Plant and Soil

, Volume 255, Issue 2, pp 571–586 | Cite as

Plant growth promoting rhizobacteria as biofertilizers

  • J. Kevin Vessey
Article

Abstract

Numerous species of soil bacteria which flourish in the rhizosphere of plants, but which may grow in, on, or around plant tissues, stimulate plant growth by a plethora of mechanisms. These bacteria are collectively known as PGPR (plant growth promoting rhizobacteria). The search for PGPR and investigation of their modes of action are increasing at a rapid pace as efforts are made to exploit them commercially as biofertilizers. After an initial clarification of the term biofertilizers and the nature of associations between PGPR and plants (i.e., endophytic versus rhizospheric), this review focuses on the known, the putative, and the speculative modes-of-action of PGPR. These modes of action include fixing N2, increasing the availability of nutrients in the rhizosphere, positively influencing root growth and morphology, and promoting other beneficial plant–microbe symbioses. The combination of these modes of actions in PGPR is also addressed, as well as the challenges facing the more widespread utilization of PGPR as biofertilizers.

Diazotrophs endophytes growth-promotion phytohormones rhizosphere root morphology 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abdel-Magid H M, Abdel-Aal S I, Rabie R K and Sabrah R E A 1995 Chicken manure as a biofertilizer for wheat in the sandy soils of Saudi Arabia. J. Arid Environ. 29, 413–420.Google Scholar
  2. An Q L, Yang X J, Dong Y M, Feng L J, Kuang B J and Li J D 2001 Using confocal laser scanning microscope to visualize the infection of rice roots by GFP-labelled Klebsiella oxytoca SA2, an endophytic diazotroph. Acta Bot. Sinica 43, 558–564.Google Scholar
  3. Andrade G, DeLeij F A and Lynch J M 1998 Plant mediated interactions between Pseudomonas fluorescens, Rhizobium leguminosarum and arbuscular mycorrhizae on pea. Lett. Appl. Microbiol. 26, 311–316.Google Scholar
  4. Andrews J H and Harris R F 2000 The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathal. 38, 145–180.Google Scholar
  5. Antoun H, Beauchamp C J, Goussard N, Chabot R and Lalande R 1998 Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204, 57–67.Google Scholar
  6. Azcon R 1993 Growth and nutrition of nodulated mycorrhizal and non-mycorrhizal Hedysarum coronarium as a result of treatment with fractions from a plant growth-promoting rhizobacteria. Soil Biol. Biochem. 25, 1037–1042.Google Scholar
  7. Baldani J I, Caruso L, Baldani V L D, Goi S R and Döbereiner J 1997 Recent advances in BNF with non-legume plants. Soil Biol. Biochem. 29, 911–922.Google Scholar
  8. Baldani V L D, Baldani J I and Döbereiner J 2001 Inoculation of rice plants with the endophytic diazatrophs Herbaspirillum seropedicae and Burkholderia spp. Biol. Fertil. Soils 30, 485–491.Google Scholar
  9. Barazani O and Friedman J 1999 Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J. Chem. Ecol. 25, 2397–2406.Google Scholar
  10. Barber S A and Cushman J H 1981 Nitrogen uptake model for agronomic crops. In Modeling Wastewater Renovation-land Treatment. Ed. I K Iskander. pp. 382–409. Wiley-Interscience, New York.Google Scholar
  11. Barber S A and Silverbush M 1984 Plant root morphology and nutrient uptake. In Roots, Nutrient and Water Influx, and Plant Growth, ASA Special Publication Number 49. Eds. S A Barber, D R Bouldin, D M Kral and S L Hawkins. pp. 65–88. American Society of Agronomy, Madison, WI.Google Scholar
  12. Bar-Ness E, Chen Y, Hadar H, Marschner H and Romheld V 1991 Siderophores of Pseudomonas putida as an iron source for dicot and monocot plants. Plant Soil 130, 231–241.Google Scholar
  13. Bar-Ness E, Hadar Y, Chen Y, Romheld V and Marschner H 1992 Short-term effects of rhizosphere microorganisms on Fe uptake from microbial siderophores by maize and oat. Plant Physiol. 100, 451–456.Google Scholar
  14. Bashan Y and Dubrovsky J G 1996 Azospirillum spp. participation in dry matter partitioning in grasses at the whole plant level. Biol. Fertil. Soils 23, 435–440.Google Scholar
  15. Belimov A A, Safronova V I, Sergeyeva T A, Egorova T N, Matveyeva V A, Tsyganov V E, Borisov A Y, Tikhonovich I A, Kluge C, Preisfeld A, Dietz K J and Stepanok V V 2001 Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol. 47, 642–652.Google Scholar
