp Bot 29:749–755

    Article  Google Scholar 

  • Cheng Z, Park E, Glick BR (2007) 1-aminocyclopropane-1carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918

    Article  PubMed  CAS  Google Scholar 

  • Choi O, Kim J, Kim JG, Jeong Y, Moon JS, Park CS, Hwang I (2008) Pyrroloquinoline quinine is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol 146:657–668

    Article  PubMed  CAS  Google Scholar 

  • Cholaky L, Giayetto O, Neuman EC, Cavaignac S (1983) Respuesta del maní (Arachis hypogaea L.) a la inoculación del suelo con Rhizobium sp. Rev UNRC 3:173–179

    Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Ait Barka E (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  PubMed  CAS  Google Scholar 

  • Condon C, Philips J, Fu ZY, Squires C, Squires CL (1999) Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli. EMBO J 11:4175–4185

    Google Scholar 

  • Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071

    Article  PubMed  CAS  Google Scholar 

  • Crossman LC, Castillo-Ramírez S, McAnnula C et al (2008) A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen fixing bacteria. PLoS One 3(7):e2567

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • de Lajudie P, Willems A, Nick G, Mohamed TS, Torck U, Wlai-Maltouf A, Kersters K, Dreyfus B, Lindström K, Gillis M (1999) Agrobacterium bv. 1 strains isolated from nodules of tropical legumes. Syst Appl Microbiol 22:119–132

    Article  Google Scholar 

  • Deshwal V, Pandey P, Kang SC, Maheshwari DK (2003) Rhizobia as biological control agents against soil borne plant pathogens. Indian J Exp Biol 41:1160–1164

    PubMed  CAS  Google Scholar 

  • Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) plant growth-promoting rhizobacteria. Microbiol Res 159:371–394

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dong YM, Iniguez AL, Triplett EW (2003) Kinetics and strains specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago saltiva and Medicago truncatula. Appl Environ Microbiol 69:1783–1790

    Article  PubMed  CAS  Google Scholar 

  • Dreyden SC, Kaplan S (1990) Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res 18:7267–7277

    Article  Google Scholar 

  • Dreyfus B, Dommergues Y (1981) Nitrogen-fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata. FEMS Microbiol Lett 10:313–317

    Article  CAS  Google Scholar 

  • Duijff B, Recobert G, Bakke P, Lóper J, Lemanceau P (1999) Microbial antagonism at the root level is involved in the suppression of Fusarium wilt by the combination of nonpathogenic Fusarium oxysporum Fo47 and Pseudomonas putida WCS358. Phytopathology 89:1073–1079

    Article  PubMed  CAS  Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  PubMed  CAS  Google Scholar 

  • Fabra A, Castro S, Taurian T, Angelini J, Ibañez F, Dardanelli M, Tonelli M, Bianucci E, Valetti L (2010) Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Crit Rev Microbiol 36:179–194

    Article  PubMed  CAS  Google Scholar 

  • Ferguson B, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid D, Gresshoff P (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52:61–76

    Article  PubMed  CAS  Google Scholar 

  • Flores-Fargas RD, O’Hara GW (2006) Isolation and characterization of rhizosphere bacteria with potential for biological control of weeds in vineyards. J Appl Microbiol 100:946–954

    Article  CAS  Google Scholar 

  • Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Bet Dtsch Bot Ges 7:332–346

    Google Scholar 

  • Frankerberger WT, Arshad M (1995) Phytohormones in soil: microbial production and function. Marcel Dekker, New York

    Google Scholar 

  • Gao JL, Terefework ZD, Chen WX, Lindstrom K (2001) Genetic diversity of rhizobia isolated from Astragalus adsurgens growing in different geographical regions of China. J Biotechnol 91:155–168

    Article  PubMed  CAS  Google Scholar 

  • Gaudin V, Vrain D, Jouanin L (1994) Bacterial genes modifying hormonal balance in plant. Plant Physiol Biochem 32:11–29

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Glick BR, Patten CL, Holguin G, Penrose DM (1999) Bio-chemical and genetic mechanisms used by plant growth-promoting bacteria. Imperial College Press, London

    Book  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-containing soil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo FR, Talon M (2001) The plant growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active giberelins. Physiol Plantarum 111:206–211

    Article  Google Scholar 

  • Haas D, Keel C (2003) Regulation of antibiotic production in root colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41:117–153

    Article  PubMed  CAS  Google Scholar 

  • Hallman J, Quadt-Hallman A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    Article  Google Scholar 

  • Hallmann J, Berg G, Schulz B (2006) Isolation procedures for endophytic microorganisms. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 299–314

