Skip to main content
SpringerLink
Log in

Plant growth promotion by four species of the genus Burkhoderia

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

Abstract

Background and aims

The genus Burkholderia is highly diverse and may mediate plant growth via several mechanisms. The current study evaluates the role of strains from four Burkholderia species in maize growth promotion.

Methods

Twenty three strains of diazotrophic Burkholderia species were applied to two maize genotypes (SHS5050 and BRS4157) under greenhouse and field conditions. Strains were tested for growth promotion in greenhouse during 40 days. Strain 41 from B. silvatlantica was used under field conditions. Parameters evaluated: biomass accumulation, N and root measurements in pots and grain yield, N % and N in the grains under field conditions.

Results

Eleven strains were evaluated under soil substrate. The inoculation of the hybrid SHS5050 showed root biomass improvement using three strains, namely M130, M209 and PPe7. The highest acetylene reduction activity was observed in strain 41 from B. silvatlantica. Strain 41 from B. silvatlantica improved plant dry mass on both genotypes. This strain produced 31 % more aerial tissue and 7 % more root dry mass in the BRS4157 variety than it did in the control. Both genotypes planted at Seropédica, RJ, produced 7 % more grains under field conditions and the variety produced 10.9 % more grains in comparison to the non-inoculated control.

Conclusion

Strain 41 from B. silvatlantica showed beneficial plant-growth promotion of maize under greenhouse and field experiments specially in a low fertility soil.

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
Fig. 2

Similar content being viewed by others

References

  • Alves GC, Videira SS, Urquiaga S, Reis VM (2015) Differential plant growth promotion and nitrogen fixation in two genotypes of maize by several Herbaspirillum inoculants. Plant Soil 387:307–321. doi:10.1007/s11104-014-2295-2

    Article  CAS  Google Scholar 

  • Anandham R, Indira Gandhi P, Kwon SW, Sa TM, Kim YK, Jee HJ (2009) Mixotrophic metabolism in Burkholderia kururiensis subsp. Thiooxydans subsp. nov., a facultative chemolithoautotrophic thiosulfate oxidizing bacterium isolated from rhizosphere soil and proposal for classification of the type strain of Burkholderia kururiensis as Burkholderia kururiensis subsp. kururiensis subsp. nov. Arch Microbiol 191:885–894. doi:10.1007/s00203-009-0517-4

    Article  CAS  PubMed  Google Scholar 

  • Anuar AR, Shemsuddin ZH, Okon Y (1995) Contribution of legume-N by nodulated groundnut for growth of maize on an acid soil. Soil Biol Biochem 27:595–601. doi:10.1016/0038-0717(95)98637-4

    Article  CAS  Google Scholar 

  • Araújo AES, Baldani VLD, Galisa PS, Pereira JA, Baldani JI (2013) 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 64:49–55. doi:10.1016/j.apsoil.2012.10.004

    Article  Google Scholar 

  • Balandreau J, Viallard V, Cournoyer B, Coenye T, Laevens S, Vandamme P (2001) Burkholderia cepacia genomovar III is a common plant-associated bacterium. Appl Environ Microbiol 67:982–985. doi:10.1128/AEM.67.2.982-985.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldani VLD, Oliveira E, Balota E, Baldani JI, Kirchhof G, Döbereiner J (1997) Burkholderia brasilensis sp. nov., uma nova espécie de bactéria diazotrófica endofítica. An Acad Bras Cienc 69:116

    Google Scholar 

  • Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biol Fertil Soils 30:485–491. doi:10.1007/s003740050027

    Article  Google Scholar 

  • Baldani JI, Reis VM, Videira SS, Boddey LH, Baldani VLD (2014) The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists. Plant Soil 384:413–431. doi:10.1007/s11104-2186-6

    Article  CAS  Google Scholar 

  • Boddey RM (1987) Methods for quantification of nitrogen fixation associated with gramineae. Crit Rev Plant Sci 6:209–266. doi:10.1080/07352688709382251

