Screening of plant growth promotion ability among bacteria isolated from field-grown sorghum under different managements in Brazilian drylands

Abstract

Sorghum [Sorghum bicolor (L.) Moench] is a multipurpose grass cultivated in drylands due to its adaptation to drought. However the characteristics of sorghum-associated bacteria are not known in the Brazilian drylands. The aim of this study was to isolate and evaluate the plant growth promotion potential bacteria from field-grown sorghum under two irrigation and manure application levels in a Brazilian semi-arid reagion. Sorghum was irrigated with 3 or 1 mm day−1 and fertilized or not with liquid goat manure. Bacteria were obtained from surface-disinfected roots applying two nitrogen-free semi-solid media. The bacteria were evaluated for the presence of nifH gene, 16S rRNA sequences, calcium-phosphate solubilization, production of auxins and siderophores and for sorghum growth promotion. We obtained 20 out of 24 positive bacteria for nifH. The isolates were classified as in six different genera. All isolates produced auxins “in vitro”, six bacteria produced siderophores and three Enterobacteriaceae solubilized calcium-phosphate. At least ten bacteria resulted in the increased total N content in the sorghum shoots, comparable to fertilization with 50 mg N plant−1 week−1 and to inoculation with Azospirillum brasilense Ab-V5. Enterobacter sp. ESA 57 was the best sorghum plant-growth promoting bacteria isolated in this study.

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

Fig. 1
Fig. 2

References

  1. Andrade LF, de Souza GLOD, Nietsche S et al (2014) Analysis of the abilities of endophytic bacteria associated with banana tree roots to promote plant growth. J Microbiol 52:27–34. https://doi.org/10.1007/s12275-014-3019-2

    CAS  Article  PubMed  Google Scholar 

  2. Annicchiarico G, Caternolo G, Rossi E, Martiniello P (2011) Effect of manure vs. fertilizer inputs on productivity of forage crop models. Int J Environ Res Public Health 8:1893–1913. https://doi.org/10.3390/ijerph8061893

    Article  PubMed  PubMed Central  Google Scholar 

  3. Baldani JI, Reis VM, Videira SS et al (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. https://doi.org/10.1007/s11104-014-2186-6

    CAS  Article  Google Scholar 

  4. Baumhardt RL, Tolk JA, Howell TA, Rosenthal WD (2007) Sorghum management practices suited to varying irrigation strategies. Agron J 99:665–672. https://doi.org/10.2134/agronj2006.0092

    Article  Google Scholar 

  5. Bergamaschi C, Roesch LFW, Quadros PD de, Camargo FA de O (2007) Ocorrência de bactérias diazotróficas associadas a cultivares de sorgo forrageiro. Ciência Rural 37:727–733

    Article  Google Scholar 

  6. Berraquero FR, Baya B, Cormenzana AR (1976) Establecimiento de índices para el estudio de la solubilización de fosfatos por bacterias del suelo. Ars Pharm 17:399–406

    Google Scholar 

  7. Brady C, Cleenwerck I, Venter S et al (2013) Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov a. Syst Appl Microbiol 36:309–319. https://doi.org/10.1016/j.syapm.2013.03.005

    Article  PubMed  Google Scholar 

  8. Brígido C, Glick BR, Oliveira S (2017) Survey of plant growth-promoting mechanisms in native portuguese chickpea mesorhizobium isolates. Microb Ecol 73:900–915. https://doi.org/10.1007/s00248-016-0891-9

    Article  PubMed  Google Scholar 

  9. da Costa EM, Nóbrega RSA, de Carvalho F et al (2013) Plant growth promotion and genetic diversity of bacteria isolated from cowpea nodules. Pesqui Agropecu Bras 48:1275–1284. https://doi.org/10.1590/S0100-204X2013000900012

    Article  Google Scholar 

  10. de Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/S1415-475738420150053

    Article  PubMed  PubMed Central  Google Scholar 

  11. Döbereiner J, Baldani VLD, Baldani JI (1995) Como isolar e identificar bactérias diazotróficas de plantas não-leguminosas. Embrapa Agrobiologia, Seropédica

