Skip to main content

Advertisement

SpringerLink
Log in

Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The potential of nitrogen-fixing (NF) bacteria to form a symbiotic relationship with leguminous plants and fix atmospheric nitrogen has been exploited in the field to meet the nitrogen requirement of the latter. This phenomenon provides an alternative to the use of the nitrogenous fertiliser whose excessive and imbalanced use over the decades has contributed to green house emission (N2O) and underground water leaching. Recently, it was observed that non-leguminous plants like rice, sugarcane, wheat and maize form an extended niche for various species of NF bacteria. These bacteria thrive within the plant, successfully colonizing roots, stems and leaves. During the association, the invading bacteria benefit the acquired host with a marked increase in plant growth, vigor and yield. With increasing population, the demand of non-leguminous plant products is growing. In this regard, the richness of NF flora within non-leguminous plants and extent of their interaction with the host definitely shows a ray of hope in developing an ecofriendly alternative to the nitrogenous fertilisers. In this review, we have discussed the association of NF bacteria with various non-leguminous plants emphasizing on their potential to promote host plant growth and yield. In addition, plant growth-promoting traits observed in these NF bacteria and their mode of interaction with the host plant have been described briefly.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp.. Biol Fert Soils 30:485–491

    Google Scholar 

  • Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 70:7246–7252

    Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000a) Rhizobial inoculation influences seedling vigor and yield of rice. Agronomy J 92:880–886

    Google Scholar 

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

    CAS  Google Scholar 

  • Boddey RM, Oliveira OCD, Urquiaga S, Reis VM, Olivares FLD, Baldani VLD, Döbereiner J (1995) Biological nitrogen fixation associated with sugarcane and rice: contributions and prospects for improvement. Plant Soil 174:195–209

    CAS  Google Scholar 

  • Bueno dos Reis Junior F, Massena Reis V, Urquiaga S, Döbereiner J (2000) Influence of nitrogen fertilisation on the population of diazotrophic bacteria Herbaspirillum spp. and Acetobacter diazotrophicus in sugar cane (Saccharum spp.). Plant Soil 219:153–159

    Google Scholar 

  • Cavalcante J, Vargas C, Nogueira E, Vinagre E, Schwarcz K, Baldani J, Ferreira P, Hemerly A (2007) Members of the ethylene signalling pathway are regulated in sugarcane during the association with nitrogen-fixing endophytic bacteria. J Exp Bot 58:673–686

    CAS  PubMed  Google Scholar 

  • Chaintreuil C, Giraud E, Prin Y, Lorquin J, Ba 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chi F, Shen S-H, Cheng H-P, Jing J-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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conn VM, Franco CMM (2004) The effect of microbial inoculants on the indigenous actinobacterial endophyte population present in the roots of wheat as determined by terminal restriction fragment length polymorphism (T-RFLP). Appl Environ Microbiol 70:6407–6413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dalton DA, Kramer S (2006) Plant-associated bacteria. Springer, The Netherlands, pp 105–130

    Google Scholar 

  • de Campos SB, Roesch LFW, Zanettini MHB, Passaglia LMP (2006) Relationship between in vitro enhanced nitrogenase activity of an Azospirillum brasilense Sp7 mutant and its growth-promoting activities in situ. Curr Microbiol 53:43–47

    CAS  PubMed  Google Scholar 

  • de Oliveira ALM, de Canuto EL, Urquiaga S, Reis VM, Baldani JI (2006) Yield of micropropagated sugarcane varieties in different soil types following inoculation with diazotrophic bacteria. Plant Soil 284:23–32

    CAS  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879

    Google Scholar 

  • Egamberdiyeva D, Höflich G (2002) Root colonization and growth promotion of winter wheat and pea by Cellulomonas spp. at different temperatures. Plant Growth Regulation 38:219–224

    CAS  Google Scholar 

  • Egener T, Hurek T, Reinhold-Hurek B (1999) Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Mol Plant–Microbe Interact 12:813–819

