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Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.)

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Abstract

This research has investigated the effect of two genotypes of maize (Zea mays L.) on the number and diversity of diazotrophic bacteria under different N-fertilization rates. Cultivars NK940 and PAU871 were grown in soil:sand with 0, 40, and 80 kg N ha−1 added as NH4NO3 under controlled conditions for 60 days. The number of diazotrophic bacteria of rhizosphere (S), disinfected roots (R), and stems (T) was determined by most probable number (MPN) method. Diazotrophic bacteria were isolated by N-free media, confirmed by amplification of nifH gene fragments, characterized by amplified 16S rDNA restriction analysis (ARDRA) and (GTG)5 fingerprinting, and identified by partial 16S ribosomal DNA (rDNA) sequence analysis. The diversity of the diazotrophic community from S and R was determined by Terminal Restriction Fragment Length Polymorphism (T-RFLP) analysis considering the nifH gene. Maize genotype had a marked effect on the number and diversity of endophytic communities, the NK940 community being more abundant and diverse than that of PAU871. Additionally, N-fertilization increased the number and diversity of diazotrophs in endophytic communities but not in rhizosphere samples. One hundred and six diazotrophs were isolated from S, R, and T samples. Pseudomonas and Enterobacter were the dominant and ubiquitous genera isolated and detected by culture-independent method. T-RFLP showed that the N-fixing populations of the rhizosphere of both cultivars were more diverse than those of inside roots. Principal component analysis (PCA) separated the samples by cultivar and demonstrated a more marked effect of N-fertilization on the NK940 diazotrophic community than on PAU871. These results support the hypothesis that plant genotype and fertilization conditions should be taken into account when searching for N-fixer inocula.

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References

  • Altschul SF, Madden TL, Schaeffer 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 Central  CAS  PubMed  Google Scholar 

  • Anand R, Chanway C (2013) N2-fixation and growth promotion in cedar colonized by an endophytic strain of Paenibacillus polymyxa. Biol Fertil Soils 49:235–239

    Article  CAS  Google Scholar 

  • Arruda L, Beneduzi A, Martins A, Lisboa B, Lopes C, Bertolo F, Passaglia LMP, Vargas LK (2013) Screening of rhizobacteria isolated from maize (Zea mays L.) in Rio Grande do Sul State (South Brazil) and analysis of their potential to improve plant growth. Appl Soil Ecol 63:15–22

    Article  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 Cienc 77:549–579

    Article  CAS  PubMed  Google Scholar 

  • Baldani JI, Caruso L, Baldani VLD, Goi SR, Döbereiner DJ (1997) Recent advances in BNF with non-legume plants. Soil Biol Biochem 29:911–922

    Article  CAS  Google Scholar 

  • Baldani VLD, Baldani JI, Olivares FL, Döbereiner J (1992) Identification and ecology of Herbaspirillum seropedicae and the closely related Pseudomonas rubrisubalbicans. Symbiosis 13:65–73

    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

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209

    Article  CAS  PubMed  Google Scholar 

  • Bohlool BB, Ladha JK, Garrity T (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant Soil 141:1–11

    Article  CAS  Google Scholar 

  • Cavalcante VA, Döbereiner J (1988) A new acid-tolerant bacterium associated with sugarcane. Plant Soil 108:23–31

    Article  Google Scholar 

  • Chelius MK, Triplett EW (2000) Diazotrophic endophyte associated with maize. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Norfolk, UK, pp 779–792

    Google Scholar 

  • Chen G, Hoglong Z, Zhang Y (2003) Soil microbial activities and carbon and nitrogen fixation. Res Microbiol 157:393–398

    Article  Google Scholar 

  • Choudhury SP, Schmid M, Hartmann A, Tripathi AK (2007) Identification of diazotrophs in the culturable bacterial community associated with roots of Lasiurus sindicus, a perennial grass of Thar desert. India Microb Ecol 54:82–90

    Article  Google Scholar 

  • Coelho MRR, Marriel I, Jenkins S, Lanyon C, Seldin L, O’Donnell A (2009) Molecular detection and quantification of nifH gene sequences in the rhizosphere of sorghum (Sorghum bicolor) sown with two levels of nitrogen fertilizer. Appl Soil Ecol 42:48–53

    Article  Google Scholar 

  • da Costa PB, Beneduzi A, de Souza R, Schoenfeld R, Vargas KL, Passaglia LMP (2013) The effects of different fertilization conditions on bacterial plant growth promoting traits: guidelines for directed bacterial prospection and testing. Plant Soil 368:267–280

    Article  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

    Article  CAS  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; London Academia Press pp. 134–141