  16. Bent E, Tuzun S, Chanway C P and Enebak S 2001 Alterations in plant growth and in root hormone levels of lodgepole pines inoculated with rhizobacteria. Can. J. Microbiol. 47, 793–800.Google Scholar
  17. Bergman B, Johansson C and Soderback E 1992 The Nostoc– Gunnera symbiosis. New Phytol. 122, 379–400.Google Scholar
  18. Bertrand H, Nalin R, Bally R and Cleyet-Marel J C 2001 Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biol. Fertil. Soils 33, 152–156.Google Scholar
  19. Bethlenfalvay G J 1993 Mycorrhizae in the agricultural plant–soil system. Symbiosis 14, 413–425.Google Scholar
  20. Bevivino A, Sarrocco S, Dalmastri C, Tabacchioni S, Cantale C and Chiarini L 1998 Characterization of a free-living maizerhizosphere population of Burkholderia cepacia: effect of seed treatment on disease suppression and growth promotion of maize. FEMS Microbiol. Ecol. 27, 225–237.Google Scholar
  21. Boddey R M, Baldani V L D, Baldani J I and Döbereiner J 1986 Effect of inoculation of Azospirillum spp. on nitrogen accumulation by field-grown wheat. Plant Soil 95, 109–121.Google Scholar
  22. Boddey R M, Polidoro J C, Resende A S, Alves B J R and Urquiaga S 2001 Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses. Aust. J. Plant Physiol. 28, 889–895.Google Scholar
  23. Bullied JW, Buss T J and Vessey J K 2002 Bacillus cereus UW85 inoculation effects on the growth, nodulation, and N accumulation in grain legumes: Field studies. Can. J. Plant Sci 82, 291–298.Google Scholar
  24. Burd G I, Dixon D G and Glick B R 1998 A plant growthpromoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol. 64, 3663–3668.Google Scholar
  25. Burdman S, Volpin H, Kapulnik Y and Okon Y 1996 Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) root inoculated with Azospirillum brasilense Cd. Appl. Environ. Microbiol. 62, 3030–3033.Google Scholar
  26. Buss T J 1998 Effects of co-inoculation with Bacillus cereus UW85 and (Brady)Rhizobia on the nodulation, nitrogen fixation and dry matter accumulation of grain legumes.MSc Thesis, University of Manitoba.Google Scholar
  27. Cattelan A J, Hartel P G and Fuhrmann J J 1999 Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci. Soc. Am. J. 63, 1670–1680.Google Scholar
  28. Chabot R, Beauchamp C J, Kloepper J W and Antoun H 1998 Effect of phosphorus on root colonization and growth promotion of maize by bioluminescent mutants of phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Soil Biol. Biochem. 30, 1615–1618.Google Scholar
  29. Chanway C P, Hynes R K and Nelson L M 1989 Plant growthpromoting rhizobacteria: Effects on growth and nitrogen fixation of lentil (Lens esculenta Moench) and pea (Pisum sativum L.). Soil Biol. Biochem. 21, 511–517.Google Scholar
  30. Chen T W, Scherer S and Boger P 1993 Nitrogen fixation of Azorhizobium in artificially induced root para-nodules in wheat. Curr. Plant Sci. Biotechnol. Agric. 14, 593–606.Google Scholar
  31. Chew K. 2002. Georgics. Hackett Publishing Company. Indianapolis, USA. 152 pp.Google Scholar
  32. Christiansen-Weniger C 1996 Endophytic establishment of Azorhizobium caulinodans through auxin-induced root tumors of rice (Oryza sativa L.). Biol. Fertil. Soils 21, 293–302.Google Scholar
  33. Christiansen-Weniger C and Vanderleyden J 1994 Ammoniumexcreting Azospirillum sp. become intracellularly established in maize (Zea mays) para-nodules. Biol. Fertil. Soils 17, 1–8.Google Scholar
  34. Costacurta A, Keijers V and Vanderleyden J 1994 Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3-pyruvate decarboxylase gene. Mol. Gen. Genet. 243, 463–472.Google Scholar
  35. Dashti N, Zhang F, Hynes R and Smith D L 1997 Application of plant growth-promoting rhizobacteria to soybean [Glycine max (L.) Merr.] increases protein and dry matter yield under shortseason conditions. Plant Soil 188, 33–41.Google Scholar
  36. Dashti N, Zhang F, Hynes R and Smith D L 1998 Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil 200, 205–213.Google Scholar
  37. de Freitas J R 2000 Yield and N assimilation of winter wheat (Triticum aestivum L., var. Norstar) inoculated with rhizobacteria. Pedobiologia 44, 97–104.Google Scholar
  38. de Freitas J R, Banerjee M R and Germida J J 1997 Phosphatesolubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol. Fertil. Soils 24, 358–364.Google Scholar
  39. de Salamone I E G, Dobereiner J, Urquiaga S and Boddey R M 1996 Biological nitrogen fixation in Azospirillum strain-maize genotype associations as evaluated by the 15N isotope dilution technique. Biol. Fertil. Soils 23, 249–256.Google Scholar
