Skip to main content
SpringerLink
Log in

Selection of phosphate-solubilizing diazotrophic Herbaspirillum and Burkholderia strains and their effect on rice crop yield and nutrient uptake

Plant and Soil volume 369, pages 115–129 (2013)Cite this article

Abstract

Background and Aims

Plant growth-promoting bacteria, mainly diazotrophs and phosphate solubilizers, can reduce the use of chemical fertilizers for rice crops. Here, diazotrophic bacteria isolated from rice were screened for their ability to solubilize inorganic P (Pi) in vitro and in association with rice plants cultivated in pots.

Methods

Forty-nine isolates were tested for the ability to solubilize Pi on NBRIP and GL agar plate media and seven selected strains were further evaluated in NBRIP liquid medium. Three of these strains were inoculated in rice plants grown in soil pots containing 15N-labeled fertilizer and two sources of P: tricalcium phosphate (TCP) or simple superphosphate (SSP). The dry matter, yield, N, P, and the 15N content accumulated in plant tissues were measured at 135 days after planting.

Results

Seven strains belonging to the genera Herbaspirillum and Burkholderia formed a halo of solubilized Pi on agar plates. The Burkholderia strains showed peak soluble P (around 200 mg P L−1) on the fifth day when grown in NBRIP liquid medium for 14 days. Inoculation of Herbaspirillum strains (H18, ZA15) and a Burkholderia vietaminensis strain (AR114) increased rice grain yield from 33 to 47 % with TCP and 18 to 44 % with TSS, respectively. The bacterial inoculation led to enhanced N-use efficiency of the 15N-labeled fertilizer.

Conclusion

These results suggest that the selection and use of P-solubilizing diazotrophic bacteria are a good strategy to promote P solubilization and/or N use efficiency in rice plants.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

39,95 €

Price includes VAT (Finland)

Fig. 1
Fig. 2

References

  • Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–992

    Article  PubMed  CAS  Google Scholar 

  • Adesemoye AO, Torbert HA, Kloepper JW (2010) Increased plant uptake of nitrogen from 15N-depleted fertilizer using plant growth-promoting rhizobacteria. Appl Soil Ecol 46:54–58

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Araújo AES, Baldani VLD, Galisa PS,Pereira JA, Baldani JI (2012) Response of traditional upland rice varieties to inoculation with selected diazotrophic bacteria isolated from rice cropped at the Northeast region of Brazil. Appl Soil Ecol, http://dx.doi.org/10.1016/j.apsoil.2012.10.004

  • Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148

    Article  CAS  Google Scholar 

  • Baldani JI, Baldani VLD (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Cienc 77:549–579

    Article  PubMed  CAS  Google Scholar 

  • Baldani JI, Krieg NR, Baldani VLD, Hartmann A, Döbereiner J (2005a) Genus II. Azospirillum. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology - the protobacteria, 2nd edn. Springer, Newark, pp 7–26

    Google Scholar 

  • Baldani JI, Baldani VLD, Döbereiner J (2005b) Genus III. Herbaspirillum. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology - the protobacteria, 2nd edn. Springer, Newark, pp 629–636

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Barriuso J, Pereyra MT, Lucas García JA, Megías Gutierrez Mañero MFJ, Ramos B (2005) Screening for putative PGPR to improve establishment of the symbiosis Lactarius deliciosus-Pinus sp. Microbial Ecol 50:82–89

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth - a critical assessment. Adv Agron 108:77–136

    Article  CAS  Google Scholar 

  • Boddey RM (1987) Methods for quantification of nitrogen fixation associated with graminae. Cr Rev Plant Sci 6:209–266

    Article  CAS  Google Scholar 

  • Buresh RJ, Reddy KR, van Kessel C (2008) Nitrogen transformations in submerged soils. In: Schepers JS, Raun WR (eds) Nitrogen in agricultural systems. Agronomy Monograph 49. ASA, CSSA, and SSSA, Madison, pp 401–436

    Google Scholar 

  • Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microb 73:5308–5319

    Article  CAS  Google Scholar 

  • Chen Y, Rekha P, Arun A, Shen F, La W, Young C (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcicum phosphate solubilizing abilities. Appl Soil Ecol 34:33–41

    Article  Google Scholar 

  • Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • CONAB (Companhia Nacional de Abastecimento) (2012) Acompanhamento da safra Brasileira: Grãos. www.conab.gov.br/OlalaCMS/uploads/arquivos/12_09_06_09_18_33_boletim_graos_-setembro_2012.pdf. Accessed 18 Sep 2012.

