Plant and Soil

, Volume 337, Issue 1–2, pp 469–480 | Cite as

Impact of inoculation with Azospirillum spp. on growth properties and seed yield of wheat: a meta-analysis of studies in the ISI Web of Science from 1981 to 2008

  • Stavros D. VeresoglouEmail author
  • George Menexes
Regular Article


Azospirillum spp. represents one of the most studied plant growth promoting bacteria. A meta-analysis was conducted on 59 available articles to evaluate the extent to which Azospirillum may contribute to wheat growth properties. A mean increase of 8.9% in seed yield and 17.8% in aboveground dry weight was found to result from inoculation of wheat with Azospirillum. However, key determinants for the plant growth promoting effect were found to be the amount of N fertilization applied–maximum plant growth promoting effect was reported in the absence of N fertilization- and identities of wheat cultivar—Triticum aestivum was superior to Triticum durum-and Azospirillum isolate—Azospirillum lipoferum was more effective than Azospirillum brasilense. Co-inoculation with Azotobacter tended to further increase the growth promoting effect of Azospirillum on seed yield. A weak relationship between plant growth promoting effect on seed yield and aboveground biomass was detected. Inoculation with Azospirillum decreased the shoot:root ratio of wheat in field trials; but for pot trials, a key determinant of the shoot:root effect was the size of the pot used. The authors, thus, raise the scepticism of whether the growth parameters recorded in pot trials are representative of those under field conditions. Results highlight the efficiency of Azospirillum as an inoculant of wheat.


Shoot:root ratio Azospirillum lipoferum Linear interpolation Azotobacter spp. Nitrogen fertilization Triticum aestivum 



The authors would like to thank professor D. S. Veresoglou for assistance in collecting the articles and comments to earlier versions of the manuscript. The authors are grateful to two anonymous reviewers for their extremely helpful comments throughout the submission process of the manuscript.