  40. de Salamone I E G, Hynes R K and Nelson L M 2001 Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can. J. Microbiol. 47, 404–411.Google Scholar
  41. Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A and Vanderleyden J 1999 Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212, 155–164.Google Scholar
  42. 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 and Okon Y 2001 Responses of agronomically important crops to inoculation with Azospirillum. Aust. J. Plant Physiol. 28, 871– 879.Google Scholar
  43. Dong Z, Canny M J, McCully M E, Roboredo M R, Cabadilla C F, Ortega E and Rodes R 1994 A nitrogen-fixing endophyte of sugarcane stems. A new role for the apoplast. Plant Physiol. 105, 1139–1147.Google Scholar
  44. Dong Z, McCully M E and Canny M J 1997 Does Acetobacter diazotrophicus live and move in the xylem of sugarcane stems? Anatomical and physiological data. Ann. Bot. 80, 147–158.Google Scholar
  45. Duijff B J, de Kogel W J, Bakker P A H M and Schippers B 1994 Influence of pseudobactin 358 on the iron nutrition of barley. Soil Biol. Biochem. 26, 1681–1688.Google Scholar
  46. Egener T, Hurek T and Reinhold-Hurek B 1999 Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Mol. Plant Microbe Interact. 12, 813–819.Google Scholar
  47. Elo S, Maunuksela L, Salkinoja-Salonen M, Smolander A and Haahtela K 2000 Humus bacteria of Norway spruce stands: plant growth promoting properties and birch, red fescue and alder colonizing capacity. FEMS Microbiol. Ecol. 31, 143–152.Google Scholar
  48. Fallik E, Sarig S and Okon Y 1994 Morphology and physiology of plant roots associated with Azospirillum. In Azospirillum/plant associations. Ed. Y Okon. pp. 77–86. CRC Press Boca Raton, FL, USA.Google Scholar
  49. Franke I H, Fegan M, Hayward C, Leonard G and Sly L I 2000 Molecular detection of Gluconacetobacter sacchari associated with the pink sugarcane mealybug Saccharicoccus sacchari (Cockerell) and the sugarcane leaf sheath microenvironment by FISH and PCR. FEMS Microbiol. Ecol. 31, 61–71.Google Scholar
  50. Fred E B, Baldwin I L and McCoy E 1932 Root Nodule Bacteria and Leguminous Plants. University of Wisconsin, Madison, WI, USA. 343 pp.Google Scholar
  51. Frey-Klett P, Churin J L, Pierrat J C and Garbaye J 1999 Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries. Soil Biol. Biochem. 31, 1555–1562.Google Scholar
  52. Frommel MI, Nowak J and Lazarovits G 1991 Growth enhancement and developmental modifications of in vitro grown potato (Solanum tuberosum ssp. tuberosum) as affected by a nonfluorescent Pseudomonas sp. Plant Physiol. 96, 928–936.Google Scholar
  53. Fuentes-Ramirez L E, Caballero-Mellado J, Sepulveda J and Martinez-Romero E 1999 Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol. Ecol. 29 117–128.Google Scholar
  54. Galleguillos C, Aguirre C, Barea J M and Azcon R 2000 Growth promoting effect of two Sinorhizobium meliloti strains (a wild type and its genetically modified derivative) on a non-legume plant species in specific interaction with two arbuscular mycorrhizal fungi. Plant Sci. 159, 57–63.Google Scholar
  55. Gantar M and Elhai J 1999 Colonization of wheat para-nodules by the N2-fixing cyanobacterium Nostoc sp. strain 2S9B. New Phytol. 141, 373–379.Google Scholar
  56. Garbaye J 1994 Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol. 128, 197–210.Google Scholar
  57. Geric B, Rupnik M and Kraigher H 2000 Isolation and identification of mycorrhization helper bacteria in Norway spruce, Picea abies (L.) Karst. Phyton 40, 65–70.Google Scholar
  58. German M A, Burdman S, Okon Y and Kigel J 2000 Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol. Fertil. Soils 32, 259–264.Google Scholar
  59. Germida J J and Walley F L 1996 Plant growth-promoting rhizobacteria alter rooting patterns and arbuscular mycorrhizal fungi colonization of field-grown spring wheat. Biol. Fertil. Soils 23, 113–120.Google Scholar
  60. Glass A D M 1989 Plant Nutrition: An Introduction to Current Concepts. Jones and Bartlett Publishers, Boston, MA, USA. 234 pp.Google Scholar
  61. Glick B R 1995 The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 41, 109–117.Google Scholar
  62. Glick B R, Penrose D M and Li J P 1998 A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J. Theor. Biol. 190, 63–68.Google Scholar