  • Deubel A, Merbach W (2005) Influence of microorganisms on phosphorus bioavailability in soils. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions. Springer, Berlin, pp 177–191

    Chapter  Google Scholar 

  • Döbereiner J (1988) Isolation and identification of root associated diazotrophs. Plant Soil 110:207–212

    Article  Google Scholar 

  • Döbereiner J (1995) Isolation and identification of aerobic nitrogen-fixing bacteria from soil and plants. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, London, pp 134–141

    Google Scholar 

  • Ferreira DF (2008) SISVAR: a program for statistical analysis and teaching. Rev Symp 6:36–41

    Google Scholar 

  • Ferreira JS, Baldani JI, Baldani VLD (2010) Seleção de inoculantes à base de turfa contendo bactérias diazotróficas em duas variedades de arroz. Acta Sci-Agron 32:179–185

    Google Scholar 

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

    Article  Google Scholar 

  • Gregory DI, Haefele SM, Buresh RJ, Singh U (2010) Fertilizer use, markets, and management. In: Pandey S, Byerlee D, Dawe D, Achim Dobermann A, Mohanty S, Rozelle S, Bill Hardy B (eds) Rice in the global economy: strategic research and policy issues for food security. International Rice Research Institute, Los Baños, pp 231–263

    Google Scholar 

  • Hazell PBR (2010) Asia’s Green Revolution: past achievements and future challenges. In: Pandey S, Byerlee D, Dawe D, Achim Dobermann A, Mohanty S, Rozelle S, Bill Hardy B (eds) Rice in the global economy: strategic research and policy issues for food security. International Rice Research Institute, Los Baños, pp 61–92

    Google Scholar 

  • Helman Y, Burdman S, Okon Y (2011) Plant growth promotion by rhizosphere bacteria through direct effects. In: Rosenberg E, Gophna U (eds) Beneficial microorganisms in multicellular life form. Springer, Heidelberg, pp 89–103

    Google Scholar 

  • IFA (International Fertilizer Industry Association). Assessment of Fertilizer Use by Crop at the Global Level 2006/07–2007/08. Accessed 15 Sep 2012.

  • Intorne AC, de Oliveira MV, Lima ML, da Silva JF, Olivares FL, de Souza Filho GA (2009) Identification and characterization of Gluconacetobacter diazotrophicus mutants defective in the solubilization of phosphorus and zinc. Arch Microbiol 191:477–483

    Article  PubMed  CAS  Google Scholar 

  • Jha B, Thakura MC, Gontia I, Albrecht V, Stoffels M, Schmid M, Hartmann A (2009) Isolation, partial identification and application of diazotrophic rhizobacteria from traditional Indian rice cultivars. Eur J Soil Biol 45:62–72

    Article  CAS  Google Scholar 

  • Kirk GJD, Santos EE, Santos MB (1999) Phosphate solubilization by organic anion excretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate solubility and uptake. New Phytol 142:185–200

    Article  CAS  Google Scholar 

  • Kumar V, Narula N (1999) Solubilization of inorganic phosphates and growth emergent of wheat as affected by Azotobacter chrococum mutants. Biol Fert Soils 28:301–305

    Article  CAS  Google Scholar 

  • Kundu B, Gaur A (1980) Establishment of nitrogen fixing and phosphate solubilizing bacteria in rhizosphere and their effect on yield and nutrient uptake of wheat crop. Plant Soil 57:223–230

    Article  CAS  Google Scholar 

  • Lucas JA, Ramos Solano B, Montes F, Ojeda J, Megias M, Gutierrez Manero FJ (2009) Use of two PGPR strains in the integrated management of blast disease in rice (Oryzae sativa) in Southern Spain. Field Crops Res 14:404–410

    Article  Google Scholar 

  • Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86:1–25

    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 

  • Marra LM, de Oliveira SM, Soares CRFS, Moreira FMS (2011) Solubilisation of inorganic phosphates by inoculant strains from tropical legumes. Sci Agric 68:603–609

    CAS  Google Scholar 

  • Maheshkumar KS, Krishnaraj PU, Alagwadi AR (1999) Mineral solubilising activity of Acetobacter diazotrophicus, a bacterium associated with sugarcane. Curr Sci 76:874–875

    Google Scholar 

  • MF-SEAE (Ministério da Fazenda - Secretaria de Acompanhamento Econômico) (2011) Panorama do mercado de fertilizantes – Maio/2011. 35p. www.seae.fazenda.gov.br/...fert_seae_-2011_fertilizantes.pdf.

  • Murty M, Ladha J (1988) Influence of Azospirillum inoculation on the mineral uptake and growth of rice under hydroponic conditions. Plant Soil 108:281–285

    Article  Google Scholar 

  • Nautiyal C (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    Article  PubMed  CAS  Google Scholar 

  • Nico M, Ribaudo CM, Gori JI, Cantore ML, Curá JA (2012) Uptake of phosphate and promotion of vegetative growth in glucose-exuding rice plants (Oryza sativa) inoculated with plant growth-promoting bacteria. Appl Soil Ecol 61:190–195

    Article  Google Scholar 

  • Öğüt M, Er F, Neumann G (2011) Increased proton extrusion of wheat roots by inoculation with phosphorus solubilising microorganism. Plant Soil 339:285–297

    Article  Google Scholar 

  • Osborne CA, Galic M, Sangwan P, Janssen PH (2005) PCR generated artefact from 16S rRNA gene-specific primers. FEMS Microbiol Lett 248:183–187

    Article  PubMed  CAS  Google Scholar 

  • Panhwar QA, Radziah O, Zaharah Rahman A, Sariah M, Mohd Razi I, Naher UA (2011) Contribution of phosphate-solubilizing bacteria in phosphorus bioavailability and growth enhancement of aerobic rice. Span J Agric Res 9:810–820