Supplementary material

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  1. Adams DC, Gurevitch J, Rosenberg S (1997) Resampling tests for meta-analysis of ecological data. Ecology 78:1277–1283CrossRefGoogle Scholar
  2. Amara MAT, Dahdoh MSA (1997) Effect of inoculation with plant—growth promoting rhizobacteria (PGPR) on yield and uptake of nutrients by wheat grown on sandy soils. Egyptian J Soil Sci 37:467–484Google Scholar
  3. Avivi Y, Feldman M (1982) The response of wheat to bacteria of the genus Azospirillum. Israel J Bot 31:237–245Google Scholar
  4. Baldani VLD, Baldani JI, Dobereiner J (1983) Effects of Azospirillum inoculation on root infection and nitrogen incorporation in wheat. Canadian J Microbiol 29:924–929CrossRefGoogle Scholar
  5. Baldani VLD, Alvarez M, Baldani JI, Dobereiner J (1986) Establishment of inoculated Azospirillum spp in the rhizosphere and in roots of field-grown wheat and sorghum. Plant Soil 90:35–46CrossRefGoogle Scholar
  6. Baldani VLD, Baldani JI, Dobereiner J (1987) Inoculation of field-grown wheat (Triticum aestivum) with Azospirillum spp in Brazil. Biol Fertil Soils 4:37–40Google Scholar
  7. Barik AK, Goswami A (2003) Efficacy of biofertilizers with nitrogen levels on growth, productivity and economics in wheat (Triticum aestivum). Indian J Agron 48:100–102Google Scholar
  8. Bashan Y, de-Bashan LE (2010) How the plant growth promoting bacterium Azospirillum promotes plant growth—A critical assessment. Adv Agron 108:77–136CrossRefGoogle Scholar
  9. Bashan Y, Dubrovsky JG (1996) Azospirillum spp. participation in dry matter partitioning in grasses at the whole plant level. Biol Fertil Soils 23:435–440CrossRefGoogle Scholar
  10. Bashan Y, Holguin G (1997) Azospirillum-plant relationships: environmental and physiological advances (1990–1996). Canadian J Microbiol 43:103–121CrossRefGoogle Scholar
  11. Bashan Y, Harrison SK, Whitmoyer RE (1990) Enhanced growth of wheat and soybean plants inoculated with Azospirillum brasilense is not necessarily due to general enhancement of mineral uptake. Appl Environ Microbiol 56:769–775PubMedGoogle Scholar
  12. Bashan Y, Holguin G, de Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural and environmental advances (1997–2003). Canadian J Microbiol 50:521–577CrossRefGoogle Scholar
  13. Bhattarai T, Hess D (1993) Yield responces of nepalese spring wheat (Triticum aestivum L) cultivars to inoculation with Azospirillum Spp of nepalese origin. Plant Soil 151:67–76CrossRefGoogle Scholar
  14. Bhattarai T, Hess D (1997) Growth and yield responses of a Nepalese spring wheat cultivar to the inoculation with Nepalese Azospirillum spp at various levels of nitrogen fertilization. Biol Fertil Soils 26:72–77CrossRefGoogle Scholar
  15. Boddey RM, Baldani VL, Baldani JI, Dobereiner J (1986) Effect of inoculation of Azospirillum spp on nitrogen accumulation by field-grown wheat. Plant Soil 95:109–121CrossRefGoogle Scholar
  16. Boranstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis. Wiley, New YorkCrossRefGoogle Scholar
  17. Caceres REA, Anta GG, Lopez JR, Di Ciocco CA, Basurco PJC, Parada JL (1996) Response of field-grown wheat to inoculation with Azospirillum brasilense and Bacillus polymyxa in the Semiarid region of Argentina. Arid Soil Res Rehabil 10:13–20Google Scholar
  18. Conover WJ (1980) Practical nonparametric statistics. Wiley, New YorkGoogle Scholar
  19. Creus CM, Sueldo RJ, Barassi CA (2004) Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Can J Bot 82:273–281CrossRefGoogle Scholar
  20. Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form and physiology. Oecologia 113:299–313CrossRefGoogle Scholar
  21. Dalta SOR, Hernandez RF, Alvarez GLM, Ronzelli P, Soccol CR (2004) Azospirillum sp inoculation in wheat, barley and oats seeds greenhouse experiments. Brazilian Arch Biol Tech 47:843–850Google Scholar
  22. Darmwal NS, Gaur AC (1988) Associative effect of cellulolytic fungi and Azospirillum lipoferum on yield and nitrogen uptake by wheat. Plant Soil 107:211–218CrossRefGoogle Scholar
  23. de Freitas JG (2000) Yield and N assimilation of winter wheat (Triticum aestivum L., var. Norstar) inoculated with rhizobacteria. Pedobiologia 44:97–104CrossRefGoogle Scholar
  24. Didonet AD, Rodrigues O, Kenner MH (1996) Nitrogen and dry matter accumulation in wheat plants inoculated with Azospirillum brasilense. Pesqui Agropecu Bras 31:645–651Google Scholar
  25. Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879Google Scholar
  26. Ebrahim MKH, Aly MM (2004) Physiological response of wheat to foliar application of zinc and inoculation with some bacterial fertilizers. J Plant Nutrition 27:1859–1874CrossRefGoogle Scholar
  27. El-Komy HM, Hamdia MA, El-Baki GKA (2003) Nitrate reductase in wheat plants grown under water stress and inoculated with Azospirillum spp. Biologia Plantarum 46:281–287CrossRefGoogle Scholar
  28. Eskew DL, Focht DD, Ting IP (1977) Nitrogen fixation, denitrification and pleiomorphic growth of a highly pigmented Spirillum lipoferum. Appl Environ Microbiol 34:582–585PubMedGoogle Scholar
