Skip to main content

Advertisement

SpringerLink
Log in

The ammonium excreting Azospirillum brasilense strain HM053: a new alternative inoculant for maize

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

We evaluated the effect of Azospirillum brasilense strain HM053 inoculation on maize seeds, a spontaneous mutant that excrete ammonium and fix nitrogen constitutively.

Methods

Maize was grown with different nitrogen (urea) concentration and inoculated with A. brasilense Ab-V5 (Brazilian commercial strain) or HM053 strain in four field experiments, in three regions of Parana State, Southern Brazil. We evaluated yield components, nutrient content on leaves and grains and productivity during the crop cycle.

Results

Inoculation with A. brasilense strain Ab-V5 and HM053 associated with base fertilization (30 kg ha−1 N) improved crop yield in all trials. Ab-V5 increased production between 2.2 to 10.4%, or 178.0 to 759.9 kg ha−1, respectively. HM053, by itself, increased production between 4.7 to 29%, or 460.5 to 1769.3 kg ha−1, respectively.

Conclusion

The new strain HM053 showed to be a great biofertilizer for maize seeds and a new alternative for a more sustainable agriculture.

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

Fig. 1

Similar content being viewed by others

References

  • AOAC (1998) official method 992.15, combustion method, 16 th Edition

  • Aquino GS, Ventura MU, Alexandrino RP, Michelon TA, Araujo Pescador PG, Nicio TT, Watanabe VS, Diniz TG, Oliveira ALM, Hata FT (2018) Plant-promoting rhizobacteria Methylobacterium komagatae increases crambe yields, root system and plant height. Ind Crop Prod 121:277–281. https://doi.org/10.1016/j.indcrop.2018.05.020

    Article  Google Scholar 

  • Araújo LM, Monteiro RA, Souza EM, Steffens MBR, Rigo LU, Pedrosa FO, Chubatsu LS (2004) GlnB is specifically required for Azospirillum brasilense NifA activity in Escherichia coli. Res Microbiol 155:491–495. https://doi.org/10.1016/j.resmic.2004.03.002

    Article  CAS  PubMed  Google Scholar 

  • Arcondéguy T, Jack R, Merrick M (2001) PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105. https://doi.org/10.1128/MMBR.65.1.80-105.2001

    Article  PubMed  PubMed Central  Google Scholar 

  • Arsene F, Kaminski PA, Elmerich C (1996) Modulation of NifA activity by PII in Azospirillum brasilense: evidence for a regulatory role of the NifA N-terminal domain. J Bacteriol 178:4830–4838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27(2):197–205. https://doi.org/10.1007/s11274-010-0444-1

    Article  CAS  Google Scholar 

  • Baldani JI, Baldani VL (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An. Acad. Bras. Ciênc. An Acad Bras Cienc 77(3):549–579. https://doi.org/10.1590/S0001-37652005000300014

    Article  CAS  PubMed  Google Scholar 

  • Bashan Y, de-Bashan L (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth. A critical assessment. Adv Agron 108:77–136. https://doi.org/10.1016/S0065-2113(10)08002-8

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36(9):591–608. https://doi.org/10.1139/m90-105

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can J Microbiol 50:521–577. https://doi.org/10.1139/w04-035

    Article  CAS  PubMed  Google Scholar 

  • Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. https://doi.org/10.1007/s11104-014-2131-8

    Article  CAS  Google Scholar 

  • Calzavara AK, Paiva PHG, Gabriel LC, Oliveira ALM, Milani K, Oliveira HC, Bianchini E, Pimenta JA, Oliveira MCN, Dias-Pereira J, Stolf-Moreira R (2018) Associative bacteria influence maize (Zea mays L.) growth, physiology and root anatomy under different nitrogen levels. Plant Biol 20(5):870–878. https://doi.org/10.1111/plb.12841

    Article  CAS  PubMed  Google Scholar 

  • Cassán F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biol Biochem 103:117–130. https://doi.org/10.1016/j.soilbio.2016.08.020

    Article  CAS  Google Scholar 

  • Cassán F, Vanderleyden J, Spaepen S (2014) Physiological and agronomical aspects of phytohormone production by model plant growth promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J Plant Growth Regul 33:440–459. https://doi.org/10.1007/s00344-013-9362-4

    Article  CAS  Google Scholar 

  • Creus C, Sueldo R, Barassi C (1997) Shoot growth and water status in Azospirillum inoculated wheat seedlings grown under osmotic and salt stresses. Plant Physiol Biochem 35:939–944

    CAS  Google Scholar 

  • Díaz-Zorita M, Fernández-Canigia MV, Bravo OA, Berger A, Satorre EH (2015) Field evaluation of extensive crops inoculated with Azospirillum sp. In: Cassán FD, Okon Y, Creus CM (eds) Handbook for Azospirillum, technical issues and protocols. Springer Int. Publishing, Cham, pp 435–445. https://doi.org/10.1007/978-3-319-06542-7_24

