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Potential of Rhizobia as Plant Growth-Promoting Rhizobacteria

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Microbes for Legume Improvement

Abstract

Nitrogen-fixing plant growth-promoting rhizobacteria collectively known as rhizobia have been extensively investigated due to their exceptional quality to establish functional symbiosis with legumes. As a result of this incredible interaction, they supply nitrogen to plants, which is one of the major nutrient elements. Rhizobia are capable of colonizing the rhizosphere of nonhost plants (nonlegumes) thus living within plant tissues as endophytes. Due to these properties and their ability to secrete phytohormones and siderophores, and solubilize insoluble phosphate, besides eliciting plant defense reactions against phytopathogens, rhizobia have been placed along the organisms with high potential to act as efficient plant growth-promoting rhizobacteria (PGPR). Here, the mechanisms adopted by rhizobia to facilitate plant growth and yields are highlighted. In addition, the application of rhizobia as PGPR in farming practices is underlined. The information available on rhizobial application and the number of rhizobia stored in different culture collection centers around the world may provide an important microbiological resource to reduce the use of expensive synthetic fertilizers and pesticides in agricultural practices.

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References

  • Abd-Alla MH (1994a) Use of organic phosphorus by Rhizobium leguminosarum biovar. viceae phosphatases. Biol Fertil Soils 18:216–218

    Article  CAS  Google Scholar 

  • Abd-Alla MH (1994b) Phosphatases and the utilization of organic phosphorus by Rhizobium leguminosarum biovar viceae. Lett Appl Microbiol 18:294–296

    Article  CAS  Google Scholar 

  • Adesemoye AO, Ugoji EO (2009) Evaluating Pseudomonas aeruginosa as plant growth-promoting rhizobacteria in West Africa. Arch Phytopathol Plant Prot 42:188–200

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2009) Effect of insecticide-tolerant and plant growth-promoting Mesorhizobium on the performance of chickpea grown in insecticide stressed alluvial soils. J Crop Sci Biotech 12:213–222

    Article  Google Scholar 

  • Ahemad M, Khan MS (2010) Comparative toxicity of selected insecticides to pea plants and growth promotion. Crop Protect. doi:10.1016/j.cropro.2010.01.005

  • Ahmad E, Khan MS, Zaidi A (2013) ACC deaminase producing Pseudomonas putida strain PSE3 and Rhizobium leguminosarum strain RP2 in synergism improves growth, nodulation and yield of pea grown in alluvial soils. Symbiosis 61:93–104

    Article  CAS  Google Scholar 

  • Alikhani H, Saleh-Rastin N, Antoun H (2007) Phosphate solubilization activity of rhizobia native to Iranian soils. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Springer, Dordrecht, pp 35–41

    Chapter  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 

  • Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027–1046

    Article  CAS  PubMed  Google Scholar 

  • Barrett CF, Parker MA (2006) Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol 72:1198–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batista JSS, Hungria M, Barcellos FG, Ferreira MC, Mendes IC (2007) Variability in Bradyrhizobium japonicum and B. elkanii seven years after introduction of both the exotic microsymbiont and the soybean host in a Cerrados soil. Microb Ecol 53:270–284

    Article  PubMed  Google Scholar 

  • Bhagat D, Sharma P, Sirari A, Kumawat KC (2014) Screening of Mesorhizobium spp. for control of Fusarium wilt in chickpea in vitro conditions. Int J Curr Microbiol Appl Sci 3:923–930

    Google Scholar 

  • Bhattacharjee RB, Jourand P, Chaintreuil C, Dreyfus B, Singh A, Mukhopadhyay SN (2012) Indole acetic acid and ACC deaminase-producing Rhizobium leguminosarum bv. trifolii SN10 promote rice growth, and in the process undergo colonization and chemotaxis. Bio Fert Soils 48:173–182

    Article  CAS  Google Scholar 

  • Biswas J, Ladha J, Dazzo F (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650

    Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880

    Article  CAS  PubMed  Google Scholar 

  • Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GE (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cattelan A, Hartel P, Fuhrmann J (1999) Screening for plant growth–promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1680