    CAS  Google Scholar 

  • Elbeltagy AK, Sato NT, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67:5285–5293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engelhard M, Hurek T, Reinhold-Hurek B (2000) Preferential occurrence of diazotrophic endophyte, Azoarcus sp. in wild rice species and land races of Oryza sativa in comparison with modern races. Environ Microbiol 2:131–141

    CAS  PubMed  Google Scholar 

  • Estrada P, Mavingui P, Cournoyer B, Fontaine F, Balandreau J, Caballero-Mellado J (2005) A N2-fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico. Int J Syst Evol Microbiol 55:1233–1237

    Google Scholar 

  • Feng Y, Shen D, Song W (2006) Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100:938–945

    CAS  PubMed  Google Scholar 

  • Fuentes-Ramírez LE, Caballero-Mellado J, Sepúlveda J, Martinez-Romero E (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol Ecol 29:117–128

    Google Scholar 

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

    CAS  Google Scholar 

  • Govindarajan M, Balandreau J, Muthukumarasamy R, Revathi G, Lakshminarasimhan C (2006) Improved yield of micropropagated sugarcane following inoculation by endophytic Burkholderia vietnamiensis. Plant Soil 280:239–252

    CAS  Google Scholar 

  • Govindarajan M, Kwon S-W, Weon H-Y (2007) Isolation, molecular characterization and growth-promoting activities of endophytic sugarcane diazotroph Klebsiella sp. World J Microbiol 23:997–1006

    CAS  Google Scholar 

  • Govindarajan M, Balandreau J, Muthukumarasamy R, Kwon S-W, Weon H-Y, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamiensis and related endophytic diazotrophic bacteria on grain yield of rice. Microbial Ecol 55:21–37

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gyaneshwar P, James EK, Mathan N, Reddy PM, Reinhold-Hurek B, Ladha JK (2001) Endophytic colonization of rice by a diazotrophic strain of Serretia marcessens. J Bacteriol 183:2634–2635

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytol 154:131–145

    CAS  Google Scholar 

  • Hilali A, Prévost D, Broughton WJ, Antoun H (2001) Effets de l’inoculation avec des souches de Rhizobium leguminosarum biovar trifolii sur la croissance du blé dans deux sols du Maroc. Can J Microbiol 47:590–59

    CAS  PubMed  Google Scholar 

  • Hurek T, Handley LL, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant–Microbe Interact 15:233–242

    CAS  PubMed  Google Scholar 

  • Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant–Microbe Interact 17:1078–1085

    CAS  PubMed  Google Scholar 

  • James EK, Olivares FL, de Oliveira ALM, dos Reis FB Jr, da Silva LG, Reis VM (2001) Further observations on the interaction between sugar cane and Gluconacetobacter diazotrophicus under laboratory and greenhouse conditions. J Exp Bot 52:747–760

    CAS  PubMed  Google Scholar 

  • James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant–Microbe Interact 15:894–906

    CAS  PubMed  Google Scholar 

  • Khalid A, Arshad M, Zahir Z (2005) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480

    Google Scholar 

  • Knauth S, Hurek T, Brar D, Reinhold-Hurek B (2005) Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environmental Microbiol 7:1725–1733

    CAS  Google Scholar 

  • Legaz M-E, de Armas R, Barriguete E, Vicente C (2000) Binding of soluble glycoproteins from sugarcane juice to cells of Acetobacter diazotrophicus. Int Microbiol 3:177–182

    CAS  PubMed  Google Scholar 

  • Matthews SS, Sparkes DL, Bullard MJ (2001) The response of wheat to inoculation with the diazotroph Azorhizobium caulinodans. Aspects Appl Biol 63:35–42

    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

    CAS  PubMed  Google Scholar 

  • Mirza MS, Rasul G, Mehnaz S, Ladha JK, So RB, Ali S, Malik KA (2000) Beneficial effects of inoculated nitrogen-fixing bacteria on rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. International Rice Research Institute, Los Baños, pp 191–204

    Google Scholar 

  • Mirza MS, Ahmad W, Latif F, Haurat J, Bally R, Normand P, Malik KA (2001) Isolation, partial characterization, and effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant Soil 237:47–54