    Chapter  Google Scholar 

  • Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694. https://doi.org/10.1111/j.1365-3040.2009.02028.x

    Article  CAS  PubMed  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirr JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Pkon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879. https://doi.org/10.1071/PP01074

    Article  Google Scholar 

  • Döbereiner J, Day JM (1976) Associative symbiosis in tropical grasses: characterization of microorganisms and dinitrogen-fixing sites. In: Newton WE, Nyman CT (eds) Proceedings of the international symposium on nitrogen fixation, vol 2. Washington State University Press, Pullman, pp 518–538

    Google Scholar 

  • Döbereiner J, Pedrosa FO (1987) Nitrogen-fixing bacteria in nonleguminous crop plants. Science tech. Springer Verlag, Madison, pp 1–155

    Google Scholar 

  • Elmerich C, Aubert JP (1971) Synthesis of glutamate by a glutamine: 2-oxo-glutarate amidotransferase (NADP oxidoreductase) in Bacillus megaterium. Biochem Biophys Res Commun 42:371–376

    Article  CAS  PubMed  Google Scholar 

  • Embrapa - Empresa Brasileira de Pesquisa Agropecuária (1999) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa, Brasilia, pp 175–180

  • Fadel-Picheth CMT, Souza EM, Rigo LU, Funayama S (1999) Regulation of Azospirillum brasilense nifA gene expression by ammonium and oxygen. FEMS Microbiol Lett 179:281–288

    Article  CAS  PubMed  Google Scholar 

  • Fu H, Hartmann A, Lowery RG, Fitzmaurice WP, Roberts GP, Burris RH (1989) Posttranslational regulatory system for nitrogenase activity in Azospirillum spp. J Bacteriol 171:4679–4685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huergo LF, Pedrosa FO, Muller-Santos M, Chubatsu LS, Monteiro RA, Merrick M, Souza EM (2012) PII signal transduction proteins: pivotal players in post-translational control of nitrogenase activity. Microbiology 158:176–190. https://doi.org/10.1099/mic.0.049783-0

    Article  CAS  PubMed  Google Scholar 

  • Hungria M, Campo RJ, Souza EM, Pedrosa FO (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331:413–425. https://doi.org/10.1007/s11104-009-0262-0

    Article  CAS  Google Scholar 

  • Machado HB, Funayama S, Rigo LU, Pedrosa FO (1991) Excretion of ammonium by Azospirillum brasilense mutants resistant to ethylenediamine. Can J Microbiol 37:549–553

    Article  CAS  Google Scholar 

  • Magalhães PC, Durães FOM (2006) Fisiologia da Produção de Milho. Embrapa. Sete Lagoas, p10. ISSN 1679-1150

  • Martins RM, Jantalia CP, Reis VM, Döwich I, Polidoro JC, Alves BJR, Boddey RM, Urquiaga S (2018) Impact of plant growth-promoting bacteria on grain yield, protein content, and urea-15 N recovery by maize in a Cerrado Oxisol. Plant Soil 422:239–250. https://doi.org/10.1007/s11104-017-3193-1

    Article  CAS  Google Scholar 

  • Meers J, Tempest D (1970) “Glutamine(amide): 2-oxoglutarate amino transferase oxido-reductase (NADP)”, an enzyme involved in the synthesis of glutamate by some bacteria. J Gen Microbiol 64:187–194

    Article  CAS  PubMed  Google Scholar 

  • Moure VR, Danyal K, Yang Z-Y, Wendroth S, Müller-Santos M, Pedrosa FO, Scarduelli M, Gerhardt EC, Huergo LF, Souza EM, Seefeldt LC (2013) The nitrogenase regulatory enzyme dinitrogenase reductase ADP ribosyltransferase (DraT) is activated by direct interaction with the signal transduction protein GlnB. J Bacteriol 195:279–286. https://doi.org/10.1128/JB.01517-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okon Y, Heytler P, Hardy W (1983) N2 fixation by Azospirillum brasilense and its incorporation into host Setaria italica. Appl Environ Microbiol 46:694–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira AL, Santos OJ, Marcelino PR, Milani KM, Zuluaga MY, Zucareli C, Gonçalves LS (2017) Maize inoculation with Azospirillum brasilense ab-V5 cells enriched with exopolysaccharides and polyhydroxybutyrate results in high productivity under low N fertilizer input. Front Microbiol 8:1873. https://doi.org/10.3389/fmicb.2017.01873