    Article  CAS  Google Scholar 

  • Chabot R, Antoun H, Kloepper JW, Beauchamp CJ (1996) Root colonization of maize and lettuce by bioluminescent Rhizobium leguminosarum biovar phaseoli. Appl Environ Microbiol 62:2767–2772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chacon N, Silver WL, Dubinsky EA, Cusack DF (2006) Iron reduction and soil phosphorus solubilization in humid tropical forests soils: the roles of labile carbon pools and an electron shuttle compound. Biogeochemistry 78:67–84

    Article  CAS  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 

  • Chakraborty U, Purkayastha R (1984) Role of rhizobitoxine in protecting soybean roots from Macrophomina phaseolina infection. Can J Microbiol 30:285–289

    Article  CAS  PubMed  Google Scholar 

  • Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobiumloti 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 

  • Chao WL (1990) Antagonistic activity of Rhizobium spp. against beneficial and plant pathogenic fungi. Lett Appl Microbiol 10:213–215

    Article  Google Scholar 

  • Chen W-M, De Faria SM, James EK, Elliott GN, Lin K-Y, Chou J-H, Sheu S-Y, Cnockaert M, Sprent JI, Vandamme P (2007) Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol 57:1055–1059

    Article  CAS  PubMed  Google Scholar 

  • Chen N, Jin M, Qu HM, Chen ZQ, Chen ZL, Qiu ZG, Wang XW, Li JW (2012) Isolation and characterization of Bacillus sp. producing broad-spectrum antibiotics against human and plant pathogenic fungi. J Microbiol Biotechnol 22:256–563

    Article  CAS  PubMed  Google Scholar 

  • Chi F, Shen S-H, Cheng H-P, Jing Y-X, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cladera-Olivera F, Caron GR, Motta AS, Souto AA, Brandelli A (2006) Bacteriocin-like substance inhibits potato soft rot caused by Erwinia carotovora. Can J Microbiol 52:533–539

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Contesto C, Desbrosses G, Lefoulon C, Béna G, Borel F, Galland M, Gamet L, Varoquaux F, Touraine B (2008) Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci 175:178–189

    Article  CAS  Google Scholar 

  • Datta B, Chakrabartty PK (2014) Siderophore biosynthesis genes of Rhizobium sp. isolated from Cicer arietinum L. 3 Biotech 4:391–401

    Article  PubMed  Google Scholar 

  • Dazzo FB, Yanni YG (2006) The natural Rhizobium-cereal crop association as an example of plant-bacterial interaction. In: Uphoff N, Ball AS, Fernandes E, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P, Sanginga N, Thies J (eds) Biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 109–127

    Chapter  Google Scholar 

  • Deshwal V, Dubey R, Maheshwari D (2003) Isolation of plant growth-promoting strains of Bradyrhizobium (Arachis) sp. with biocontrol potential against Macrophomina phaseolina causing charcoal rot of peanut. Curr Sci 84:443–448

    Google Scholar 

  • Diep CN, So DB, Trung NB, Lam PVH (2016) Effects of rhizobia and phosphate-solubilizing bacteria on soybean (Glycine max L. Merr.) cultivated on ferralsols of Daklak Province, Vietnam. Int J Pharm Pharm Sci 5:318–333

    CAS  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 

  • Dobert RC, Rood SB, Blevins DG (1992) Gibberellins and the legume-Rhizobium symbiosis: I. Endogenous gibberellins of Lima Bean (Phaseolus lunatus L.) stems and nodules. Plant Physiol 98:221–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domit L, Costa J, Vidor C, Pereira J (1990) Inoculation of cereal seeds with Bradyrhizobium japonicum and its effect on soyabeans grown in succession. R Bras Ci Solo 14:313–319

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dutta S, Mishra A, Kumar BD (2008) Induction of systemic resistance against fusarial wilt in pigeon pea through interaction of plant growth promoting rhizobacteria and rhizobia. Soil Biol Biochem 40:452–461