    CAS  Google Scholar 

  • Muñoz-Rojas J, Caballero-Mellado J (2003) Population dynamics of Gluconacetobacter diazotrophicus in sugarcane cultivars and its effect on plant growth. Microb Ecol 46:454–464

    PubMed  Google Scholar 

  • Muthukumarasamy R, Revathi G, Lakshminarasimhan C (1999) Diazotrophic associations in sugar cane cultivation in South India. Trop Agric 76:171–178

    Google Scholar 

  • Muthukumarasamy R, Revathi G, Loganathan P (2002) Effect of inorganic N on the population, in vitro colonization and morphology of Acetobacter diazotrophicus (syn Gluconacetobacter diazotrophicus). Plant Soil 243:91–102

    CAS  Google Scholar 

  • Muthukumarasamy R, Cleenwerck I, Revathi G, Vadivelu M, Janssens D, Hoste B, Ui Gum K, Park K, Son CY, Sa T, Caballero-Mellado J (2005) Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28:277–286

    CAS  PubMed  Google Scholar 

  • Muthukumarasamy R, Kang UG, Park KD, Jeon W-T, Park CY, Cho YS, Kwon S-W, Song J, Roh D-H, Revathi G (2007) Enumeration, isolation and identification of diazotrophs from Korean wetland rice varieties grown with long-term application of N and compost and their short-term inoculation effect on rice plants. J Appl Microbiol 102:981–991

    CAS  PubMed  Google Scholar 

  • Oliveira ALM, Urquiaga S, Döbereiner J, Baldani JI (2002) The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants. Plant Soil 242:205–215

    CAS  Google Scholar 

  • Ormeño-Orrillo E, Rosenblueth M, Luyten E, Vanderleyden J, Martínez-Romero E (2008) Mutations in lipopolysaccharide biosynthetic genes impair maize rhizosphere and root colonization of Rhizobium tropici CIAT899. Environ Microbiol 10:1271–1284

    PubMed  Google Scholar 

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

    Google Scholar 

  • Perrine-Walker FM, Hocart CH, Hynes MF, Rolfe BG (2005) Plasmid-associated genes in the model micro-symbiont Sinorhizobium meliloti 1021 affect the growth and development of young rice seedlings. Environ Microbiol 7:1826–1838

    Google Scholar 

  • Perrine-Walker FM, Gartner E, Hocart CH, Becker A, Rolfe BG (2007a) Rhizobium-initiated rice growth inhibition caused by nitric oxide accumulation. Mol Microbe Plant Interact 20:283–292

    CAS  Google Scholar 

  • Perrine-Walker FM, Prayitno J, Rolfe BG, Weinman JJ, Hocart CH (2007b) Infection process and the interaction of rice roots with rhizobia. J Exp Bot 58:3343–50

    CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Van Wees SCM, Ton J, Van Pelt JA, van Loon LC (2002) Signalling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol (Stuttgart) 4:535–544

    CAS  Google Scholar 

  • Pinheiro RD, Boddey LH, James EK, Sprent JI, Boddey RM (2002) Adsorption and anchoring of Azospirillum strains to roots of wheat seedlings. Plant Soil 246:151–166

    Google Scholar 

  • Prayitno J, Stefaniak J, McIver J, Weinmen JJ, Dazzo FB, Ladha JK, Barraquio W, Yanni YG, Rolfe BG (1999) Interactions of rice seedlings with bacteria isolated from rice roots. Aust J Plant Physiol 26:521–535

    Google Scholar 

  • Reinhold-Hurek B, Hurek T (1997) Azoarcus spp. and their interactions with grass roots. Plant Soil 194:57–64

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rejesus RM, Hornbaker RH (1999) Economic and environmental evaluation of alternative pollution-reducing nitrogen management practices in central Illinois. Agric Ecosyst Environ 75:41–53

    Google Scholar 

  • Riggs PJ, Chelius MK, Iniguez AL, Kaeppler SM, Triplett EW (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust J Plant Physiol 28:829–836

    Google Scholar 

  • Roncato-Maccari LDB, Ramos HJO, Pedrosa FO, Alquini Y, Chubatsu LS, Yates MG, Rigo LU, Steffens MBR, Souza EM (2003) Endophytic Herbaspirillum seropedicae expresses nif genes in gramineous plants. FEMS Microbiol Ecol 45:39–47