  63. Gresshoff P M, Newton S, Mohapatra S S, Scott K F, Howitt S, Price G D, Bender G L, Shine J and Rolfe B G 1984 Symbiotic nitrogen fixation involving Rhizobium and the non-legume Parasponia. Adv. Agric. Biotechnol. 4, 483–489.Google Scholar
  64. Grichko V P and Glick B R 2001 Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol. Biochem. 39, 11–17.Google Scholar
  65. Griffiths B S, Ritz K, Ebblewhite N and Dobson G 1999 Soil microbial community structure: effects of substrate loading rates. Soil Biol. Biochem. 31 145–153.Google Scholar
  66. Gualtieri G and Bisseling T 2000 The evolution of nodulation. Plant Mol. Biol. 42 181–194.Google Scholar
  67. Gutierrez-Manero F J, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo F R and Talon M 2001 The plant-growthpromoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plant. 111, 206–211.Google Scholar
  68. Hansen A P 1994 Symbiotic N2 Fixation of Crop Legumes. Margraf Verlag, Weikershein, Germany. 248 pp.Google Scholar
  69. Hashem MA 2001 Problems and prospects of cyanobacterial biofertilizer for rice cultivation. Aust. J. Plant Physiol. 28, 881–888.Google Scholar
  70. Hiifte M, Vande Woestyne M and Verstraete W 1994 Role of siderophores in plant growth promotion and plant protection by fluorescent pseudomonads. In Biochemistry of Metal Micronutrients in the Rhizosphere. Eds. J A Manthey, D E Crowley and D G Luster. pp. 81–92. Lewis Publishers, Boca Raton, FL, USA.Google Scholar
  71. Hilali A, Prevost D, Broughton W J and Antoun H 2001 Effects of inoculation with strains of Rhizobium leguminosarum biovar trifolii on the growth of wheat in two different Morrocan soils. Can. J. Microbiol. 47, 590–593.Google Scholar
  72. Holguin G and Glick B R 2001 Expression of the ACC deaminase gene from Enterobacter cloacae UW4 in Azospirillum brasilense. Microbial Ecol. 41, 281–288.Google Scholar
  73. Hurek T, Reinhold-Hurek B, van Montagu M and Kellenberger E 1994 Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J. Bacteriol. 176, 1913–1923.Google Scholar
  74. Hurek T, Handley L L, Reinhold-Hurek B and Piche Y 2002 Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol. Plant Microbe Interact. 15, 233–242.Google Scholar
  75. Huss-Danell K 1997 Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol. 136, 375–405.Google Scholar
  76. Isopi R, Fabbri P, Del-Gallo M and Puppi G 1995 Dual inoculation of Sorghum bicolor (L.) Moench ssp. bicolor with vesicular arbuscular mycorrhizas and Acetobacter diazotrophicus. Symbiosis 18, 43–55.Google Scholar
  77. Jacoud C, Job D, Wadoux P and Bally R 1999 Initiation of root growth stimulation by Azospirillum lipoferum CRT1 during maize seed germination. Can. J. Microbiol. 45, 339–342.Google Scholar
  78. James E K and Olivares F L 1998 Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit. Rev. Plant Sci. 17, 77–119.Google Scholar
  79. James E K, Olivares F L, Baldani J I and Dobereiner J 1997 Herbaspirillum, an endophytic diazotroph colonizing vascular tissue in leaves of Sorghum bicolor L. Moench. J. Exp. Bot. 48, 785–797.Google Scholar
  80. James E K, Olivares F L, de Oliveira A L M, dos Reis F B, da Silva L G and Reis V M 2001 Further observations on the interaction between sugar cane and Gluconacetobacter diazotrophicus under laboratory and greenhouse conditions. J. Exp. Bot. 52, 747–760.Google Scholar
  81. James E K, Gyaneshwar P, Mathan N, Barraquio Q L, Reddy P M, Iannetta P P M, Olivares F L, Ladha J K 2002 Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67 Mol. Plant Microbe. Interact. 15, 894–906.Google Scholar
  82. Kaushik R, Saxena A K, Tilak K V B R 2000 Selection of Tn5::lacZ mutants isogenic to wild type Azospirillum brasilense strains capable of growing at sub-optimal temperature. World J. Microbiol. Biotechnol. 16, 567–570.Google Scholar
  83. Kim K Y, Jordan D and McDonald G A 1998 Effect of phosphatesolubilizing bacteria and vesicular–arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol. Fertil. Soils 26, 79–87.Google Scholar
  84. Kloepper J W and Schroth M N 1978 Plant growth-promoting rhizobacteria on radishes. In Proceedings of the 4th International Conference on Plant Pathogenic Bacteria. pp. 879–882. Gilbert-Clarey, Tours, France.Google Scholar
  85. Knight T J and Langston-Unkefer P J 1988 Enhancement of symbiotic dinitrogen fixation by a toxin-releasing plant pathogen. Science 241, 951–954.Google Scholar