    Article  CAS  Google Scholar 

  • Bremner J, Mulvaney C (1982) Nitrogen—total. Methods of soil analysis part 2 chemical and microbiological properties. Meth Soil Anal 2:595–624

    Google Scholar 

  • Caballero-Mellado J, Onofre-Lemus J, Eestrada-de-Los Santos J, Martinez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319. doi:10.1128/AEM.00324-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro-Gonzalez R, Martinez-Aguilar L, Ramirez-Trujillo A, Estrada-de Los Santos P, Caballero-Mellado J (2011) High diversity of culturable Burkholderia species associated with sugarcane. Plant Soil 345:155–169. doi:10.1007/s11104-011-0768-0

    Article  CAS  Google Scholar 

  • Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729. doi:10.1046/j.1462-2920.2003.00471.x

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Nowak J, Coenye T, Clément C, Ait Barka E (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626. doi:10.1111/j.1574-6976.2008.00113.x

    Article  CAS  PubMed  Google Scholar 

  • Coutinho BG, Silva DP, Previato JO, Mendonça-Previato L, Venturi V (2013) Draft genome of the rice endophyte Burkholderia kururiensis M130. Genome Announc 1:e00225–e00212. doi:10.1128/genomeA.00225-12

    Article  PubMed Central  Google Scholar 

  • Estrada-De Los Santos P, Bustillos-Cristales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798. doi:10.1128/AEM.67.6.2790-2798.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Euclydes R (2004) Sistema para análises estatísticas (SAEG 9.0). Viçosa: Funarbe

  • Fages, J. Azospirillum inoculants and field experiments Y. Okon (Ed.), Azospirillum/plant associations, CRC Press, Boca Raton (1994), pp. 87–109

    Google Scholar 

  • Ferreira D (2010) Sisvar: versão 5.3. Lavras: UFLA

  • Fiore A, Laevens S, Bevivino A, Dalmastri C, Tabacchioni S, Vandamme P, Chiarini L (2001) Burkholderia cepacia complex: distribution of genomovars among isolates from the maize rhizosphere in Italy. Environ Microbiol 3:137–143. doi:10.1046/j.1462-2920.2001.00175.x

    Article  CAS  PubMed  Google Scholar 

  • Gillis M, Trân Van V, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis. sp. nov. for N2-fixing isolates from rice in Vietnam. J Syst Evol Microbiol 45:274–289

    CAS  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. Microb Ecol 55:21–37. doi:10.1007/s00248-007-9247-9

    Article  PubMed  Google Scholar 

  • Guimarães SL, Campos DTS, Baldani VLD, Jacob-Neto J (2010) Diazotrophic bacteria and nitrogen fertilization in rice cultivars. R Caatinga 23:32–39

    Google Scholar 

  • Halvorson AD, Peterson GA, Reule CA (2002) Tillage system and crop rotation effects on dry land crop yields and soil carbon in the central great plains. Agron J 94:1429–1436

    Article  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. doi:10.1007/s11104-009-0262-0

    Article  CAS  Google Scholar 

  • Ikeda AC, Bassani LL, Adamoski D, Stringari D, Cordeiro VK, Glienke C, Steffens MBR, Hungria M, Galli-Terasawa LV (2013) Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microb Ecol 65:154–160. doi:10.1007/s00248-012-0104-0

    Article  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J Mol Evol 16:111–120. doi:10.1007/Bf01731581

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zuo S, Zou YY, Wang JH (2012) Song W (2012) investigation of diversity and population succession dynamics of indigenous bacteria of the maize spermosphere. World J Microbiol Biotechnol 28:391–396. doi:10.1007/s11274-011-0822-3

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biolumin Chemilumin 193:265–275

    CAS  Google Scholar 

  • Luvizotto D, Marcon J, Andreote F, Dini-Andreote F, Neves A, Araújo W, Pizzirani-Kleiner A (2010) Genetic diversity and plant-growth related features of Burkholderia spp. from sugarcane roots. World J Microbiol Biotechnol 26:1829–1836. doi:10.1007/s11274-010-0364-0