    Article  CAS  Google Scholar 

  • Elbadry M, Taha R, Eldougdoug K, Gamal-Eldin H (2006) Induction of systemic resistance in faba bean (Vicia faba L.) to bean yellow mosaic potyvirus (BYMV) via seed bacterization with plant growth promoting rhizobacteria. J Plant Dis Protect 113:247–251

    Article  Google Scholar 

  • Ferguson L, Lessenger JE (2006) Plant growth regulators. In: Lessenger JE (ed) Agricultural medicine. Springer, New York, pp 156–166

    Chapter  Google Scholar 

  • Ferguson BJ, Ross JJ, Reid JB (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol 138:2396–2405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernando WD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964

    Article  CAS  Google Scholar 

  • Flores-Félix JD, Menéndez E, Rivera LP, Marcos-García M, Martínez-Hidalgo P, Mateos PF, Martínez-Molina E, Velázquez ME, García-Fraile P, Rivas R (2013) Use of Rhizobium leguminosarum as a potential biofertilizer for Lactuca sativa and Daucus carota crops. J Plant Nutr Soil Sci 176:876–882

    Article  CAS  Google Scholar 

  • Foster RC (1998) Microenvironments of soil microorganisms. Bio Fert Soils 6:189–203

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gandhi PM, Narayanan K, Naik P, Sakthivel N (2009) Characterization of Chryseobacterium aquaticum strain PUPC1 producing a novel antifungal protease from rice rhizosphere soil. J Microbiol Biotechnol 19:99–107

    CAS  Google Scholar 

  • García-Fraile P, Carro L, Robledo M, Ramírez-Bahena MH, Flores-Félix JD, 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 7:38122

    Article  CAS  Google Scholar 

  • Ghosh PK, Kumar De T, Maiti TK (2015) Production and metabolism of indole acetic acid in root nodules and symbiont (Rhizobium undicola) isolated from root nodule of aquatic medicinal legume Neptunia oleracea Lour. J Bot 2015. Article ID 575067

    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  CAS  PubMed  Google Scholar 

  • Glick BR, Liu C, Ghosh S, Dumbroff EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239

    Article  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  CAS  PubMed  Google Scholar 

  • Gray E, Smith D (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hafeez F, Safdar M, Chaudhry A, Malik K (2004) Rhizobial inoculation improves seedling emergence, nutrient uptake and growth of cotton. Anim Prod Sci 44:617–622

    Article  Google Scholar 

  • Hafeez FY, Naeem FI, Naeem R, Zaidi AH, Malik KA (2005) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv. viciae isolated from agriculture soils in Faisalabad. Environ Exp Bot 54:142–147

    Article  CAS  Google Scholar 

  • Hayashi S, Gresshoff PM, Ferguson BJ (2014) Mechanistic action of gibberellins in legume nodulation. J Integr Plant Biol 56:971–978

    Article  CAS  PubMed  Google Scholar 

  • Hemissi I, Mabrouk Y, Abdi N, Bouraoui M, Saidi M, Sifi B (2011) Effects of some Rhizobium strains on chickpea growth and biological control of Rhizoctonia solani. Afr J Microbiol Res 5:4080–4090

    CAS  Google Scholar 

  • Hossain MS, Mårtensson A (2008) Potential use of Rhizobium spp. to improve fitness of non-nitrogen-fixing plants. Acta Agric Scand 58:352–358

    Google Scholar 

  • Hungria M, Campo R (2005) Fixação biológica do nitrogênio em sistemas agrícolas. In: Congresso brasileiro de ciência do solo. SBCS, UFPE Embrapa Solos Pernambuco Rio de Janeiro

    Google Scholar 

  • Imen H, Neila A, Adnane B, Manel B, Mabrouk Y, Saidi M, Bouaziz S (2015) Inoculation with phosphate solubilizing Mesorhizobium strains improves the performance of chickpea (Cicer aritenium L.) under phosphorus deficiency. J Plant Nutr 38:1656–1671

    Article  CAS  Google Scholar 

  • Kacem M, Kazouz F, Merabet C, Rezki M, de Lajudie P, Bekki A (2009) Antimicrobial activity of Rhizobium sp. strains against Pseudomonas savastanoi, the agent responsible for the olive knot disease in Algeria. Grasas Aceites 60:139–146