    Google Scholar 

  12. dos Santos MCM, dos Santos DR, Bakke A, Bakke IA (2013) Ocorrência e atividade de bactérias diazotróficas em forrageiras cultivadas na rregião semiárida do Brasil. Caatinga 26:27–34

    Google Scholar 

  13. dos Santos CLR, Alves GC, de Matos Macedo AV et al (2017) Contribution of a mixed inoculant containing strains of Burkholderia spp. and Herbaspirillum ssp. to the growth of three sorghum genotypes under increased nitrogen fertilization levels. Appl Soil Ecol 113:96–106. https://doi.org/10.1016/j.apsoil.2017.02.008

    Article  Google Scholar 

  14. Felestrino ÉB, Vieira IT, Caneschi WL et al (2018) Biotechnological potential of plant growth-promoting bacteria from the roots and rhizospheres of endemic plants in ironstone vegetation in southeastern Brazil. World J Microbiol Biotechnol 34:156. https://doi.org/10.1007/s11274-018-2538-0

    CAS  Article  PubMed  Google Scholar 

  15. Fernandes Júnior PI, Pereira GMD, Perin L et al (2013) Diazotrophic bacteria isolated from wild rice Oryza glumaepatula (Poaceae) in the Brazilian Amazon. Rev Biol Trop 61:991–999

    Article  Google Scholar 

  16. Fernandes-Júnior PI, Aidar de ST, Morgante CV, et al (2015) The resurrection plant Tripogon spicatus (Poaceae) harbors a diversity of plant growth promoting bacteria in northeastern Brazilian Caatinga. Rev Bras Cienc do Solo 39:993–1002. https://doi.org/10.1590/01000683rbcs20140646

    Article  Google Scholar 

  17. Ferrara FIS, Oliveira ZM, Gonzales HHS et al (2012) Endophytic and rhizospheric enterobacteria isolated from sugar cane have different potentials for producing plant growth-promoting substances. Plant Soil 353:409–417. https://doi.org/10.1007/s11104-011-1042-1

    CAS  Article  Google Scholar 

  18. Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cienc e Agrotecnol 35:1039–1042

    Article  Google Scholar 

  19. Fretes CE, De Suryani R, Purwestri YA, Nuringtyas TR (2018) Diversity of endophytic bacteria in sweet sorghum (Sorghum bicolor (L.) Moench) and their potential for promoting plant growth. Indian J Sci Technol 11:1–10. https://doi.org/10.17485/ijst/2018/v11i11/120283

    CAS  Article  Google Scholar 

  20. Govindasamy V, Raina SK, George P et al (2017) Functional and phylogenetic diversity of cultivable rhizobacterial endophytes of sorghum [Sorghum bicolor (L.) Moench]. Antonie Van Leeuwenhoek 110:925–943. https://doi.org/10.1007/s10482-017-0864-0

    CAS  Article  PubMed  Google Scholar 

  21. Hai B, Diallo NH, Sall S et al (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75:4993–5000. https://doi.org/10.1128/AEM.02917-08

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Haiyambo DH, Chimwamurombe PM, Reinhold-Hurek B (2015a) Isolation and screening of rhizosphere bacteria from grasses in East Kavango region of Namibia for plant growth promoting characteristics. Curr Microbiol 71:566–571. https://doi.org/10.1007/s00284-015-0886-7

    CAS  Article  PubMed  Google Scholar 

  23. Haiyambo DH, Reinhold-Hurek B, Chimwamurombe PM (2015b) Effects of plant g rowth promoting bacterial isol ates from Kavango on the vegetative growth of Sorghum bicolor. Afr J Microbiol Res 9:725–729

    Article  Google Scholar 

  24. Hons FM, Moresco RF, Wiedenfeld RP, Cothren JT (1986) Applied nitrogen and phosphorus effects on yield and nutrient uptake by high-energy sorghum produced for grain and biomass. Agron J 78:1069–1078. https://doi.org/10.2134/agronj1986.00021962007800060026x

    Article  Google Scholar 

  25. 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

    CAS  Article  Google Scholar 

  26. Hungria M, Nogueira MA, Araujo RS (2016) Inoculation of Brachiaria spp. with the plant growth-promoting bacterium Azospirillum brasilense: an environment-friendly component in the reclamation of degraded pastures in the tropics. Agric Ecosyst Environ 221:125–131. https://doi.org/10.1016/j.agee.2016.01.024