  29. Fayez M, Emam NF, Makboul HE (1985) The possible use of nitrogen fixing Azospirillum as biofertilizer for wheat plants. Egypt J Microbiol 20:199–206Google Scholar
  30. Gaballeromellado J, Carcamontiel MG, Mascaruaesparza MA (1992) Field inoculation of wheat (Triticum aestivum) with Azospirillum brasilense under temperate climate. Symbiosis 13:243–253Google Scholar
  31. Gaikwad AP, Bhate SB (1996) Effect of different strains of Azospirillum on yield of wheat. J Environ Biol 17:305–309Google Scholar
  32. Galai YGM (2003) Assessment of nitrogen availability to wheat (Triticum aestivum L.) from inorganic and organic N sources as affected by Azospirillum brasilense and Rhizobium leguminosarum inoculation. Egypt J Microbiol 38:57–73Google Scholar
  33. Galai YGM, Thaber EMA (2002) Effect of soybean residues, Azospirillum and fertilizer-N on nitrogen accumulation and biological fixation in two wheat cultivars. Egypt J Microbiol 37:15–27Google Scholar
  34. Ganguly TK, Jana AK, Moitra DN (1999) An evaluation of agronomic potential of Azospirillum brasilense and Bacillus megaterium in fibre-legume-cereal system in an Aeric Haplaquept. Indian J Agric Res 33:35–39Google Scholar
  35. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analysis. Ecology 80:1142–1149CrossRefGoogle Scholar
  36. Hartmann A, Baldani JI (2003) The genus Azospirillum. In: Dworkin M, Rosenberg S, Schleifer KH, Stackebrandt E (eds) The prokaryotes, 3rd edn. Springer, New YorkGoogle Scholar
  37. Hoeksema JD, Forde SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. Am Nat 171:275–290CrossRefPubMedGoogle Scholar
  38. Ishac YZ, Elhaddad ME, Daft MJ, Ramadan EM, Eldemerdash ME (1986) Effect of seed inoculation, mycorrhizal infection and organic ammendment on wheat growth. Plant Soil 90:373–382CrossRefGoogle Scholar
  39. Kapulnik Y, Kigel J, Okon Y, Nur I, Henis Y (1981) Effect of Azospirillum inoculation on some growth-parameters and N-content of wheat, sorghum and panicum. Plant Soil 61:65–70CrossRefGoogle Scholar
  40. Kapulnik Y, Sarig S, Nur I, Okon Y (1983) Effect of Azospirillum inoculation on yield of field-grown wheat. Can J Microbiol 29:895–899CrossRefGoogle Scholar
  41. Kapulnik Y, Feldman M, Okon Y, Henis Y (1985) Contribution of nitrogen fixed by Azospirillum to the N nutrition of spring wheat in Israel. Soil Biol Biochem 17:509–515CrossRefGoogle Scholar
  42. Kapulnik Y, Okon Y, Henis Y (1987) Yield response of spring wheat cultivars (Triticum aestivum and Triticum turgidum) to inoculation with Azospirillum brasilense under field conditions. Biol Fertil Soils 4:27–35Google Scholar
  43. Kucey RMN (1988) Plant growth-altering effects of Azospirillum brasilense and Bacillus C-11-25 on 2 wheat cultivars. J Appl Bacteriol 64:187–195Google Scholar
  44. Lauwong MM (1987) Field testing of the effectiveness of bacterial fertilizer in Nepal. Agric Ecos Environ 19:145–153CrossRefGoogle Scholar
  45. Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204CrossRefPubMedGoogle Scholar
  46. Lipsey MW, Wilson DB (2001) Practical meta-analysis. SAGE Publications, Thousand OaksGoogle Scholar
  47. McDaniel MA (2005) Big-brained people are smarter: a meta-analysis of the relationship between in vivo brain volume and intelligence. Intelligence 33:337–346CrossRefGoogle Scholar
  48. Mehta C, Patel R (1996) SPSS exact tests 7.0 for Windows. SPSS IncGoogle Scholar
  49. Mertens T, Hess D (1984) Yield increases in spring wheat (Triticum aestivum L.) inoculated with Azospirillum lipoferum under greenhouse and field conditions of a temperate region. Plant Soil 82:87–99CrossRefGoogle Scholar
  50. Millet E, Feldman M (1984) Yield response of a common spring wheat cultivar to inoculation with Azospirillum brasilense at various levels of nitrogen-fertilization. Plant Soil 80:255–259CrossRefGoogle Scholar
  51. Millet E, Avivi Y, Deldman M (1984) Yield response of various wheat genotypes to inoculation with Azospirillum brasilense. Plant Soil 80:261–266CrossRefGoogle Scholar
  52. Millet E, Avivi Y, Feldman M (1985) Effects of rhizospheric bacteria on wheat yield under field conditions. Plant Soil 86:347–355CrossRefGoogle Scholar
  53. Okon Y, Labandeea-Gonzalez CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years of worldwide field inoculation. Soil Biol Biochem 26:1591–1601CrossRefGoogle Scholar
  54. Ozturk A, Caglar O, Sahin F (2003) Yield response of wheat and barley to inoculation of plant growth promoting rhizobacteria at various levels of nitrogen fertilization. J Plant Nutr Soil Sci 166:262–266CrossRefGoogle Scholar
  55. Panwar JDS (1991) Effect of VAM and Azospirillum brasilence on photosynthesis nitrogen metabolism and grain yield in wheat. Indian J Plant Physiol 34:357–361Google Scholar
  56. Panwar JDS (1992) Effect of VAM and Azospirillum inoculation on metabolic changes and grain yield of wheat under moisture stress condition. Indian J Plant Physiol 35:157–161Google Scholar