    CAS  PubMed  Google Scholar 

  • Saleh SA, Mekhemar GAA, El-Soud AAA, Ragab AA, Mikhaeel FT (2001) Survival of Azorhizobium and Azospirillum in different carrier materials: inoculation of wheat and Sesbania rostrata. Bulletin of Faculty of Agriculture, Cairo University 52:319–338

    Google Scholar 

  • Sevilla M, Kennedy C (2000) Genetic analysis of nitrogen fixation and plant-growth stimulating properties of Acetobacter diazotrophicus, an endophyte of sugarcane. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific, Norwich, UK, pp 737–760

    Google Scholar 

  • Sevilla M, Gunapala N, Burris RH, Kennedy C (2001) Comparison of benefit to sugarcane plant growth and 15N2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and nif− mutant strains. Mol Plant–Microbe Interact 14:358–366

    CAS  PubMed  Google Scholar 

  • Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–59

    CAS  PubMed  Google Scholar 

  • Suman A, Gaur A, Shrivastava AK, Yadav RL (2005) Improving sugarcane growth and nutrient uptake by inoculating Gluconacetobacter diazotrophicus. Plant Growth Regul 47:155–162

    CAS  Google Scholar 

  • Suman A, Gaur A, Shrivastava AK, Gaur A, Singh P, Singh J, Yadav RL (2007) Nitrogen use efficiency of sugarcane in relation to its BNF potential and population of endophytic diazotrophs at different N levels. Plant Growth Regul 54:1–11

    Google Scholar 

  • Trân Van V, Berge O, Kê SN, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensis on early and late yield components in low fertility sulphate acid soils of Vietnam. Plant Soil 218:273–284

    Google Scholar 

  • Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–41

    CAS  PubMed  Google Scholar 

  • Verma SC, Singh A, Paul Chowdhury S, Tripathi AK (2004) Endophytic colonization ability of two deep-water rice endophytes, Pantoea sp. and Ochrobactrum sp. using green fluorescent protein reporter. Biotechnol Lett 26:425–429

    CAS  PubMed  Google Scholar 

  • Wang K, Conn K, Lazarovits G (2006) Involvement of quinolinate phosphoribosyl transferase in promotion of potato growth by a Burkholderia strain. Appl Environ Microbiol 72:760–768

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruinj 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

    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, 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 

  • You M, Nishiguchi T, Saito A, Isawa T, Mitsui H, Minamisawa K (2005) Expression of the nifH gene of a Herbaspirillum endophyte in wild rice species: daily rhythm during the light–dark cycle. Appl Environ Microbiol 71:8183–8190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Hurek T, Reinhold-Hurek B (2007) A nifH-based oligonucleotide microarray for functional diagnostics of nitrogen-fixing microorganisms. Microbiol Ecol 53:456–470

    CAS  Google Scholar 

Download references

Acknowledgments

One of the authors, RBB, is thankful to Council of Scientific and Industrial Research, India, for the Ph.D. fellowship. We are thankful to Sujay Bhattacharjee for his editorial help.

Author information

Author notes

  1. Rumpa Biswas Bhattacharjee

    Present address: Department of Molecular and Cell Biology, University of Guelph, Guelph, Ontario, Canada, N1G 2W1

Authors and Affiliations

  1. Department of Biochemical Engineering and Biotechnology, Indian Institute of Technology Delhi, Hauz Khas, New Delhi, 100 016, India

    Rumpa Biswas Bhattacharjee & S. N. Mukhopadhyay

  2. National Research Centre on Plant Biotechnology, Indian Agricultural Research Institute, Pusa, New Delhi, 100 012, India

    Aqbal Singh

Authors
  1. Rumpa Biswas Bhattacharjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aqbal Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. N. Mukhopadhyay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aqbal Singh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhattacharjee, R.B., Singh, A. & Mukhopadhyay, S.N. Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80, 199–209 (2008). https://doi.org/10.1007/s00253-008-1567-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-008-1567-2

Keywords

Search

Navigation