    Article  CAS  Google Scholar 

  • Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156. doi:10.1038/nrmicro1085

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Aguilar L, Diaz R, Pena-Cabriales JJ, Estrada-de los Santos P, Dunn MF, Caballero-Mellado, J (2008) Multichromosomal genome structure and confirmation of diazotrophy in novel plant-associated Burkholderia species. Appl Environ Microbiol 74:4574–4579. doi:10.1128/AEM.00201-08

  • Mattos KA, Padua VL, Romeiro A, Hallack LF, Neves BC, Ulisses TM, Barros CF, Todeschini AR, Previato JO, Mendonca-Previato L (2008) Endophytic colonization of rice (Oryza sativa L.) by the diazotrophic bacterium Burkholderia kururiensis and its ability to enhance plant growth. An Acad Bras Cienc 80:477–493. doi:10.1590/S0001-37652008000300009

    Article  CAS  PubMed  Google Scholar 

  • Mehnaz S, Kowalik T, Reynolds B, Lazarovits G (2010) Growth promotion effects of corn (Zea mays) bacterial isolates under greenhouse and field conditions. Soil Biol Biochem 42:1848–1856. doi:10.1016/j.soilbio.2010.07.003

    Article  CAS  Google Scholar 

  • Montañez A, Blanco AR, 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. doi:10.1016/j.apsoil.2012.02.009

    Article  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of proteobacteria. Nature 411:948–950. doi:10.1038/35091106

    Article  CAS  PubMed  Google Scholar 

  • Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2013) Drought stress ameliotation in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73:121–131. doi:10.1007/s10725-013-9874-8

    Article  Google Scholar 

  • Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkolderia phytofirmans PsJN and Enterobacter sp FD17. Environ Exp Bot 97:30–39. doi:10.1016/j.envexpbot.2013.09.014

    Article  CAS  Google Scholar 

  • Oliveira ALM, Canuto EL, Reis VM, Baldani JI (2003) Response of micropropagated sugarcane varieties to inoculation with endophytic diazotrophic bacteria. Braz J Microbiol 34:59–61

    Article  Google Scholar 

  • Oliveira ALM, 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. doi:10.1007/s11104-006-0025-0

    Article  CAS  Google Scholar 

  • Paungfoo-Lonhienne C, Lonhienne TGA, Yeoh YK, Webb RI, Lakshmanan P, Chan CH, Lim P-E, Ragan MA, Schmidt S, Hugenholtz P (2014) A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microb Biotechnol 7:142–154. doi:10.1111/1751-7915.12105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perin L, Martinez-Aguilar L, Paredes-Valdez G, Baldani JI, Estrada-de Los Santos P, Reis VM, Caballero-Mellado J (2006) Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize. Int J Syst Evol Microbiol 56:1931–1937. doi:10.1099/ijs.0.64362-0

    Article  CAS  PubMed  Google Scholar 

  • Reis VM, Estrada-de Los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VL, Schmid M, Baldani JI, Balandreau J, Hartmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162. doi:10.1099/ijs.0.02879-0

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues EP, Rodrigues LS, de Oliveira ALM, Baldani VLD, Teixeira KRD, 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. doi:10.1007/s11104-007-9476-1

    Article  CAS  Google Scholar 

  • Rodrigues-Blanco A, Sicardi M, Frioni L (2015) 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. doi:10.1007/s00374-014-0986-8

    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. doi:10.1007/s11104-007-9458-3

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schloter M, Bode W, Hartmann A, Beese F (1992) Sensitive chemoluminescence-based immunological quantification of bacteria in soil extracts with monoclonal-antibodies. Soil Biol Biochem 24:399–403. doi:10.1016/0038-0717(92)90201-8

    Article  Google Scholar 

  • Schultz N, Morais RF, Silva JA, Baptista RB, Oliveira RP, Leite JM, Pereira W, Carneiro Júnior JB, Alves BJR, Baldani JI, Boddey RM, Urquiga S, Reis VM (2012) Avaliação agronômica de duas variedades de Cana de açúcar inoculadas com bactérias diazotróficas e adubadas com nitrogênio. Pesq Agrop Brasileira 47:261–268