  86. Korzhenevskaya T G, Lobakova E S, Dol'nikova G A and Gusev M V 1999 Topography of microsymbionts in apogeotropic roots of the cycads Cycas revoluta Thunb. and Encephalartos horridus (Jacq.) Lehm. Microbiology 68, 437–442.Google Scholar
  87. Koval'skaya N Y, Lobakova E S and Umarov M M 2001 The formation of artificial nitrogen-fixing symbioses with rape (Brassica napus var. napus) plants in nonsterile soil. Microbiology 70, 606–612.Google Scholar
  88. Kovtunovych G, Lar O, Kamalova S, Kordyum V, Kleiner D and Kozyrovska N 1999 Correlation between pectate lyase activity and ability of diazotrophic Klebsiella oxytoca VN 13 to penetrate into plant tissues. Plant Soil 215, 1–6.Google Scholar
  89. Kumar V and Narula N 1999 Solubilization of inorganic phosphates and growth emergence of wheat as affected by Azotobacter chroococcum mutants. Biol. Fertil. Soils 28, 301–305.Google Scholar
  90. Li D M and Alexander M 1988 Co-inoculation with antibioticproducing bacteria to increase colonization and nodulation by rhizobia. Plant Soil 108, 211–219.Google Scholar
  91. Li J, Ovakim D H, Charles T C and Glick B R 2000 An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Curr. Microbiology 41, 101–105.Google Scholar
  92. Ma W, Zalec K and Glick B R 2001 Biological activity and colonization pattern of the bioluminesence-labeled plant growthpromoting bacterium Kluyvera ascorbata SUD165/26. FEMS Microbiol. Ecol. 35, 137–144.Google Scholar
  93. Malik K A, Bilal R, Mehnaz S, Rasul G, Mirza M S and Ali S 1997 Association of nitrogen-fixing, plant promoting rhizobacteria (PGPR) with kallar grass and rice. Plant Soil 194, 37–44.Google Scholar
  94. Marek-Kozaczuk M and Skorupska A 2001 Production of B-group vitamins by plant growth-promoting Pseudomonas fluorescens strain 267 and the importance of vitamins in the colonization and nodulation of red clover. Biol. Fertil. Soils 33, 146–151.Google Scholar
  95. Marschener H 1998 Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crops Res. 56, 203–207.Google Scholar
  96. Masalha J, Kosegarten H, Elmaci Ö and Mengel K 2000 The central role of microbial activity for iron acquisition in maize and sunflower. Biol. Fertil. Soils 30, 433–439.Google Scholar
  97. Mayak S, Tirosh T and Glick B R 1999 Effect of wild-type and mutant plant growth-promoting rhizobacteria on the rooting of mung bean cuttings. J. Plant Growth Regul. 18, 49–53.Google Scholar
  98. McCully M E 1987 Selected aspects of the structure and development of field-grown roots with special reference to maize. In Root Development and Function. Eds. P J Gregory, J V Lake and D A Rose. pp. 53–70. Cambridge University Press, Cambridge, UK.Google Scholar
  99. McCully M E 2001 Niches for bacterial endophytes in crop plants: a plant biologist's view. Aust. J. Plant Physiol. 28, 983–990.Google Scholar
  100. Mehnaz S, Mirza MS, Haurat J, Bally R, Normand P, Bano A, Malik K A 2001 Isolation and 16S rRNA sequence analysis of the beneficial bacteria from the rhizosphere of rice. Can. J. Microbiol. 472, 110–117.Google Scholar
  101. Michiels K W, Croes C L and Vanderleyden J 1991 Two different modes of attachment of Azospirillum brasilense, a gram negative nitrogen-fixing bacterium. J. Gen. Microbiol. 137, 2241–2246.Google Scholar
  102. Mirza M S, Ahmad W, Latif F, Haurat J, Bally R, Normand P and Malik K A 2001 Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant Soil 237, 47–54.Google Scholar
  103. Molla A H, Shamsuddin Z H, Halimi M S, Morziah M and Puteh A B 2001 Potential for enhancement of root growth and nodulation of soybean co-inoculated with Azospirillum and Bradyrhizobium in laboratory systems. Soil Biol. Biochem. 33, 457–463.Google Scholar
  104. Mrkovacki N and Milic V 2001 Use of Azotobacter chroococcum as potentially useful in agricultural application. Ann. Microbiol. 51, 145–158.Google Scholar
  105. Nautiyal C S, Bhadauria S, Kumar P, Lal H, Mondal R and Verma D 2000 Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol. Lett. 182, 291–296.Google Scholar
  106. Ness R L L and Vlek P L G 2000 Mechanism of calcium and phosphate release from hydroxy-apatite by mycorrhizal hyphae. Soil Sci. Soc. Am. J. 64, 949–955.Google Scholar
  107. Noel T C, Sheng C, Yost C K, Pharis R P and Hynes M F 1996 Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can. J. Microbiol. 42, 279–283.Google Scholar