    Chapter  Google Scholar 

  • Hammond-Kosack KE, Jones J (1996) Resistance gene dependent plant defense responses. Plant Cell 8:1773–1791

    Article  PubMed  CAS  Google Scholar 

  • Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  PubMed  CAS  Google Scholar 

  • Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd G (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557

    Article  PubMed  CAS  Google Scholar 

  • Höfte M, Buysens S, Koedam N, Cornelis P (1993) Zinc affects siderophore mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Biometals 6:85–91

    Article  PubMed  Google Scholar 

  • Ibañez F, Fabra A (2011) Rhizobial Nod factors are required for cortical cell division in the nodule morphogenetic programme of the Aeschynomeneae legume Arachis. Plant Biol 13(5):794–800

    Article  PubMed  CAS  Google Scholar 

  • Ibañez F, Angelini J, Taurian T, Tonelli ML, Fabra A (2009) Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. Syst Appl Microbiol 32:49–55

    Article  PubMed  CAS  Google Scholar 

  • Ibañez F, Reinoso H, Fabra A (2010) Experimental evidences of pSym transfer in a native peanut-associated rhizobia. Microbiol Res 165(6):505–515

    Article  PubMed  CAS  Google Scholar 

  • Imaizumi-Anraku H, Takeda N, Kawaguchi M, Parniske M, Hayashi M, Kawasaki S (2005) Host genes involved in activation and perception of calcium spiking. Plant Cell Physiol 46:S5–S5

    Google Scholar 

  • Indrasumunar A (2007) Molecular cloning and functional characterization of soybean (Glycine max L.) nod factor receptor genes. Ph.D. thesis, The University of Queensland

    Google Scholar 

  • Indrasumunar A, Kereszt A, Searle I, Miyagi M, Li D, Nguyen CDT, Men A, Carroll BJ, Gresshoff PM (2009) Inactivation of duplicated nod-factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol. doi:10.1093/pcp/pcp178

  • Jousset A, Lara E, Wall LG, Valverde C (2006) Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHAO to escape protozoan grazing. Appl Environ Microbiol 72:7083–7090

    Article  PubMed  CAS  Google Scholar 

  • Jurkevitch E, Hadar Y, Chen Y (1986) The remedy of lime-induced chlorosis in peanuts by Pseudomonas sp. siderophores. J Plant Nutr 9:535–545

    Article  Google Scholar 

  • Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789

    Article  PubMed  CAS  Google Scholar 

  • Kan FL, Chen ZY, Wang ET, Tian CF, Sui XH, Chen WX (2007) Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Arch Microbiol 188:103–115

    Article  PubMed  CAS  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364

    Article  PubMed  CAS  Google Scholar 

  • Kang JG, Shin SY, Kim MJ, Bajpai V, Maheshwari DK, Kang SC (2004) Isolation and anti-fungal activities of 2-hydroxymethyl-chroman-4-one produced by Burkholderia sp. MSSP. J Antibiot 57(11):726–731

    Article  PubMed  CAS  Google Scholar 

  • Kevei Z, Lougnon G, Mergaert P, Horv’ath GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, Kondorosi A, Endre G, Kondorosi E, An’e JM (2007) 3-Hydroxy-3-methylglutaryl coenzyme A reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19:3974–3989

    Article  PubMed  CAS  Google Scholar 

  • Kiely PD, Haynes JM, Higgins CH, Franks A, Mark GL, Morrissey JP, O’Gara F (2006) Exploiting new systems-based strategies to elucidate plant-bacterial interactions in the rhizosphere. Microb Ecol 51:257–266

    Article  PubMed  CAS  Google Scholar 

  • Kishore GK, Pande S, Podile AR (2005) Chitin-supplemented foliar application of Serratia maecescens GPS 5 improves control of late leaf spot disease of groundnut by activating defence-related enzymes. J Phytopathol 153:19–173

    Article  Google Scholar 

  • Kloepper JW, Leong M, Teintze SMN (1980) Enhanced plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286:885–886

    Article  CAS  Google Scholar 

  • Kloepper J, Ryu C, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  PubMed  CAS  Google Scholar 

  • Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara T, Suganuma N, Kawaguchi M (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51:1381–1397

    Article  PubMed  CAS  Google Scholar 

  • Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner A, Azevedo J (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251

    Article  PubMed  CAS  Google Scholar 

  • Kuykendall LD (2005) Family I. Rhizobiaceae Conn 1938, 321 AL. In: Brenner DJ, Krieg NR, Stanley JT (eds) Bergey’s manual of systematic bacteriology, vol 2(c). Springer, New York, pp 324–361

