Microbial Ecology

, Volume 58, Issue 4, pp 921–929 | Cite as

Plant Growth-Promoting Rhizobacteria Allow Reduced Application Rates of Chemical Fertilizers

  • A. O. Adesemoye
  • H. A. Torbert
  • J. W. Kloepper
Plant Microbe Interactions


The search for microorganisms that improve soil fertility and enhance plant nutrition has continued to attract attention due to the increasing cost of fertilizers and some of their negative environmental impacts. The objectives of this greenhouse study with tomato were to determine (1) if reduced rates of inorganic fertilizer coupled with microbial inoculants will produce plant growth, yield, and nutrient uptake levels equivalent to those with full rates of the fertilizer and (2) the minimum level to which fertilizer could be reduced when inoculants were used. The microbial inoculants used in the study were a mixture of plant growth-promoting rhizobacteria (PGPR) strains Bacillus amyloliquefaciens IN937a and Bacillus pumilus T4, a formulated PGPR product, and the arbuscular mycorrhiza fungus (AMF), Glomus intraradices. Results showed that supplementing 75% of the recommended fertilizer rate with inoculants produced plant growth, yield, and nutrient (nitrogen and phosphorus) uptake that were statistically equivalent to the full fertilizer rate without inoculants. When inoculants were used with rates of fertilizer below 75% of the recommended rate, the beneficial effects were usually not consistent; however, inoculation with the mixture of PGPR and AMF at 70% fertility consistently produced the same yield as the full fertility rate without inoculants. Without inoculants, use of fertilizer rates lower than the recommended resulted in significantly less plant growth, yield, and nutrient uptake or inconsistent impacts. The results suggest that PGPR-based inoculants can be used and should be further evaluated as components of integrated nutrient management strategies.


Fertilizer Rate Hoagland Solution Microbial Inoculant PGPR Strain Week After Planting 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are grateful to Ms. Sheryl Morey, a former technician at the National Soil Dynamics Laboratory in Auburn, a part of the Agricultural Research Services of United States Department of Agriculture, for her help during this study.