  108. Obreht Z, Kerby NW, Gantar M and Rowell P 1993 Effects of rootassociated N2-fixing cyanobacteria on the growth and nitrogen content of wheat (Triticum vulgare L.) seedlings. Biol. Fertil. Soils 15, 68–72.Google Scholar
  109. O'Callaghan K J, Dixon R A and Cocking E C 2001 Arabidopsis thaliana: a model for studies of colonization by nonpathogenic and plant-growth-promoting rhizobacteria. Aust. J. Plant Physiol. 28, 975–982.Google Scholar
  110. O'Donnell A G, Seasman M, Macrae A, Waite I and Davies J T 2000 Plants and fertilisers as drivers of change in microbial community structure and function in soils. Plant Soil 232, 135–145.Google Scholar
  111. Okon Y and Labandera-Gonzalez CA 1994 Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol. Biochem. 26, 1591–1601.Google Scholar
  112. Omar M N A, Mahrous N M and Hamouda A M 1996. Evaluating the efficiency of inoculating some diazatrophs on yield and protein content of 3 wheat cultivars under graded levels of nitrogen fertilization. Ann. Agric. Sci. 41, 579–590.Google Scholar
  113. Pal S S 1998 Interactions of an acid tolerant strain of phosphate solubilizing bacteria with a few acid tolerant crops. Plant Soil 198, 169–177.Google Scholar
  114. Pandey A, Sharma E and Palni L M S 1998 Influence of bacterial inoculation on maize in upland farming systems of the Sikkim Himalaya. Soil Biol. Biochem. 30, 379–384.Google Scholar
  115. Peters G A and Meeks J C 1989 The Azolla-Anabaena symbiosis: basic biology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 193–210.Google Scholar
  116. Peterson C A and Moon G J 1993 The effect of lateral root outgrowth on the structure and permeability of the onion root exodermeis. Bot. Acta 106, 411–418.Google Scholar
  117. Phillips D A, Joseph C M, Yang G P, Martinez-Romero E, Sanborn J R and Volpin H 1999 Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth. Proc. Natl. Acad. Sci. USA 96, 12275–12280.Google Scholar
  118. Pimentel J P, Olivares F, Pitard R M, Urquiaga S, Akiba F and Dobereiner J 1991 Dinitrogen fixation and infection of grass leaves by Pseudomonas rubrisubalbicans and Herbaspirillum seropedicae. Dev. Plant Soil Sci. 48, 225–229.Google Scholar
  119. Rao D L N and Gill H S 1995 Biomass and biofertilizer production by Sesbania cannabina in alkaline soil. Bioresource Tech. 53, 169–172.Google Scholar
  120. Ratti N, Kumar S, Verma H N and Gautam S P 2001 Improvement in bioavailability of tricalcium phosphate to Cymbopogon martinii var. motia by rhizobacteria, AMF and Azospirillum inoculation. Microbiol. Res. 156, 145–149.Google Scholar
  121. Raverkar K P and Konde BK 1988 Effect of Rhizobium and Azospirillum lipoferum inoculation on the nodulation, yield and nitrogen uptake of peanut cultivars. Plant Soil 106, 249–252.Google Scholar
  122. Requena N, Jimenez I, Toro M and Barea J M 1997 Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol. 136, 667–677.Google Scholar
  123. Revsbech N P, Pedersen O, Reichardt Wand Briones A 1999 Microsensor analysis of oxygen and pH in the rice rhizosphere under field and laboratory conditions. Biol. Fertil. Soils 29, 379–385.Google Scholar
  124. Richardson A E 2001 Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust. J. Plant Physiol. 28, 897–906.Google Scholar
  125. Riggs P J, Chelius M K, Iniguez A L, Kaeppler S M and Triplett E W 2001 Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust. J. Plant Physiol. 28, 829–836.Google Scholar
  126. Rodriguez H and Fraga R 1999 Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319–339.Google Scholar
  127. Rojas A, Holguin G, Glick B R and Bashan Y 2001 Synergism between Phyllobacterium sp. (N2-fixer) and Bacillus licheniformis (P-solubilizer), both from a semiarid mangrove rhizosphere. FEMS Microbiol. Ecol. 35, 181–187.Google Scholar
  128. Saleh S S and Glick B R 2001 Involvement of gacS and rpoS in enhancement of the plant growth-promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can. J. Microbiol. 47, 698–705.Google Scholar
  129. Salisbury F B 1994 The role of plant hormones. In Plant– Environment Interactions. Ed. R E Wilkinson. pp. 39–81. Marcel Dekker, New York, USA.Google Scholar
  130. Salisbury F B and Ross C W 1992 Plant Physiology, Wadsworth Pub. Co., Belmont, USA. 682 pp.Google Scholar
  131. Sarig S, Okon Y and Blum A 1992 Effect of Azospirillum brasilense inoculation on growth dynamics and hydraulic conductivity of Sorghum bicolor roots. J. Plant Nutr. 15, 805–819.Google Scholar