    Google Scholar 

  • Leeman M, den Ouden F, van Pelt J, Dirkx F, Steij H, Bakker Schippers B (1996) Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149–155

    Article  CAS  Google Scholar 

  • Lei X, Wang ET, Chen WF, Sui XH, Chen WX (2008) Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate region of China. Arch Microbiol 190:657–671

    Article  PubMed  CAS  Google Scholar 

  • Li JH, Wang ET, Chen WF, Chen WX (2008) Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biol Biochem 40:238–246

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Wang ET, Chen WX (2005) Diverse rhizobia associated with woody legumes Wisteria sinensis, Cercis racemosa and Amorpha fruticosa grown in the temperate zone of China. Syst Appl Microbiol 28:465–477

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Wang ET, da Ren W, Chen WX (2010) Mixture of endophytic Agrobacterium and Sinorhizobium meliloti strains could induce nonspecific nodulation on some woody legumes. Arch Microbiol 192:229–234

    Article  PubMed  CAS  Google Scholar 

  • Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS One 3:e2702

    Article  PubMed  CAS  Google Scholar 

  • Lozano L, Hernández-González I, Bustos P, Santamaría RI, Souza V, Young JPW, Dávila G, González V (2010) Evolutionary dynamics of insertion sequences in relation to the evolutionary histories of the chromosome and symbiotic plasmid genes of Rhizobium etli populations. Appl Environ Microbiol 76:6504–6513

    Article  PubMed  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  PubMed  CAS  Google Scholar 

  • Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Mhamdi R, Laguerre G, Aouani ME, Mars M, Amarger N (2002) Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. FEMS Microbiol Ecol 41:77–84

    Article  PubMed  CAS  Google Scholar 

  • Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kalo P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, Dudas B, Vanden-Bosch K, Long SR, Cook DR, Kiss GB, Oldroyd GE (2007) An ERF transcription factor in Medicago truncatula that is essential for nod factor signal transduction. Plant Cell 19:1221–1234

    Article  PubMed  CAS  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    Article  PubMed  CAS  Google Scholar 

  • Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, Cappuccinelli P, Alberghini S, Benhizia Y, Benhizia H, Benguedouar A, Mori B, Calamassi R, Dazzo FB, Squartini A (2008) Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbial Ecol 63:383–400

    Article  CAS  Google Scholar 

  • Muresu R, Maddau G, Delogu G, Cappuccinelli P, Squartini A (2010) Bacteria colonizing root nodules of wild legumes exhibit virulence-associated properties of mammalian pathogens. Antonie Van Leeuwenhoek 97:143–153

    Article  PubMed  CAS  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Lerat E, Daubin V (2005) Examining bacterial species under the specter of gene transfer and exchange. Proc Natl Acad Sci USA 102:6595–6599

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pal KK, Dey R, Bhatt DM, Chauhan SM (2000) Plant growth promoting fluorescent pseudomonads enhanced peanut growth, yield and nutrient uptake. In: Proceedings of fifth international PGPR workshop, Carboda, Argentina, 29 Oct–2 Sept 2000

    Google Scholar 

  • Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils 46:807–816

    Article  Google Scholar 

  • Pandey P, Maheshwari DK (2007) Bioformulation of Burkholderia sp. MSSP with a multi-species consortium for growth promotion of Cajanus cajan. Can J Microbiol 53:213–222

    Article  PubMed  CAS  Google Scholar 

  • Patten CL, Glick BR (2002) The role of bacterial indole acetic acid in the development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  PubMed  CAS  Google Scholar 

  • Péchy-Tarr M, Bruck DJ, Maurhofer M, Fisher E, Vogne C, Henkels MD, Donahue KM, Grunder J, Loper JE, Keel C (2008) Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ Microbiol 10:2368–2386

    Article  PubMed  CAS  Google Scholar 

  • Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183

    Article  PubMed  CAS  Google Scholar 

  • Podile AR, Kishore GK (2006) Plant growth promoting rhizobacteria. In: Gnanamanickam SS (ed) Plant associated bacteria. Springer, Dordrecht, pp 195–230

    Chapter  Google Scholar 

  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  PubMed  CAS  Google Scholar 

  • Rai R, Dash P, Prasanna BM, Singh A (2007) Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World J Microbiol Biotechnol 23:853–858

    Article  Google Scholar 

  • Rainey FA, Ward-Rainey NL, Janssen PH, Hippe H, Stackebrandt E (1996) Clostridium paradoxum DSM 7308T contains multiple 16S rRNA genes with heterogeneous intervening sequences. Microbiology 142:2087–2095