    CAS  Article  Google Scholar 

  27. Kämpfer P, Ruppel S, Remus R (2005) Enterobacter radicincitans sp. nov., a plant growth promoting species of the family Enterobacteriaceae. Syst Appl Microbiol 28:213–221. https://doi.org/10.1016/j.syapm.2004.12.007

    CAS  Article  PubMed  Google Scholar 

  28. Kavamura VN, Santos SN, Silva da JL, et al (2013a) Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol Res. https://doi.org/10.1016/j.micres.2012.12.002

    Article  PubMed  Google Scholar 

  29. Kavamura VN, Taketani RG, Lançoni MD et al (2013b) Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the brazilian caatinga biome. PLoS ONE. https://doi.org/10.1371/journal.pone.0073606

    Article  Google Scholar 

  30. Kruasuwan W, Thamchaipenet A (2016) Diversity of culturable plant growth-promoting bacterial endophytes associated with sugarcane roots and their effect of growth by co-inoculation of diazotrophs and actinomycetes. J Plant Growth Regul 35:1074–1087. https://doi.org/10.1007/s00344-016-9604-3

    CAS  Article  Google Scholar 

  31. Lin W, Okon Y, Hardy RWF (1983) Enhanced mineral uptake by Zea mays and Sorghum bicolor roots inoculated with Azospirillum brasilense. Appl Environ Microbiol 45:1775–1779

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lopes KBA, Carpentieri-Pipolo V, Oro TH et al (2016) Culturable endophytic bacterial communities associated with field-grown soybean. J Appl Microbiol 120:740–755. https://doi.org/10.1111/jam.13046

    CAS  Article  Google Scholar 

  33. Mando A, Ouattara B, Sédogo M et al (2005) Long-term effect of tillage and manure application on soil organic fractions and crop performance under Sudano-Sahelian conditions. Soil Tillage Res 80:95–101. https://doi.org/10.1016/j.still.2004.03.002

    Article  Google Scholar 

  34. Mareque C, Taulé C, Beracochea M, Battistoni F (2015) Isolation, characterization and plant growth promotion effects of putative bacterial endophytes associated with sweet sorghum (Sorghum bicolor (L) Moench). Ann Microbiol 65:1057–1067. https://doi.org/10.1007/s13213-014-0951-7

    CAS  Article  Google Scholar 

  35. Meng X, Bertani I, Abbruscato P et al (2015) Draft genome sequence of rice endophyte-associated isolate Kosakonia oryzae KO348. Genome Announc 3:e00594–e00515. https://doi.org/10.1128/genomeA.00594-15

    Article  PubMed  PubMed Central  Google Scholar 

  36. Pariona-Llanos R, Ferrara FIS, Gonzales HHS, Barbosa HR (2010) Influence of organic fertilization on the number of culturable diazotrophic endophytic bacteria isolated from sugarcane. Eur J Soil Biol 46:387–393. https://doi.org/10.1016/j.ejsobi.2010.08.003

    Article  Google Scholar 

  37. Pereira JAR, Cavalcante VA, Baldani JI, Döbereiner J (1989) Field inoculation of sorghum and rice with Azospirillum spp. and Herbaspirillum seropedicae. In: Skinner FA, Boddey RM, Fendrik I (eds) Nitrogen Fixation with Non-Legumes: The Fourth International Symposium on `Nitrogen Fixation with Non-Legumes’, Rio de Janeiro, 23–28 August 1987. Springer Netherlands, Dordrecht, pp 219–224

  38. 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

    CAS  Article  PubMed  Google Scholar 

  39. Ribeiro CM, Cardoso EJBN (2012) Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol Res 167:69–78. https://doi.org/10.1016/j.micres.2011.03.003

    CAS  Article  PubMed  Google Scholar 

  40. Rodrigues Neto J, Malavolta Jr VA , Victor O (1986) Meio simples para o isolamento e cultivo de Xanthomonas campestris pv. citri tipo B. Summa Phytopathol 12:32