  132. Schloter M, Lebuhn M, Heulin T and Hartmann A 2000 Ecology and evolution of bacterial microdiversity. FEMS Microbiol. Rev. 24, 647–660.Google Scholar
  133. Schultze M and Kondorosi A 1998 Regulation of symbiotic root nodule development. Annu. Rev. Gen. 32, 33–57.Google Scholar
  134. Sessitsch A, Howieson J G, Perret X, Antoun H, Martinez-Romero E 2002 Advances in Rhizobium research. Crit. Rev. Plant Sci. 21, 323–378.Google Scholar
  135. Sevilla M, Burris R H, Gunapala N, Kennedy C 2001 Comparison of benefit to sugarcane plant growth and 15N2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and Nif- mutant strains. Mol. Plant Microbe. Interact. 14, 358–366.Google Scholar
  136. Shah S, Li J, Moffatt B A and Glick B R 1998 Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Can. J. Microbiol. 44, 833–843.Google Scholar
  137. Shishido M and Chanway C P 1998 Storage effects on indigenous soil microbial communities and PGPR efficacy. Soil Biol. Biochem. 30, 939–947.Google Scholar
  138. Shishido M, Breuil C and Chanway C P 1999 Endophytic colonization of spruce by plant growth-promoting rhizobacteria. FEMS Microbiol. Ecol. 29, 191–196.Google Scholar
  139. Singh S and Kapoor K K 1999 Inoculation with phosphatesolubilizing microorganisms and a vesicular arbuscular mycorrhizal fungus improves dry matter yield and nutrient uptake by wheat grown in a sandy soil. Biol. Fertil. Soils 28, 139–144.Google Scholar
  140. Singh C S and Subba Rao N S 1979 Associative effect of Azospirillum basilense with Rhizobium japonicum on nodulation and yield of soybean (Glycine max). Plant Soil 53, 387–392.Google Scholar
  141. Spaink H P 2000 Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54, 257–288.Google Scholar
  142. Spencer D, James E K, Ellis G J, Shaw J E and Sprent J I 1994 Interaction between rhizobia and potato tissues. J. Exp. Bot. 45, 1475–1482.Google Scholar
  143. Sprent J I 1990 Evolution, structure and function of nitrogen-fixing root nodules: Confessions of ignorance. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G. Stacey and W E Newton. pp. 45–54. Chapman and Hall, London, UK.Google Scholar
  144. Srinivasan M, Petersen D J and Holl F B 1996 Influence of indoleacetic-acid-producing Bacillus isolates on the nodulation of Phaseolus vulgaris by Rhizobium etli under gnotobiotic conditions. Can. J. Microbiol. 42, 1006–1014.Google Scholar
  145. Steenhoudt O and Vanderleyden J 2000 Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev. 24, 487–506.Google Scholar
  146. Stein T, Hayen-Schneg N and Fendrik I 1997 Contribution of BNF by Azoarcus sp. BH72 in Sorghum vulgare. Soil Biol. Biochem. 29, 969–971.Google Scholar
  147. Stevenson F J and Cole M A 1999 Cycles of Soil: Carbon, Nitrogen, Phosphorus, Sulfur, Micronutrients, 2nd Edition. Wiley, New York, USA. 427 pp.Google Scholar
  148. Suslow T V, Kloepper J W, Schroth M N and Burr T J 1979 Bene-ficial bacteria enhance plant growth Rhizobacteria. Calif. Agric. Exp. Stn. 33, 15–17.Google Scholar
  149. Tavaria F K and Zuberer D A 1998 Effect of low pO2 on colonization of maize roots by a genetically altered Pseudomonas putida [PH6(L1019)]. Biol. Fert. Soils 26, 43–49.Google Scholar
  150. Tchan Y T, Zeman A M M and Kennedy I R 1991 Nitrogen fixation in para-nodules of wheat roots by introduced free-living diazotrophs. Dev. Plant Soil Sci. 48, 269–273.Google Scholar
  151. Timmusk S, Nicander B, Granhall U and Tillberg E 1999 Cytokinin production by Paenibacillus polymyxa. Soil Biol. Biochem. 31, 1847–1852.Google Scholar
  152. Tisdale SL and Nelson WL 1975 Soil Fertility and Fertilizers, 3rd Edition. Macmillan Publishing, New York, USA. 694 pp.Google Scholar
  153. Toal M E, Yeomans C, Killham K and Meharg A A 2000 A review of rhizosphere carbon flow modelling. Plant Soil 222, 263–281.Google Scholar
  154. Tobar R, Azcon R and Barea J M 1994 Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol. 26, 119–122.Google Scholar
  155. Toro M, Azcon R and Barea J M 1997 Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphatesolubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl. Environ. Microbiol. 63, 4408–4412.Google Scholar
  156. Uren N C and Reisenauer H M 1988 The role of root exudates in nutrient acquisition. Adv. Plant Nutr. 3, 79–114.Google Scholar