    Article  PubMed  CAS  Google Scholar 

  • Rajendran G, Sing F, Desai AJ, Archana G (2008) Enhanced growth and nodulation of pigeon pea by co-inoculation of Bacillus strains with Rhizobium spp. Bioresour Technol 99:4544–4550

    Article  PubMed  CAS  Google Scholar 

  • Reinhold-Hurek B, Hurek T (1998a) Interactions of gramineous plants with Azoarcus spp. and other diazotrophs: identification, localization, and perspectives to study their function. Crit Rev Plant Sci 17:29–54

    Article  Google Scholar 

  • Reinhold-Hurek B, Hurek T (1998b) Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139–144

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Farmer E (1998) Jasmonate and salicylate as global signals for defence gene expression. Curr Opin Plant Biol 5:404–411

    Article  Google Scholar 

  • Riely BK, Lougnon G, Ane JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49:208–216

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21

    Article  CAS  Google Scholar 

  • Rosenblueth M, Martinez Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 181:337–344

    Article  PubMed  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wie HX et al (2003) Bacterial volatiles promote growth of Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) Nucleoporin85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624

    Article  PubMed  CAS  Google Scholar 

  • Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195

    Article  PubMed  CAS  Google Scholar 

  • Sen D, Weaver RW (1984) A basis for different rates of N2-fixation by the same strain of Rhizobium in peanut and cowpea root nodules. Plant Sci Lett 34:239–246

    Article  CAS  Google Scholar 

  • Siddiqui S, Siddiqui ZA, Iqbal A (2005) Evaluation of fluorescent pseudomonads and Bacillus isolates for the biocontrol of wilt disease complex of pigeon pea. World J Microbiol Biotechol 21:729–732

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Smit P, Raedts J, Portyanko V, Debellè F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791

    Article  PubMed  CAS  Google Scholar 

  • Stajković O, De Meyer S, Miličić B, Willems A, Delić D (2009) Isolation and characterization of endophytic non-rhizobial bacteria from root nodules of alfalfa (Medicago sativa L.). Bot Serb 33:107–114

    Google Scholar 

  • Steinsham H, Thuen E, Beken MA, Brenoe UT, Ekerholt G, Yri C (2004) Utilization of nitrogen (N) and phosphorus (P) in an organic dairy farming system in Norway. Agric Ecosyst Environ 104:509–522

    Article  CAS  Google Scholar 

  • Stevenson FJ, Cole MA (1999) Cycles of soil: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, New York

    Google Scholar 

  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both fungal and bacterial symbiosis. Nature 417:959–962

    Article  PubMed  CAS  Google Scholar 

  • Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30

    Article  Google Scholar 

  • Subba-Rao NS, Mateos P, Baker D, Stuart Pankratz H, Palma J, Dazzo F, Sprent J (1995) The unique root-nodule symbiosis between Rhizobium and the aquatic legume Neptunia natans (L.f.) Druce. Planta 2:311–320

    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 

  • Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95:5145–5149

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JT, Trzebiatowski JR, Cruickshank RW et al (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184:3086–3095

    Article  PubMed  CAS  Google Scholar 

  • Taurian T, Aguilar OM, Fabra A (2002) Characterization of nodulating peanut rhizobia isolated from a native soil population in Córdoba, Argentina. Symbiosis 33:59–72

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Ludueña L, Pena D, Ibáñez F, Fabra A (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431

    Article  CAS  Google Scholar 

  • Timmers AC, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628

    PubMed  CAS  Google Scholar 

  • Timmusk S, Wagner EG (1999) The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant Microbe Interact 12:951–959

    Article  PubMed  CAS  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107

    Article  PubMed  CAS  Google Scholar 

  • Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171

    Article  PubMed  CAS  Google Scholar 

  • Tonelli ML, Taurian T, Ibáñez F, Angelini J, Fabra A (2010) Selection and in vitro characterization of bioantagonistic activities in peanut associated bacteria. J Plant Pathol 92:73–82

    Google Scholar 

  • Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E, Alonso P, Martínez-Molina E (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 4:1265–1281

    Article  PubMed  Google Scholar 

  • Turner JA, Rice EL (1975) Microbial decomposition of ferulic acid in soil. J Chem Ecol 1:41–58

    Article  CAS  Google Scholar 

  • Ude S, Arnold DL, Moon CD, Timms-Wilson T, Spiers AJ (2006) Biofilm formation and cellulose expression among diverse environmental Pseudomonads isolates. Environ Microbiol 8:1997–2011