  • dos Reis FB, Jr RVM, Urquiaga S, Döbereiner J (2000) Influence of nitrogen fertilization on the population of diazotrophic Herbaspirillum spp. and Gluconacetobacter diazotrophicus in sugar cane (Saccharum spp.). Plant Soil 219:153–159

    Article  Google Scholar 

  • Dunbar J, Lawrence O, Kuske C (2000) Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl Environ Microbiol 66:2943–2950

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • El-Komy HMA, Moharram TMM, Safwat MSA (1998) Effect of Azospirillum inoculation on growth and N2 fixation of maize subjected to different levels of FYM using 15N-dilution method. In: Malik KA, Mirza MS, Ladha JK (eds) Nitrogen Fixation with Non-Legumes. Kluwer Academic Publishers, Dordrecht, pp 49–59

    Chapter  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

    Article  Google Scholar 

  • Fuentes-Ramirez 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 29:117–127

    Article  CAS  Google Scholar 

  • García de Salamone I, Döbereiner J (1996) Maize genotype effects on the response to Azospirillum inoculation. Biol Fert Soils 21:193–196

    Article  Google Scholar 

  • Garcia de Salamone I, Döbereiner J, Urquiaga S, Boddey RM (1996) Biological nitrogen fixation in Azospirillum strain-maize genotype associations as evaluated by the 15N isotope dilution technique. Biol Fert Soils 23:249–256

    Article  CAS  Google Scholar 

  • García de Salamone I, Funes JM, Di Salvo LP, Escobar-Ortega JS, D’Auria F, Ferrando L, Fernandez-Scavino A (2012) Inoculation of paddy rice with Azospirillum brasilense and Pseudomonas fluorescens: impact of plant genotypes on rhizosphere microbial communities and field crop production. Appl Soil Ecol 61:196–204

    Article  Google Scholar 

  • Gillis M, Kersters K, Hoste B, Janssens D, Kroppenstedt M, Stephan MP, Teixeira KRS, Dobereiner J, De Ley J (1989) Acetobacter diazotrophicus sp. nov., a nitrogen fixing acetic acid bacterium associated with sugarcane. Int J Syst Bacteriol 39:361–364

    Article  Google Scholar 

  • Gopalakrishnan S, Humayun P, Kiran BK, Kannan IGK, Vidya MS, Deepthi K, Rupela O (2011) Evaluation of bacteria isolated from rice rhizosphere for biological control of charcoal rot of sorghum caused by Macrophomina phaseolina (Tassi) Goid. World J Microbiol Biotechnol 27:1313–1321

    Article  CAS  PubMed  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 154:131–146

    Article  CAS  Google Scholar 

  • Herrera-Cervera JA, Caballero-Mellado J, Laguerre G, Hans-Volker T, Requena N, Amarger N, Martinez-Romero E, Olivares J, Sanjuan J (1999) At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 30:87–97

    Article  CAS  Google Scholar 

  • Hungria M, Campo RI, 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

    Article  CAS  Google Scholar 

  • Islam R, Trivedi P, Madhaiyan M, Seshadri S, Lee G, Yang J, Kim Y, Kim M, Han G, Singh Chauhan P, Sa T (2010) Isolation, enumeration, and characterization of diazotrophic bacteria from paddy soil sample under long-term fertilizer management experiment. Biol Fertil Soils 46:261–269

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jiménez-Salgado T, Fuentes-Ramírez LE, Tapia-Hernández A, Mascarua-Esparza MA, Martínez-Romero E, Caballero-Mellado J (1997) Coffea arabica L., a new host plant for Acetobacter diazotrophicus, and isolation of other nitrogen-fixing acetobacteria. Appl Environ Microbiol 63:3676–3683

    PubMed Central  PubMed  Google Scholar 

  • Josey DP, Beynon JL, Johnston AWB, Beringer JE (1979) Strain identification in Rhizobium using intrinsic antibiotic resistance. J Appl Bacteriol 46:343–50

    Article  Google Scholar 

  • Juraeva D, George E, Davranov K, Ruppel S (2006) Detection and quantification of the nifH gene in shoot and root of cucumber plants. Can J Microbiol 52:731–739

    Article  CAS  PubMed  Google Scholar 

  • Kennedy IR, Choudhury ATMA, Kecskés ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems; can their potential for plant growth promotion be better explained? Soil Biol Biochem 36:1229–1244

    Article  CAS  Google Scholar 

  • Kennedy N, Egger KN (2010) Impact of wildfire intensity and logging on fungal and nitrogen-cycling bacterial communities in British Columbia forest soils. Forest Ecol Manag 260:787–794

    Article  Google Scholar 

  • Kim Y, Wegner CE, Liesack W (2014) Soil metatranscriptomic. In: Nannipieri P, Renella G, PIetramellara G (eds) Omics in soil science. Caster Academic Press, Norfolk