  57. Panwar JDS, Singh O (2000) Response of Azospirillum and Bacillus on growth and yield of wheat under field conditions. Indian J Plant Physiol 5:108–110Google Scholar
  58. Panwar JDS, Pandey M, Abrol YP (1990) Effect of Azospirillum brasilense on photosynthesis transpiration and yield of wheat under low fertility conditions. Indian J Plant Physiol 33:185–189Google Scholar
  59. Pozzo MG, Giorgetti H, Martinez R, Aschkar G, Margiotta F (1993) Wheat inoculation with native strains of Azospirillum: field-experiments carried out in Patagones district. Investig Agrar Prod Prot Veg 8:49–54Google Scholar
  60. Pradhan S, Mohan J (1998) Response of cereals to Azospirillum brasilense. Indian J Agricul Sci 68:701–703Google Scholar
  61. Rai SN, Gaur AC (1982) Nitrogen-fixation by Azospirillum spp and effect of Azospirillum lipoferum on the yield and N-uptake of wheat crop. Plant Soil 69:233–238CrossRefGoogle Scholar
  62. Rai SN, Gaur AC (1988) Characterization of Azotobacter spp and effect of Azotobacter and Azospirillum as inoculant on the yield and N-uptake of wheat crop. Plant Soil 109:131–134CrossRefGoogle Scholar
  63. Ram T, Mir MS (2006) Effect of integrated nutrient management on yield and yield-attributing characters of wheat (Triticum aestivum). Indian J Agron 51:189–192Google Scholar
  64. Reynders L, Vlassak K (1982) Use of Azospirillum brasilense as biofertilizer in intensive wheat cropping. Plant Soil 66:217–223CrossRefGoogle Scholar
  65. Rodrigues O, Didonet AD, Gouveia JA, Soares RC (2000) Nitrogen translocation in wheat inoculated with Azospirillum and fertilized with nitrogen. Pesqui Agropecu Bras 35:1473–1481Google Scholar
  66. Saha KC, Sannigrahi S, Ghosh TK (1990) Response of wheat to Azospirillum inoculation in presence of nitrogen and phosphorus fertilizer. J Indian Soc Soil Sci 38:322–324Google Scholar
  67. Sala VMR, Cardoso EJBN, de Freitas JG, da Silveira APD (2007) Wheat genotypes response to inoculation of diazotrophic bacteria in field conditions. Pesqui Agropecu Bras 42:833–842Google Scholar
  68. Sala VMR, Cardoso EJBN, de Freitasm JG, da Silveira APD (2009) Interaction of new diazotrophic endophytic bacteria and nitrogen fertilization on wheat crop under field conditions. Rev Bras Cienc Solo 32:1099–1106Google Scholar
  69. 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
  70. Sawarkar SD, Goydani BM (1996) Effect of fertilizer and Azospirillum on grain yield of rainfed wheat (Triticum aestivum). Indian J Agron 41:409–411Google Scholar
  71. Singh O, Panwar JDS (1997) Effect of nitrogen fixing and phosphorus solubilising bacteria on nutrient uptake and yield of wheat. Indian J Plant Physiol 2:211–213Google Scholar
  72. Singh CS, Amawate JS, Tyagi SP, Kapoor A (1990) Interaction effect of Glomus fasciculatum and Azospirillum brasilense on yields of various genotypes of wheat (Triticum aestivum) in pots. Zbl Mikrobiol 145:203–208Google Scholar
  73. Singh RK, Singh SK, Singh LB (2007) Integrated nitrogen management in wheat (Triticum aestivum). Indian J Agron 52:124–126Google Scholar
  74. Steenhoodt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506CrossRefGoogle Scholar
  75. Swdrzynska D (2000) Effect of inoculation with Azospirillum brasilense on development and yielding of winter wheat and oat under different cultivation conditions. Pol J Environ Stud 9:423–428Google Scholar
  76. Tarrand JJ, Krieg NR, Dobereiner J (1978) A taxonomy study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980CrossRefPubMedGoogle Scholar
  77. Thuler DS, Floh EIS, Handro W, Barbosa HR (2003) Plant growth regulators and amino acids released by Azospirillum sp in chemically defined media. Lett Appl Microbiol 37:174–178CrossRefPubMedGoogle Scholar
  78. van Dommelen A, Vanderleyden J (2007) Associative nitrogen fixation. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, AmsterdamGoogle Scholar
  79. Vande Broek A, Dobbelaere S, Vanderleyden J, van Dommelen A (2000) Azospirillum-plant interactions: signaling and metabolic interactions. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Wymondham, pp 761–777Google Scholar
  80. Waremboiurg FR, Dreessen R, Vlassak K, Lafont F (1987) Peculiar effect of Azospirillum inoculation on growth and nitrogen-balance of winter-wheat (Triticum aestivum). Biol Fertil Soils 4:55–59Google Scholar
  81. Wilson D B (2005) Meta-analysis macros for SAS, SPSS and Stata. Retrieved March, 24, 2010 from
  82. Zambre MA, Konde BK (1990) Growth and yield responses of wheat cultivars to inoculation with N2-fixing bacteria under field conditions. Int J Trop Agric 8:109–116Google Scholar
  83. Zar J (1996) Biostatistical analysis. Prentice Hall International, Inc, New JerseyGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Environmental and Geographical SciencesManchester Metropolitan UniversityManchesterUK
  2. 2.Laboratory of Agronomy, School of AgricultureAristotle University of ThessalonikiThessalonikiGreece

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