    Article  Google Scholar 

  • Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, Wirthner P, Haas D, Defago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHAO: importance of bacterial secondary metabolite, 2,4-diacetylphoroglucinol. Mol Plant Microbe Interact 5:4–13

    Article  CAS  Google Scholar 

  • Khaitov B, Kurbonov A, Abdiev A, Adilov M (2016) Effect of chickpea in association with Rhizobium to crop productivity and soil fertility. Eurasian J Soil Sci 5:105–112

    Article  Google Scholar 

  • Khan M, Zaidi A, Wani P (2009) Role of phosphate solubilizing microorganisms in sustainable agriculture – a review. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer, Netherlands, pp 551–570. doi:10.1007/978-90-481-2666-8_34

    Chapter  Google Scholar 

  • Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi–current perspective. Arch Agron Soil Sci 56:73–98

    Article  CAS  Google Scholar 

  • Kloepper JW (1978) Schroth MN Plant growth-promoting rhizobacteria on radishes. In: Proceedings of the fourth international conference on plant pathogenic bacteria, pp 879–882

    Google Scholar 

  • Kloepper JA (2003) Review of mechanisms for plant growth promotion by PGPR. In: Sixth international PGPR workshop, pp 5–10

    Google Scholar 

  • Kloepper JW, Beauchamp CJ (1992) A review of issues related to measuring colonization of plant roots by bacteria. Can J Microbiol 38:1219–1232

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kumar G, Raghu Ram M (2014) Phosphate solubilizing rhizobia isolated from Vigna trilobata. Am J Microbiol Res 2:105–109

    Article  Google Scholar 

  • LA Favre JS, Eaglesham ARJ (1986) Rhizobitoxine: a phytotoxin of unknown function which is commonly produced by bradyrhizobia. Plant Soil 92:443–452

    Article  CAS  Google Scholar 

  • Lievens S, Goormachtig S, Den Herder J, Capoen W, Mathis R, Hedden P, Holsters M (2005) Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol 139:1366–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindström K, Martinez-Romero M (2005) International Committee on Systematics of Prokaryotes; Subcommittee on the taxonomy of Agrobacterium and Rhizobium Minutes of the meeting, 26 July 2004, Toulouse, France. Int J Syst Evol Microbiol 55:1383–1383

    Article  Google Scholar 

  • Loper J, Schroth M (1986) Influence of bacteria sources of indol-3-acetic acid on root elongation of sugar beet. Phytopathol 76:386–389

    Article  CAS  Google Scholar 

  • López-López A, Rogel MA, Ormeno-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327

    Article  PubMed  Google Scholar 

  • Lukkani NJ, Reddy ECS (2014) Evaluation of plant growth promoting attributes and biocontrol potential of native fluorescent pseudomonas spp. against Aspergillus niger causing collar rot of ground nut. Int J Plant Anim Environ Sci 4:267–262

    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 

  • Machado RG, Sá ELS, Bruxel M, Giongo A, Santos NS, Nunes AS (2013) Indoleacetic acid producing rhizobia promote growth of Tanzania grass (Panicum maximum) and Pensacola grass (Paspalum saurae). Int J Agric Biol 15:827–834

    CAS  Google Scholar 

  • Matthijs S, Tehrani KA, Laus G, Jackson RW, Cooper RM, Cornelis P (2007) Thioquinolobactin, a Pseudomonas siderophore with antifungal and anti-Pythium activity. Environ Microbiol 9:425–434

    Article  CAS  PubMed  Google Scholar 

  • Messele B, Pant LM (2012) Effects of inoculation of Sinorhizobium ciceri and phosphate solubilizing bacteria on nodulation, yield and nitrogen and phosphorus uptake of chickpea (Cicer arietinum L.) in Shoa Robit Area. J Biofertil Biopestici 3:129

    Article  Google Scholar 

  • Minamisawa K (1990) Division of rhizobitoxine-producing and hydrogen-uptake positive strains of Bradyrhizobium japonicum by nifDKE sequence divergence. Plant Cell Physiol 31:81–89

    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 RP, 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 