    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. Environ Microbiol 7:1725–1733

    Article  CAS  PubMed  Google Scholar 

  • Kolb W, Martin P (1988) Influence of nitrogen on the number of N2-fixing and total bacteria in the rhizosphere. Soil Boil Biochem 20:221–225

    Article  CAS  Google Scholar 

  • Liu XM, Zhao HX, Chen SF (2006) Colonization of maize and rice plants by strain Bacillus megaterium C4. Curr Microbiol 52:186–190

    Article  CAS  PubMed  Google Scholar 

  • Loaces I, Ferrando L, Fernandez Scavino A (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microb Ecol 61:606–618

    Article  PubMed  Google Scholar 

  • Loiret FG, Ortega E, Kleiner D, Ortega-Rode’s P, Rode’s P, Dong Z (2004) A putative new endophytic nitrogen-fixing bacterium Pantoea sp. from sugarcane. J Appl Microbiol 97:504–511

    Article  CAS  PubMed  Google Scholar 

  • Martin DE, Reinhold-Hurek B (2002) Distinct roles of PII-like signal transmitter protein and amtB. regulation of nif gene expression, nitrogenase activity, and posttranslational modification of NifH in Azoarcus sp. strain BH72. J Bacteriol 184:2251–2259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mehnaz S, Kowalik T, Reynolds B, Lazarovitz G (2010) Growth promoting effects of corn (Zea mays) bacterial isolates under greenhouse and field conditions. Soil Biol Biochem 42:1848–1856

    Article  CAS  Google Scholar 

  • Meng X, Wang L, Long X, Liu Z, Zhang Z, Zed R (2012) Influence of nitrogen fertilization on diazotrophic communities in the rhizosphere of the Jerusalem artichoke (Helianthus tuberosus L. Research Microbiol 163:349–356

    Article  CAS  Google Scholar 

  • Montañez A, Abreu C, Gill PR, Hardarson G, Sicardi M (2009) Biological nitrogen fixation in maize (Zea mays L.) by 15N isotope dilution and identification of associated culturable diazotrophs. Biol Fertil Soils 45:253–263

    Article  Google Scholar 

  • Montañez A, Rodriguez-Blanco A, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28

    Article  Google Scholar 

  • Muthukumarasamy R, Kang UG, Park KD, Jeon WT, Park CY, Cho YS, Kwon SW, Song J, Roh DH, 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 

  • Muthukumarasamy R, Revathi G, Lakshminarasimhan C (1999) Influence of N fertilization on the isolation of Acetobacter diazotrophicus and Herbaspirillum spp. from Indian sugarcane varieties. Biol Fertil Soils 29:157–164

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A (2014) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils 50:249–262

    Article  CAS  Google Scholar 

  • Nguyen TH, Deaker R, Kennedy IR, Roughley RJ (2003) The positive yield response of field-grown rice to inoculation with a multi strain biofertilizer in the Hanoi area, Vietnam. Symbiosis 35:231–245

    Google Scholar 

  • Ohkuma M, Noda S, Kudo T (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pariona-Llanos R, de Santi I, Ferrara F, Soto Gonzales HH, Ramos Barbosa H (2010) Influence of organic fertilization on the number of culturable diazotrophic endophytic bacteria isolated from sugarcane. Eur J Soil Biol 46:387–393

    Article  Google Scholar 

  • Park M, Chungwoo K, Jinchul Y, Lee H, Wansik S, Seunghwan K, Tongmin S (2005) Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol Res 160:127–133

    Article  CAS  PubMed  Google Scholar 

  • Piceno Y, Lovell C (2000) Stability in natural bacterial communities: I. Nutrient addition effects on rhizosphere diazotroph assemblage composition. Microb Ecol 39:32–40

    Article  CAS  PubMed  Google Scholar 

  • Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N (2009) The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L). Soil Ecol Appl 42:141–14

    Article  Google Scholar 

  • Reinhold-Hurek B, Hurek T, Claeyssens M, van Montagu M (1993) Cloning, expression in Escherichia coli, and characterization of cellulolytic enzymes of Azoarcus sp., a root invading diazotroph. J Bacteriol 175:7056–7065

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rennie RJ (1981) A single medium for the isolation of acetylene-reducing (dinitrogen-fixing) bacteria from soils. Can J Microbiol 27:8–14

    Article  CAS  PubMed  Google Scholar 

  • Riggs PJ, Chelious MK, Inguez AL, Kaeppler SM, Triplett EW (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust J Plant Physiol 28:8–14