    Article  PubMed  PubMed Central  Google Scholar 

  • Pankievicz VCS, Amaral FP, Santos KFDN, Agtuca B, Xu Y, Schueller MJ, Arisi ACM, Steffens MBR, Souza EM, Pedrosa FO, Stacey G, Ferrieri RA (2015) Robust biological nitrogen fixation in a model grass-bacterial association. Plant J 81:907–919. https://doi.org/10.1111/tpj.12777

    Article  CAS  PubMed  Google Scholar 

  • Pauletti V, Motta ACV (2017) Manual de adubação e calagem para o estado do Paraná. Curitiba: Sociedade Brasileira de Ciência do Solo, Núcleo Estadual Paraná. ISBN 978–85–69146-04-9

  • Pavan MA, Bloch MF, Zempulski HD, Miyazawa M, Zocoler DC (1992) Manual de análise química do solo e controle de qualidade. Instituto Agronômico do Paraná, Londrina, Brazil, 40 pp ISSN: 0100–3356

  • Puente M, Li C, Bashan Y (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. II. Growth promotion of cactos seedlings. Plant Biol 6:643–650. https://doi.org/10.1055/s-2004-821101

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2018) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rodrigues, RC (2010) Métodos de análises bromatológicas de alimentos: métodos físicos, químicos e bromatológicos. Embrapa, Pelotas. ISSN 1806-9193

  • Santos ARS, Etto RM, Furmam RW, de Freitas DL, Santos KFDEN, Souza EM, Pedrosa FO, Ayub RA, Steffens MBR, Galvão CW (2017a) Labeled Azospirillum brasilense wild type and excretion-ammonium strains in association with barley roots. Plant Physiol Biochem 118:422–426. https://doi.org/10.1016/j.plaphy.2017.07.003

    Article  CAS  PubMed  Google Scholar 

  • Santos KFDN, Moure VR, Hauer V, Santos ARS, Donatti L, Galvão CW, Pedrosa FO, Souza EM, Wassem R, Steffens MBR (2017b) Wheat colonization by an Azospirillum brasilense ammonium-excreting strain reveals upregulation of nitrogenase and superior plant growth promotion. Plant Soil 415:245–255. https://doi.org/10.1007/s11104-016-3140-6

    Article  CAS  Google Scholar 

  • Singh DP, Singh HB, Prabha R (2016) Microbial inoculants in sustainable agricultural productivity. Springer, New York ISBN: 978-8132226420

    Book  Google Scholar 

  • Tarrand JJ, Krieg NR, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. Nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980

    Article  CAS  PubMed  Google Scholar 

  • Tiepo AN, Hertel MF, Rocha SS, Calzavara AK, Oliveira ALM, Pimenta JA, Oliveira HC, Bianchini E, Stolf-Moreira R (2018) Enhanced drought tolerance in seedlings of Neotropical tree species inoculated with plant growth-promoting bacteria. Plant Physiol Biochem 130:277–288. https://doi.org/10.1016/j.plaphy.2018.07.021

    Article  CAS  PubMed  Google Scholar 

  • Timmusk S, Behers L, Muthon J, Muraya A, Aronsson AC (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:49. https://doi.org/10.3389/fpls.2017.00049

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the Brazilian Program of National Institutes of Science and Technology-INCT/Brazilian Research Council-CNPq/MCT, CNPq, CAPES and Fundação Araucária for the financial support.

Author information

Authors and Affiliations

  1. Nucleus of Nitrogen Fixation, Federal University of Paraná (UFPR), Curitiba, PR, CEP 81531-980, Brazil

    F. O. Pedrosa & E. M. Souza

  2. Laboratory of Agricultural Ecophysiology and Biotechnology, State University of Londrina (UEL), Londrina, PR, CEP 86057-970, Brazil

    A. L. M. Oliveira, O. J. A. P. Santos & L. S. A. Gonçalves

  3. Laboratory of Plant Physiology, State University of Western Paraná (UNIOESTE), Marechal Candido Rondon, PR, CEP 85960-000, Brazil

    V. F. Guimarães & A. G. Battistus

  4. Microbial Molecular Biology Laboratory, State University of Ponta Grossa (UEPG), Ponta Grossa, PR, CEP 84030-900, Brazil

    R. M. Etto, F. G. Furmam, D. R. P. Gonçalves & C. W. Galvão

Authors
  1. F. O. Pedrosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. L. M. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. F. Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. M. Etto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. M. Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. G. Furmam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. R. P. Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. O. J. A. P. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. L. S. A. Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. A. G. Battistus
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. C. W. Galvão
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. W. Galvão.

Additional information

Responsible Editor: Anton Hartmann.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 280 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pedrosa, F.O., Oliveira, A.L.M., Guimarães, V.F. et al. The ammonium excreting Azospirillum brasilense strain HM053: a new alternative inoculant for maize. Plant Soil 451, 45–56 (2020). https://doi.org/10.1007/s11104-019-04124-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04124-8

Keywords

Search

Navigation