  • Muthuselvan I, Balagurunathan R (2013) Siderophore production from Azotobacter sp. and its application as biocontrol agent. Int J Curr Res Rev 5:23–35

    Google Scholar 

  • Nabti E, Bensidhoum L, Tabli N, Dahel D, Weiss A, Rothballer M, Schmid M, Hartman A (2014) Growth inhibition of barley and biocontrol effect on plant pathogenic fungi by a Cellulosimicrobium isolated from salt affected rhizosphere soil in northwestern Algeria. Eur J Soil Biol 61:20–26

    Article  CAS  Google Scholar 

  • Nandi A, Sengupta B, Sen S (1982) Utility of Rhizobium in the phyllosphere of crop plants in nitrogen-free sand culture. J Agric Sci 98:167–171

    Article  Google Scholar 

  • O'hara GW, Goss TJ, Dilworth MJ, Glenn AR (1989) Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Appl Environ Microbiol 55:1870–1876

    PubMed  PubMed Central  Google Scholar 

  • Okazaki S, Sugawara M, Yuhashi K-I, Minamisawa K (2007) Rhizobitoxine-induced chlorosis occurs in coincidence with methionine deficiency in soybeans. Ann Bot 100:55–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omar S, Abd-Alla M (1998) Biocontrol of fungal root rot diseases of crop plants by the use of Rhizobia and Bradyrhizobia. Folia Microbiol 43:431–437

    Article  CAS  Google Scholar 

  • Panhwar QA, Naher UA, Jusop S, Othman R, Latif MA, Ismail MR (2014) Biochemical and molecular characterization of potential phosphate solubilizing bacteria in acid sulphate soils and their beneficial effects on rice growth. PLoS One 9:e97241

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peix A, Rivas-Boyero A, Mateos P, Rodriguez-Barrueco C, Martınez-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 

  • Prabhavati E, Anthony J (2012) Bacteriocin production by rhizobia isolated from root nodules of Horse gram. Bangladesh J Med Sci 11:28–32

    Article  Google Scholar 

  • Prasad JS, Reddy RS, Reddy PN, Rajashekar AU (2014) Isolation, screening and characterization of Azotobacter from rhizospheric soils for different plant growth promotion (PGP) & antagonistic activities and compatibility with agrochemicals: an in vitro study. Ecol Environ Conserv 20:959–966

    Google Scholar 

  • Prashar P, Kapoor N, Sachdeva S (2014) Rhizosphere: its structure, bacterial diversity and significance. Rev Environ Sci Biol 13:63–77

    Article  CAS  Google Scholar 

  • Prayitno J, Stefaniak J, McIver J, Weinman J, Dazzo F, Ladha J, Barraquio W, Yanni Y, Rolfe B (1999) Interactions of rice seedlings with bacteria isolated from rice roots. Funct Plant Biol 26:521–535

    Google Scholar 

  • Probanza A, Lucas J, Acero N, Mañero FG (1996) The influence of native rhizobacteria on European alder (Alnus glutinosa (L.) Gaertn.) growth. Plant Soil 182:59–66

    Article  CAS  Google Scholar 

  • Probanza A, Mateos J, García JL, Ramos B, De Felipe M, Mañero FG (2001) Effects of inoculation with PGPR Bacillus and Pisolithus tinctorius on Pinus pinea L. growth, bacterial rhizosphere colonization, and mycorrhizal infection. Microb Ecol 41:140–148

    Article  CAS  PubMed  Google Scholar 

  • Rao SSR, Vardhini BV, Sujatha E, Anuradha S (2002) Brassinosteroids – a new class of phytohormones. Curr Sci 82:1239–1245

    Google Scholar 

  • Recep K, Fikrettin S, Erkol D, Cafer E (2009) Biological control of the potato dry rot caused by Fusarium species using PGPR strains. Biol Control 50:194–198

    Article  Google Scholar 

  • Reimann S, Hauschild R, Hildebrandt U, Sikora RA (2008) Interrelationships between Rhizobium etli G12 and Glomus intraradices and multitrophic effects in the biological control of the root-knot nematode Meloidogyne incognita on tomato. J Plant Dis Protect 115:108–113