    Google Scholar 

  • Rodríguez-Blanco A, Sicardi M, Frioni L (2010) Competition for nodule occupancy between introduced and native strains of Rhizobium leguminosarum biovar trifolii. Biol Fertil Soils 46:419–425

    Article  Google Scholar 

  • Roesch LFW, Camargo FAO, Bento FM, Triplett EW (2008) Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 302:91–104

    Article  CAS  Google Scholar 

  • Roesch LFW, Olivares F, Pereira L, Selbach PA, Saccol de Sá E, Camargo FAO (2006) Characterization of diazotrophic bacteria associated with maize: effect of plant genotype, ontogeny and nitrogen- supply. World J Microbiol Biotechnol 22:967–974

    Article  Google Scholar 

  • Roesch LFW, Passaglia LMP, Bento FM, Triplett EW, Camargo FAO (2007) Diversidade de bactérias diazotróficas endofíticas associadas a plantas de milho. R Bras Ci Solo 31:1367–1380

    Article  CAS  Google Scholar 

  • Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837

    Article  CAS  PubMed  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. LSMR 21:1–30

    Google Scholar 

  • Sajjad M, 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

    Article  Google Scholar 

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  • Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Cura JA (2009) Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biol Biochem 1:1768–1774

    Article  Google Scholar 

  • Solomon BD, Barnes JR, Halvorsen KE (2007) Grain and cellulosic ethanol: history, economics, and energy policy. Biomass Bioenerg 31:416–425

    Article  Google Scholar 

  • Tan Z, Hurek T, Reinhold-Hurek B (2003) Effect of N-fertilization, plant genotype and environmental conditions on nifH gene pools in roots of rice. Environ Microbiol 5:1009–1015

    Article  CAS  PubMed  Google Scholar 

  • Tan ZY, Peng GX, Xu PZ (2009) Diversity and high nitrogenase activity of endophytic diazotrophs isolated from Oryza rufipogon Griff. Chin Sci Bull 54:2839–2848

    Article  CAS  Google Scholar 

  • Taulé C, Mareque C, Barlocco C, Hackembruch F, Reis V, Sicardi M, Battistoni F (2012) Contribution of nitrogen fixation to sugarcane (Saccharum officinarum L.) growth by 15-N isotope dilution and identification of associated endophytic diazotrophs. Plant Soil 356:35–49

    Article  Google Scholar 

  • Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995) Remarkable N2- fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J Bacteriol 177:1414–1417

    PubMed Central  CAS  PubMed  Google Scholar 

  • Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence based PCR (rep-PCR). Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  • Wei CY, Lin L, Luo L-J, Xing Y-X, Hu C-J, Yang L-T, Y-R L, An Q (2014) Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol Fertil Soils 50:657–666

    Article  CAS  Google Scholar 

  • Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166

    Article  Google Scholar 

  • Yeager CM, Kornosky J, Housman DC, Grote EE, Belnap J, Kuske CR (2004) Diazotrophic community structure and function in two successional stages of biologicals crusts from the Colorado plateau and Chihuahuan desert. Appl Environ Microbiol 70:973–983

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yim WJ, Poonguzhali S, Madhaiyan M, Palaniappan P, Siddijee MA, Sa T (2009) Characterization of plant growth promoting diazotrophic bacteria isolated from field grown Chinese cabbage under different fertilization conditions. J Microbiol 47:147–155

    Article  CAS  PubMed  Google Scholar 

  • Zani S, Mellon MT, Collier JL, Zehr JP (2000) Expression of nifH genes in natural assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol 66:3119–3124

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554

    Article  CAS  PubMed  Google Scholar 

  • Zlotnikova AK, Kazakova ML, Zlotnikov KM, Kazakov AV, Umarov MM (2007) Physiological and biochemical properties of the bacterial association of Klebsiella terrigena E6 and Bacillus firmus E3. Appl Biochem Microbiol 43:304–312

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partially supported by PEDECIBA (Programa de Desarrollo de Ciencias Básicas), UdelaR, Uruguay. Andrea Rodríguez-Blanco thanks the Agencia Nacional de Investigación e Innovación (ANII) for awarding a Ph. D. grant.

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  1. Laboratorio de Microbiología, Departamento de Biología Vegetal. Facultad de Agronomía, Universidad de la República, Av. Garzón 780. CP, 12900, Montevideo, Uruguay

    Andrea Rodríguez-Blanco & Lillian Frioni

  2. Laboratorio de Microbiología del Suelo, Instituto de Ecología y Ciencias Ambientales (IECA). Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay

    Margarita Sicardi

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Rodríguez-Blanco, A., Sicardi, M. & Frioni, L. Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol Fertil Soils 51, 391–402 (2015). https://doi.org/10.1007/s00374-014-0986-8

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