    Google Scholar 

  • Park KH, Lee OM, Jung HI, Jeong JH, Jeon YD, Hwang DY, Lee CY, Son HJ (2010) Rapid solubilization of insoluble phosphate by a novel environmental stress-tolerant Burkholderia vietnamiensis M6 isolated from ginseng rhizospheric soil. Appl Microbiol Biot 86:947–995

    Article  CAS  Google Scholar 

  • Pedraza RO, Bellone CH, de Bellone S, Boa Sorte PMB, Teixeira KRD (2009) Azospirillum inoculation and nitrogen fertilization effect on grain yield and on the diversity of endophytic bacteria in the phyllosphere of rice rainfed crop. Eur J Soil Biol 45:36–43

    Article  CAS  Google Scholar 

  • Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

    Article  PubMed  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    Article  PubMed  CAS  Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321,305:339

    Google Scholar 

  • Rodrigues EP, Rodrigues LS, Oliveira ALM, Baldani VLD, Teixeira KRS, Urquiaga S, Reis VM (2008) Azospirillum amazonense inoculation: effects on growth yield and N2 fixation of rice (Oryza sativa L). Plant Soil 302:249–261

    Article  CAS  Google Scholar 

  • Rodrigues LS, Baldani VLD, Reis VM, Baldani JI (2006) Diversidade de bactérias diazotróficas endofíticas dos generos Herbaspirillum e Burkholderia na cultura de arroz inundado. Pesqui Agropecu Bras 41:275–284

    Article  Google Scholar 

  • Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Rojas-Tapias D, Moreno-Galván A, Pardo-Díaz S, Obando M, Rivera D, Bonilla R (2012) Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl Soil Ecol 61:264–272

    Article  Google Scholar 

  • Saravanan VS, Madhaiyan M, Osborne J, Thangaraju M, Sa TM (2008) Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Microb Ecol 55:130–140

    Article  PubMed  CAS  Google Scholar 

  • Sarwar M, Kremer RJ (1995) Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol 20:282–285

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth-promoting actions of rhizobacteria. Adv Bot Res 51:283–320

    Article  CAS  Google Scholar 

  • Spencer JFT, Ragout AL (2001) Food microbiology protocols, 1st edn. Humana Press, Totowa

    Google Scholar 

  • Sylvester-Bradley R, Asakawa N, Latorraca S, Magalhães FMM, Oliveira LA, Pereira RM (1982) Levantamento quantitativo de microrganismos solubilizadores de fosfato na rizosfera de gramíneas e leguminosas forrageiras na amazônia. Acta Amazon 12:15–22

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ (1995) Análise de solos plantas e outros materiais, 2nd edn. UFRGS, Porto Alegre

    Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    Article  PubMed  CAS  Google Scholar 

  • Thomson CJ, Marschner H, Römheld V (1993) Effect of nitrogen fertilizer form on pH of the bulk soil and rhizosphere, and on the growth, phosphorus, and micro-nutrient uptake of bean. J Plant Nutr 16:493–506

    Article  CAS  Google Scholar 

  • Van Tran V, Berge O, Ngô Kê S, 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 Vietnan. Plant Soil 218:273–284

    Article  Google Scholar 

  • Videira SS, de Oliveira DM, de Morais RF, Borges WL, Baldani VLD, Baldani JI (2012) Genetic diversity and plant growth promoting traits of diazotrophic bacteria isolated from two Pennisetum purpureum Schum. genotypes grown in the field. Plant Soil 356:51–66

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Embrapa, Faperj, MCTI/INCT-FBN and CNPq for financial support of this research.

Author information

Authors and Affiliations

  1. Curso Pós-graduação Fitotecnia, Embrapa Agrobiologia, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7, CEP 23891-000, Seropédica, RJ, Brazil

    German Andres Estrada

  2. Embrapa Agrobiologia, BR 465, Km 7, CEP 23891-000, Seropédica, RJ, Brazil

    Vera Lúcia Divan Baldani, Segundo Urquiaga & José Ivo Baldani

  3. Universidade Federal Rural do Rio de Janeiro/Embrapa Agrobiologia, BR 465, Km 7, CEP 23891-000, Seropédica, RJ, Brazil

    Danilo Messias de Oliveira

Authors
  1. German Andres Estrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vera Lúcia Divan Baldani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Danilo Messias de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Segundo Urquiaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José Ivo Baldani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Ivo Baldani.

Additional information

Responsible Editor: Jesus Mercado-Blanco.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Estrada, G.A., Baldani, V.L.D., de Oliveira, D.M. et al. Selection of phosphate-solubilizing diazotrophic Herbaspirillum and Burkholderia strains and their effect on rice crop yield and nutrient uptake. Plant Soil 369, 115–129 (2013). https://doi.org/10.1007/s11104-012-1550-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-012-1550-7

Keywords

  • Oryza sativa
  • Biofertilizer
  • Nitrogen use efficiency
  • Tricalcium phosphate
  • Bacterial inoculation
  • Indole production

Search

Navigation