    Article  Google Scholar 

  • Richardson A, Hadobas P, Simpson R (2001) Phytate as a source of phosphorus for the growth of transgenic Trifolium subterraneum. In: Horst WJ, Schenk MK, Bürkert A, Claassen N, Flessa H, Frommer WB, Goldbach H, Olfs HW, Römheld V, Sattelmacher B, Schmidhalter U, Schubert S, Wirén NV, Wittenmayer L (eds) Plant nutrition. Springer, Netherlands, pp 560–561

    Chapter  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Google Scholar 

  • Rogers NJ, Carson KC, Glenn AR, Dilworth MJ, Hughes MN, Poole RK (2001) Alleviation of aluminum toxicity to Rhizobium leguminosarum bv. viciae by the hydroxamate siderophore vicibactin. Biometals 14:59–66

    Article  CAS  PubMed  Google Scholar 

  • Roy N, Chakrabartty PK (2000) Effect of aluminum on the production of siderophore by Rhizobium sp. (Cicer arietinum). Curr Microbiol 41:5–10

    Article  CAS  PubMed  Google Scholar 

  • Ruangsanka S (2014) Identification of phosphate-solubilizing fungi from the asparagus rhizosphere as antagonists of the root and crown rot pathogen Fusarium oxysporum. Science Asia 40:16–20

    Article  Google Scholar 

  • Sabry SR, Saleh SA, Batchelor CA, Jones J, Jotham J, Webster G, Kothari SL, Davey MR, Cocking EC (1997) Endophytic establishment of Azorhizobium caulinodans in wheat. Proc R Soc Lon B 264:341–346

    Article  Google Scholar 

  • Sahasrabudhe MM (2011) Screening of rhizobia for indole acetic acid production. Ann Biol Res 2:460–468

    CAS  Google Scholar 

  • Sahgal M, Johri B (2003) The changing face of rhizobial systematics. Curr Sci 84:43–48

    Google Scholar 

  • Sangeetha G, Thangavelu R, Usha Rani S, Muthukumar A, Udayakumar R (2010) Induction of systemic resistance by mixtures of antagonist bacteria for the management of crown rot complex on banana. Acta Physiol Plant 32:1177–1187

    Article  Google Scholar 

  • Saravanakumar D, Kumar CV, Kumar N, Samiyappan R (2007) PGPR-induced defense responses in the tea plant against blister blight disease. Crop Protect 26:556–565

    Article  Google Scholar 

  • Schlindwein G, Vargas LK, Lisboa BB, Azambuja AC, Granada CE, Gabiatti NC, Prates F, Stumpf R (2008) Influence of rhizobial inoculation on seedling vigor and germination of lettuce. Cienc Rural 38:658–664

    Article  Google Scholar 

  • Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Höflich G, Hartmann A (1997) Root colonization of different plants by plant-growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63:2038–2046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sivasakthivelan P, Saranraj P (2013) Azospirillum and its formulations: a review. Int J Microbiol Res 4:275–287

    Google Scholar 

  • Solano BR, Maicas JB, FJG M (2008) Physiological and molecular mechanisms of plant growth promoting rhizobacteria (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant-bacteria interactions: strategies and techniques to promote plant growth. Wiley, Weinheim, Germany, pp 41–52

    Chapter  Google Scholar 

  • Sturtevant DB, Taller BJ (1989) Cytokinin Production by Bradyrhizobium japonicum. Plant Physiol 89:1247–1252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Susilowati LE, Syekhfani S (2014) Characterization of phosphate solubilizing bacteria isolated from Pb contaminated soils and their potential for dissolving tricalcium phosphate. J Degrad Mining Lands Manag 1:57–62

    Google Scholar 

  • Suzuki A, Akune M, Kogiso M, Imagama Y, Osuki K-i, Uchiumi T, Higashi S, Han S-Y, Yoshida S, Asami T (2004) Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol 45:914–922