    Google Scholar 

  41. Sánchez-Cañizares C, Jorrín B, Poole PS, Tkacz A (2017) Understanding the holobiont: the interdependence of plants and their microbiome. Curr Opin Microbiol 38:188–196. https://doi.org/10.1016/j.mib.2017.07.001

    CAS  Article  PubMed  Google Scholar 

  42. Sarathambal C, Ilamurugu K, Balachandar D et al (2015) Characterization and crop production efficiency of diazotrophic isolates from the rhizosphere of semi-arid tropical grasses of India. Appl Soil Ecol 87:1–10. https://doi.org/10.1016/j.apsoil.2014.11.004

    Article  Google Scholar 

  43. Sarwar M, Kremer RJ (1995) Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol 20:282–285. https://doi.org/10.1111/j.1472-765X.1995.tb00446.x

    CAS  Article  Google Scholar 

  44. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9

    CAS  Article  PubMed  Google Scholar 

  45. Sharma S, Singh DK (2017) Temporal variations in diazotrophic communities and nifH transcripts level across the agricultural and fallow land at Jaipur, Rajasthan, India. Indian J Microbiol 57:92–99. https://doi.org/10.1007/s12088-016-0634-0

    Article  PubMed  Google Scholar 

  46. Signor D, Cerri CEP (2013) Nitrous oxide emissions in agricultural soils: a review. Pesqui Agropecuária Trop 43:322–338. https://doi.org/10.1590/S1983-40632013000300014

    Article  Google Scholar 

  47. Silva K, Perin L, Gomes MDL et al (2016) Diversity and capacity to promote maize growth of bacteria isolated from the Amazon region. Acta Amaz 46:111–118. https://doi.org/10.1590/1809-4392201502502

    Article  Google Scholar 

  48. Sylvester-Bradley R, Asakawa N, La Torraca S et al (1982) Levantamento quantitativo de microrganismos solubilizadores de fosfatos na rizosfera de gramíneas e leguminosas forrageiras na Amazônia. Acta Amaz 12:15–22

    Article  Google Scholar 

  49. Valetti L, Iriarte L, Fabra A (2018) Growth promotion of rapeseed (Brassica napus) associated with the inoculation of phosphate solubilizing bacteria. Appl Soil Ecol 132:1–10. https://doi.org/10.1016/j.apsoil.2018.08.017

    Article  Google Scholar 

  50. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Witzel K, Strehmel N, Baldermann S et al (2017) Arabidopsis thaliana root and root exudate metabolism is altered by the growth-promoting bacterium Kosakonia radicincitans DSM 16656T. Plant Soil 419:557–573. https://doi.org/10.1007/s11104-017-3371-1

    CAS  Article  Google Scholar 

  52. Yoon S-H, Ha S-M, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755

    Article  PubMed  PubMed Central  Google Scholar 

  53. Zhang Y, Kang X, Liu H et al (2018) Endophytes isolated from ginger rhizome exhibit growth promoting potential for Zea mays. Arch Agron Soil Sci 64:1302–1314. https://doi.org/10.1080/03650340.2018.1430892

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Acknowledgments are given to Brazilian Council for Scientific and Technological Development (CNPq 485168/2013-8), to INCT—Plant Growth Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (CNPq/Fundação Araucária INCT-MPCPAgro 465133/2014-4) and the Brazilian Agricultural Research Corporation (Embrapa 03.13.08.003.00.00 and 06.13.06.002.00.00) by financial support. Acknowledgments are also given to the Science foundation of the Pernambuco State (FACEPE), for the scholarship to the first and second authors, and to Coordination of Improvement of Higher Education Personnel (CAPES) for providing the scholarship for the third to seventh authors. The last author is a research fellow of CNPq (311218/2017-2).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Paulo Ivan Fernandes-Júnior.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 15 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

da Silva, J.F., da Silva, T.R., Escobar, I.E.C. et al. Screening of plant growth promotion ability among bacteria isolated from field-grown sorghum under different managements in Brazilian drylands. World J Microbiol Biotechnol 34, 186 (2018). https://doi.org/10.1007/s11274-018-2568-7

Download citation

Keywords

  • Biological nitrogen fixation
  • Inoculant
  • Enterobacteriaceae
  • Plant growth promotion