    Article  Google Scholar 

  • Schultz N, da Silva JA, Sousa JS, Monteiro RC, Oliveira RP, Chaves VA, Pereira W, da Silva MF, Baldani JI, Boddey RM, Reis VM, Urquiaga S (2014) Inoculation of sugarcane with diazotrophic bacteria. Rev Bras Cienc Solo 38:407–414

    Article  Google Scholar 

  • Sessitsch A, Coenye T, Sturz AV, Vandamme P, Ait Barka E, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirman sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192. doi:10.1099/ijs.0.63149-0

    Article  CAS  PubMed  Google Scholar 

  • Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266. doi:10.1007/s00248-011-9929-1

    Article  PubMed  Google Scholar 

  • Scott A, Knott M (1974) A cluster analysis method for grouping means in the analysis of variance. Biometrics 30:507–512

  • 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. doi:10.1093/molbev/msr121

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tranvan V, Mavingui P, Berge O, Balandreau J, Heulin T (1994) Growth promotion of rice after inoculation with a nitrogen-fixing bacteria Burkholderia vietnamiensis isolated from an acid-sulfate soil in Vietnam. Agronomie 14:697–707. doi:10.1051/agro:19941006

    Article  Google Scholar 

  • Van VT, Berge O, Ke 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

    Article  CAS  Google Scholar 

  • Vargas L, de Carvalho TLG, Ferreira PCG, Baldani VLD, Baldani JI, Hermerly A (2012) Early responses of rice (Oriza sativa L.) seedlings to inoculation with beneficial diazotrophic bacteria are dependent on plant and bacterial genotypes. Plant Soil 356:127–137. doi:10.1007/s11104-012-1274-8

    Article  CAS  Google Scholar 

  • Zhang L, Xie G (2007) Diversity and distribution of Burkholderia cepacia complex in the rhizosphere of rice and maize. FEMS Microbiol Lett 266:231–235. doi:10.1111/j.1574-6968.2006.00530.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hanada S, Shigematsu T, Shibuya K, Kamagata Y, Kanagata T, Kurame R (2000) Burkholderia kururiensis sp.nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int J Syst Evol Microbiol 50:743–749

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was funded by Embrapa n. 02.05.1.06.00.01 and 02.09.01.11.00.06 and by INCT/CNPq Proc. no. 573828/2008-3. The authors would like to thank Universidade Federal Rural do Rio de Janeiro and the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES) for granting the postdoctoral scholarship to the first author, as well as the National Council for Scientific and Technological Development (CNPq) for the research scholarship granted to the last author. The study publication was authorized by Embrapa Agrobiologia Editorial Committee of Publication.

Author information

Authors and Affiliations

  1. Instituto de Agronomia, Departamento de Solos, Universidade Federal Rural do Rio de Janeiro, BR-465 Km 07., Seropédica, CEP 23890-000, Brazil

    Gabriela Cavalcanti Alves

  2. Embrapa Agrobiologia, km 07 BR 465, Seropédica, RJ, CEP 23891-000, Brazil

    Aline Vieira de Matos Macedo, Segundo Urquiaga & Veronica Massena Reis

  3. Embrapa Cerrados, Rodovia BR-020, km 18, Planaltina, DF, CEP 73310-970, Brazil

    Fabio Bueno dos Reis Jr.

Authors
  1. Gabriela Cavalcanti Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aline Vieira de Matos Macedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fabio Bueno dos Reis Jr.
    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. Veronica Massena Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Veronica Massena Reis.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Responsible Editor: Ian Dodd.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves, G.C., de Matos Macedo, A.V., dos Reis, F.B. et al. Plant growth promotion by four species of the genus Burkhoderia . Plant Soil 399, 373–387 (2016). https://doi.org/10.1007/s11104-015-2701-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2701-4

Keywords

Search

Navigation