    Article  CAS  PubMed  Google Scholar 

  • Tagore GS, Namdeo SL, Sharma SK, Kumar N (2013) Effect of Rhizobium and phosphate solubilizing bacterial inoculants on symbiotic traits, nodule leghemoglobin, and yield of chickpea genotypes. Int J Agron 2013. Article ID 581627

    Google Scholar 

  • Tominaga A, Nagata M, Futsuki K, Abe H, Uchiumi T, Abe M, Kucho K-i, Hashiguchi M, Akashi R, Hirsch A (2010) Effect of abscisic acid on symbiotic nitrogen fixation activity in the root nodules of Lotus japonicus. Plant Signal Behav 5:440–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vardhini BV, Ram Rao SS (1999) Effect of brassionosteriods on nodulation and nitrogenase activity in groundnut (Arachis hypogaea L.) Plant Growth Regul 28:165–167

    Article  CAS  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 

  • Vershinina Z, Baimiev AK, Blagova D, Knyazev A, Baimiev AK, Chemeris A (2011) Bioengineering of symbiotic systems: Creation of new associative symbiosis with the use of lectins on the example of tobacco and oil seed rape. Appl Biochem Microbiol 47:304–310

    Article  CAS  Google Scholar 

  • Vershinina ZR, Baymiev AK, Blagova DK, Chubukova OV, Baymiev AK, Chemeris AV (2012) Artificial colonization of non-symbiotic plants roots with the use of lectins. Symbiosis 56:25–33

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang TL, Wood EA, Brewin NJ (1982) Growth regulators, and nodulation in peas. The cytokinin content of a wild type and a Ti plasmid containing strain of R. leguminosarum. Planta 155:350–355

    Article  CAS  PubMed  Google Scholar 

  • Warda A, Zoubida B-h, Faiza BZ, Yamina A, Bekki A (2014) Selection and characterization of inhibitor agents (bacteriocin like) produced by rhizobial strains associated to Medicago in western Algeria. Int J Agric Crop Sci 7:393

    CAS  Google Scholar 

  • Weir B (2016) The current taxonomy of rhizobia. New Zealand rhizobia website. http://www.rhizobia.co.nz/taxonomy/rhizobia.html. Accessed 22 Jan 2016

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

    Article  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  CAS  PubMed  Google Scholar 

  • Yanni YG, Rizk R, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stoltzfus J, Buckley D (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 

  • Yanni YG, Rizk RY, El-Fattah FKA, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Funct Plant Biol 28:845–870

    Article  CAS  Google Scholar 

  • Yu X, Liu X, Zhu T, Liu G, Mao C (2012) Co-inoculation with phosphate-solubilzing and nitrogen-fixing bacteria on solubilization of rock phosphate and their effect on growth promotion and nutrient uptake by walnut. Euro J Soil Biol 50:112–117

    Article  CAS  Google Scholar 

  • Yuhashi K, Ichikawa N, Ezura H, Akao S, Minakawa Y, Nukui N, Yasuta T, Minamisawa K (2000) Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Appl Environ Microbiol 66:PMC110596

    Article  Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M, Wani P (2009) Recent advances in plant growth promotion by phosphate-solubilizing microbes. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer, Berlin, Heidelberg, pp 23–50

    Chapter  Google Scholar 

  • Zaidi A, Ahmad E, Khan MS, Saif S, Rizvi A (2015) Role of plant growth promoting rhizobacteria in sustainable production of vegetables: current perspective. Sci Hort 193:231–239

    Article  Google Scholar 

  • Ziaf K, Latif U, Amjad M, Shabir MZ, Asghar W, Ahmed S, Ahmad I, Jahangir MM, Anwar W (2016) Combined use of microbial and synthetic amendments can improve radish (Raphanus sativus) yield. J Environ Agric Sci 6:10–15

    Google Scholar 

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Vargas, L.K., Volpiano, C.G., Lisboa, B.B., Giongo, A., Beneduzi, A., Passaglia, L.M.P. (2017). Potential of Rhizobia as Plant Growth-Promoting Rhizobacteria. In: Zaidi, A., Khan, M., Musarrat, J. (eds) Microbes for Legume Improvement. Springer, Cham. https://doi.org/10.1007/978-3-319-59174-2_7

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