    Article  PubMed  CAS  Google Scholar 

  • Van Berkum P, Terefework Z, Paulin L, Suomalainen S, Lindström K, Eardly BD (2003) Discordant Phylogenies within the rrn Loci of Rhizobia. J Bacteriol 185:2988–2998

    Article  PubMed  CAS  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  CAS  Google Scholar 

  • Van Loon LC, Bakker PAHM (2003) Signalling in rhizobacteria-plant interactions. In: De Kroon H, Visser EJW (eds) Root ecology, vol 168, Ecological studies. Springer, Berlin, pp 297–330

    Google Scholar 

  • Van Loon LC, Bakker PAHM (2006) Root-associated bacteria inducing systemic resistance. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 269–316

    Chapter  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728–734

    Article  Google Scholar 

  • Van Rossum D, Muyotcha A, Van Verseveld HW, Stouthamer AH, Boogerd FC (1993) Effects of Bradyrhizobium strain and host genotype, nodule dry weight and leaf area on groundnut (Arachis hypogaea L. ssp. fastigiata) yield. Plant Soil 154:279–288

    Article  Google Scholar 

  • Vargas R, Ramirez C (1989) Respuesta de la soya y el maní a Rhizobium y a la fertilización con N, P y Mo en un Tepic pellustert de cañas, Guanacaste. Agronomía Costarricense 13:175–182

    Google Scholar 

  • Verma JP, Yadav J, Yiwari KN, Lavakush SV (2010) Impact of plant growth promoting rhizobacteria on crop production. Int J Agric Res 5:954–983

    Article  Google Scholar 

  • Vessey KJ (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil, 255:571–586

    Article  CAS  Google Scholar 

  • Volkmar KM, Bremer E (1998) Effects of seed inoculation with a strain of Pseudomonas fluorescens on root growth and activity of wheat in well-watered and drought-stressed glass-fronted rhizotrons. Can J Plant Sci 78:545–551

    Article  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    Article  PubMed  CAS  Google Scholar 

  • Wang ET, Tan ZY, Guo XW, Rodríguez-Duran R, Boll G, Martínez-Romero E (2006) Diverse endophytic bacteria isolated from a leguminous tree Conzattia multiflora grown in Mexico. Arch Microbiol 186:251–259

    Article  PubMed  CAS  Google Scholar 

  • Weir BS (2010) The current taxonomy of rhizobia. New Zealand rhizobia website. http://www.rhizobia.co.nz/taxonomy/rhizobia.html. Last updated 21 Oct 2010

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256

    Article  PubMed  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Tang F, Gao M, Krishnan H, Zhu H (2010) R gene-controlled host specificity in the legume–rhizobia symbiosis. Proc Natl Acad Sci USA. doi:0.1073/pnas.1011957107

  • Zakhia F, Jeder H, Willems A, Gillis M, Dreyfus B, de Lajudie P (2006) Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb Ecol 51:375–393

    Article  PubMed  Google Scholar 

  • Zakria M, Njoloma J, Saeki Y, Akao S (2007) Colonization and nitrogen fixing ability of Herbaspirillum sp. strain B501 gfp1 and assessment of its growth promoting ability in cultivated rice. Microbes Environ 22:197–206

    Article  Google Scholar 

  • Zhukov V, Radutoiu S, Madsen LH, Rychagova T, Ovchinnikova E, Borisov A et al (2008) The pea sym37 receptor kinase gene controls infection-thread initiation and nodule development. Mol Plant Microbe Interact 21:1600–1608

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

The authors are indebted to UNRC, CONICET, ANPCYT, Ministerio de Ciencia y Tecnología de Córdoba (Argentina) that are currently supporting our research or did so in the past.

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  1. Dpto. Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto (UNRC), Río Cuarto, Córdoba, Argentina

    Tania Taurian, Fernando Ibáñez, Jorge Angelini, María Laura Tonelli & Adriana Fabra

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  1. Tania Taurian
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  2. Fernando Ibáñez
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  3. Jorge Angelini
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Correspondence to Adriana Fabra .

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  1. Dept. of Botany Microbiology, Gurukul Kangri Univ., Haridwar (U.K.), 249404, India

    Dinesh K. Maheshwari

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Taurian, T., Ibáñez, F., Angelini, J., Tonelli, M.L., Fabra, A. (2012). Endophytic Bacteria and Their Role in Legumes Growth Promotion. In: Maheshwari, D. (eds) Bacteria in Agrobiology: Plant Probiotics. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27515-9_8

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