  157. Vande Broek A, Lambrecht M, Eggermont K and Vanderleyden J 1999 Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J Bacteriol. 181, 1338–1342.Google Scholar
  158. Vazquez M M, Cesar S, Azcon R and Barea J M 2000a Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl. Soil Ecol. 15, 261–272.Google Scholar
  159. Vazquez P, Holguin G, Puente M E, Lopez-Cortez A and Bashan Y 2000b Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol. Fertil. Soils 30, 460–468.Google Scholar
  160. Vedder-Weiss D, Jurkevitch E, Burdman S, Weiss D and Okon Y 1999 Root growth, respiration and beta-glucosidase activity in maize (Zea mays) and common bean (Phaseolus vulgaris) inoculated with Azospirillum brasilense. Symbiosis 26, 363–377.Google Scholar
  161. Ventura W and Ladha J K 1997 Sesbania phosphorus requirements when used as biofertilizer for long-term rice cultivation. Soil Sci. Soc. Am. J. 61, 1240–1244.Google Scholar
  162. Verma S C, Ladha J K and Tripathi A K 2001 Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J. Biotechnol. 91, 127–141.Google Scholar
  163. Vessey J K and Buss T J 2002 Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes. Controlled-environment studies. Can. J. Plant Sci. 82, 282–290.Google Scholar
  164. Vessey J K and Heisinger K G 2001 Effect of Penicillium bilaii inoculation and phosphorus fertilization on root and shoot parameters of field-grown pea. Can. J. Plant Sci. 81, 361–366.Google Scholar
  165. Volkmar K M and Bremer E 1998 Effects of seed inoculation with a strain of Pseudomonas fluorescens on root growth and activity of wheat in well-watered and drought-stressed glass-fronted rhizotrons. Can. J. Plant Sci. 78, 545–551.Google Scholar
  166. von Wiren N, Khodr H and Hider R C 2000 Hydroxylated phytosiderophore species possess an enhanced chelate stability and affinity for iron(III). Plant Physiol. 124, 1149–1157.Google Scholar
  167. Vose P B and Ruschel A P 1981 Associative N2-Fixation, Volume 1. CRC Press, Boca Raton, FL, USA. 215 pp.Google Scholar
  168. Walley F L and Germida J J 1997 Response of spring wheat (Triticum aestivum) to interactions between Pseudomonas species and Glomus clarum NT4. Biol. Fertil. Soils 24, 365–371.Google Scholar
  169. Wang C, Knill E, Glick B R and Defago G 2000 Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHAO and its gacA derivative CHA96 on their growth-promoting and diseasesuppressive capacities. Can. J. Microbiol. 46, 898–907.Google Scholar
  170. Wang Y, Brown H N, Crowley D E and Szaniszlo P J 1993 Evidence for direct utilization of a siderophore, ferrioxamine B, in axenically grown cucumber. Plant Cell Environ. 16, 579–585.Google Scholar
  171. Wani S P 1986 Cereal Nitrogen Fixation: Proceedings of the Working Group Meeting Held at Icrisat Center, India, 9–12 October, 1984. ICRISAT, Patancheru, India. 128 pp.Google Scholar
  172. Whipps J M 2001 Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487–511.Google Scholar
  173. Xu H L 2000 Soil–root interface water potential in sweet corn as affected by organic fertilizer and a microbial inoculant. J. Crop Prod. 3, 139–156.Google Scholar
  174. Yanni Y G, Rizk R Y, Abd El-Fattah F K, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth R I, Martinez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Garcia M, Anarna J A, Rolfe B G, Ladha J K, Hill J, Mujoo R, Ng P K and Dazzo F B 2001 The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust. J. Plant Physiol. 28, 845–870.Google Scholar
  175. Youssef H, Monib M, Fayez M and Hegazi NA 1998 Induction of paranodulation by 2,4-D, IAA and tryptophan in wheat inoculated with various diazotrophs. Dev. Plant Soil Sci. 79, 43–150.Google Scholar
  176. Zehnder G W, Murphy J F, Sikora E J and Kloepper J W 2001 Application to rhizobacteria for induced resistance. Eur. J. Plant Pathol. 107, 39–50.Google Scholar
  177. Zhang F, Dashti N, Hynes R K and Smith D L 1996 Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann. Bot. 77, 453–459.Google Scholar
  178. Zhang F, Dashti N, Hynes R K and Smith D L 1997 Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] growth and physiology at suboptimal root zone temperatures. Ann. Bot. 79, 243–249.Google Scholar
  179. Zodape S T 2001 Seaweeds as a biofertilizer. J. Sci. Indust. Res. 60, 378–382.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • J. Kevin Vessey
    • 1
  1. 1.Department of Plant ScienceUniversity of ManitobaWinnipegCanada

Personalised recommendations