  1. 1.
    Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886CrossRefPubMedGoogle Scholar
  2. 2.
    Altomare C, Norvell WA, Bjorkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65:2926–2933PubMedGoogle Scholar
  3. 3.
    Amir HG, Shamsuddin ZH, Halimi MS, Marziah M, Ramlan MF (2005) Enhancement in nutrient accumulation and growth of oil palm seedlings caused by PGPR under field nursery conditions. Commun Soil Sci Plant Anal 36:2059–2066CrossRefGoogle Scholar
  4. 4.
    Aseri GK, Jain N, Panwar J, Rao AV, Meghwal PR (2008) Biofertilizers improve plant growth, fruit yield, nutrition, metabolism and rhizosphere enzyme activities of pomegranate (Punica granatum L.) in Indian Thar Desert. Sci Hortic 117:130–135CrossRefGoogle Scholar
  5. 5.
    Bakker PAHM, Raaijmakers JM, Bloemberg GV, Hofte M, Lemanceau P, Cooke M (2007) New perspectives and approaches in plant growth-promoting rhizobacteria research. Eur J Plant Pathol 119:241–242CrossRefGoogle Scholar
  6. 6.
    Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bonfante P, O'Gara F, Azcon-Anguilar C (1998) Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Appl Environ Microbiol 64:2304–2307PubMedGoogle Scholar
  7. 7.
    Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek 81:343–351CrossRefPubMedGoogle Scholar
  8. 8.
    Belimov AA, Kojemiakov AP, Chuvarliyeva CV (1995) Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant Soil 173:29–37CrossRefGoogle Scholar
  9. 9.
    Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650Google Scholar
  10. 10.
    Canbolat MY, Bilen S, Cakmakci R, Sahin F, Aydin A (2006) Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biol Fertil Soils 42:350–357CrossRefGoogle Scholar
  11. 11.
    Clarholm M (1985) Possible roles for roots, bacteria, protozoa, and fungi in supplying nitrogen in plants. Ecol Interact Soil 4:355–365Google Scholar
  12. 12.
    de Freitas JR Germida JJ (1990) Plant growth-promoting rhizobacteria for winter wheat. Can J Microbiol 36:265–272CrossRefGoogle Scholar
  13. 13.
    Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Anguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Response of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879Google Scholar
  14. 14.
    Egamberdiyeva D, Höflich G (2004) Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ 56:293–301CrossRefGoogle Scholar
  15. 15.
    Elkoca E, Kantar F, Sahin F (2008) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth, and yield of chickpea. J Plant Nutr 31:157–171CrossRefGoogle Scholar
  16. 16.
    Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242CrossRefGoogle Scholar
  17. 17.
    Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93CrossRefGoogle Scholar
  18. 18.
    Han HS, Lee KD (2005) Phosphate and potassium solubilizing bacteria effect on mineral uptake, soil availability, and growth of egg plant. Res J Agric Biol Sci 1:176–180Google Scholar
  19. 19.
    Hernandez MI, Chailloux M (2004) Las micorrizas arbusculares y las bacterias rizosfericas como alternativa a la nutricion mineral del tomate. Cult Trop 25(2):5–12Google Scholar
  20. 20.
    Hershley DR (1994) Solution culture hydroponics: history & inexpensive equipment. Am Biol Teach 56:111–118Google Scholar
  21. 21.
    Horwath WR, Paul EA (1994) Microbial biomass. In: Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A (eds) Methods of soil analysis, part 2, microbiological and biochemical properties-sssa book series, no. 5. Soil Science Society of America Inc, Madison, Wisconsin, USA, pp 753–773Google Scholar
  22. 22.
    Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Gilchrist K, Katupitiya S (1997) Biological nitrogen fixation in non-leguminous field crops: facilitating the evolution of an effective association between Azospirillum and wheat. Plant Soil 194:65–79CrossRefGoogle Scholar
  23. 23.
    Kloepper JW, Gutierrez-Estrada A, McInroy JA (2007) Photoperiod regulates elicitation of growth promotion but not induced resistance by plant growth-promoting rhizobacteria. Can J Microbiol 53:159–167CrossRefPubMedGoogle Scholar
  24. 24.
    Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS® for mixed models, 2nd edn. SAS Institute Inc, Cary, North Carolina, USA, pp 21–41Google Scholar
  25. 25.
    Lucy M, Reed E, Glick BR (2004) Application of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86:1–25CrossRefPubMedGoogle Scholar
  26. 26.
    Mahaffee WF, Kloepper JW (1997) Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.). Microb Ecol 34:210–223CrossRefPubMedGoogle Scholar
  27. 27.
    Malakoff D (1998) Coastal ecology: death by suffocation in the Gulf of Mexico. Science 281:190–192CrossRefGoogle Scholar
  28. 28.
    Maynard DN, Hochmuth GJ (2007) Knott's handbook for vegetable growers. 5th edn Wiley, Hoboken, New Jersey, pp. 65-68, 92-101, 170-213.Google Scholar
  29. 29.
    Mills HA, Jones JB (1996) Plant analysis handbook II: a practical sampling, preparation, analysis, and interpretation guide. Micromacro Publishing, Athens, Georgia, USA, pp. 6-18, 69, 81.Google Scholar
  30. 30.
    Olivares FL, Baldani VLD, Reis VM, Baldani JI, Döbereiner J (1996) Occurrence of the endophytic diazotroph Herbaspirillum spp. in roots, stems, and leaves predominantly of Gramineae. Biol Fertil Soils 2:197–200CrossRefGoogle Scholar
  31. 31.
    Probanza A, Mateos JL, Luca Garcia JA, Ramos B, de Felipe MR, Guiterrez Manero FJ (2001) Effects of inoculation with PGPR Bacillus and Pisolithus tinctorius on Pinus pinea L. growth, bacterial rhizosphere colonization and mycorrhizal infection. Microb Ecol 41:140–148PubMedGoogle Scholar
  32. 32.
    Raupach GS, Kloepper JW (2000) Biocontrol of cucumber diseases in the field by plant growth-promoting rhizobacteria with and without methyl bromide fumigation. Plant Dis 84:1073–1075CrossRefGoogle Scholar
  33. 33.
    Raynaud X, Lata JC, Leadley PW (2006) Soil microbial loop and nutrient uptake by plants: a test using a coupled C:N model of plant-microbial interactions. Plant Soil 287:95–116CrossRefGoogle Scholar
  34. 34.
    Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefPubMedGoogle Scholar
  35. 35.
    Runion GB, Prior SA, Reeves DW, Rogers HH, Reicosky DC, Peacock AD, White DC (2004) Microbial responses to wheel-traffic in conventional and no-tillage systems. Commun Soil Sci Plant Anal 35:2891–2903CrossRefGoogle Scholar
  36. 36.
    Ryu C-M, Murphy JF, Reddy MS, Kloepper JW (2007) A two-strain mixture of rhizobacteria elicits induction of systemic resistance against Pseudomonas syringae and Cucumber mosaic virus coupled to promotion of plant growth on Arabidopsis thaliana. J Microbiol Biotechnol 17:280–286PubMedGoogle Scholar
  37. 37.
    Saubidet MI, Fatta N, Barneix AJ (2002) The effect of inoculation with Azospirillum brasilense on growth and nitrogen utilization by wheat plants. Plant Soil 245:215–222CrossRefGoogle Scholar
  38. 38.
    Shaharooma B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155CrossRefGoogle Scholar
  39. 39.
    Tahmatsiodu V, O'Sullivan J, Cassells AC, Voyiatzis D, Paroussi G (2006) Comparison of AMF and PGPR inoculants for the suppression of Verticillium wilt of strawberry (Fragaria × ananassa cv. Selva). Appl Soil Ecol 32:316–324CrossRefGoogle Scholar
  40. 40.
    Vassey JK, Buss TJ (2002) Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes: controlled-environment studies. Can J Plant Sci 82:283–290Google Scholar
  41. 41.
    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 125:155–166CrossRefGoogle Scholar
  42. 42.
    Zhang S, Reddy MS, Kokalis-Burelle N, Wells LW, Nightengale SP, Kloepper JW (2001) Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Dis 85:879–884CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • A. O. Adesemoye
    • 1
  • H. A. Torbert
    • 2
  • J. W. Kloepper
    • 1
  1. 1.Department of Entomology & Plant PathologyAuburn UniversityAuburnUSA
  2. 2.USDA Agricultural Research ServicesNational Soil Dynamics LaboratoryAuburnUSA

Personalised recommendations