Agronomy for Sustainable Development

, Volume 27, Issue 1, pp 29–43 | Cite as

Role of phosphate-solubilizing microorganisms in sustainable agriculture — A review

  • Mohammad Saghir Khan
  • Almas Zaidi
  • Parvaze A. Wani
Review Article

Abstract

Compared with the other major nutrients, phosphorus is by far the least mobile and available to plants in most soil conditions. Although phosphorus is abundant in soils in both organic and inorganic forms, it is frequently a major or even the prime limiting factor for plant growth. The bioavailability of soil inorganic phosphorus in the rhizosphere varies considerably with plant species, nutritional status of soil and ambient soil conditions. To circumvent phosphorus deficiency, phosphate-solubilizing microorganisms (PSM) could play an important role in supplying phosphate to plants in a more environmentally-friendly and sustainable manner. The solubilization of phosphatic compounds by naturally abundant PSM is very common under in vitro conditions; the performance of PSM in situ has been contradictory. The variability in the performance has thus greatly hampered the large-scale application of PSM in sustainable agriculture. Numerous reasons have been suggested for this, but none of them have been conclusively investigated. Despite the variations in their performance, PSM are widely applied in agronomic practices in order to increase the productivity of crops while maintaining the health of soils. This review presents the results of studies on the utilization of PSM for direct application in agriculture under a wide range of agro-ecological conditions with a view to fostering sustainable agricultural intensification in developing countries of the tropics and subtropics.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abd-Alla M.H. (1994) Solubilization of rock phosphates by Rhizobium and Bradyrhizobium, Folia Microbiol. 39, 53–56.CrossRefGoogle Scholar
  2. Ahmed S. (1995) Agriculture — Fertilizer Interface In Asia Issues of Growth and sustainability, Oxford and IBH publishing Co, New Delhi.Google Scholar
  3. Algawadi A.R., Gaur A.C. (1988) Associative effect of Rhizobium and phosphate solubilizing bacteria on the yield and nutrient uptake of chickpea, Plant Soil 105, 241–246.CrossRefGoogle Scholar
  4. Amann R.I. (1995) Fluorescently labeled rRNA targeted nucleotide probes in the study of microbial ecology, Microbial. Ecol. 4, 543–554.Google Scholar
  5. Ames R.N., Reid C.P.P., Ingham E.R. (1984) Rhizosphere bacterial population responses to root colonization by a vesicular arbuscular mycorrhizal fungus, New Phytol. 96, 555–563.CrossRefGoogle Scholar
  6. Amijee F., Tinker P.B., Stribley D.P. (1989) Effect of phosphorus on the morphology of vesicular-arbuscular mycorrhizal root system of leek (Allium porrum L.), Plant Soil 119, 334–336.CrossRefGoogle Scholar
  7. Antunes V., Cardoso E.J.B.E. (1991) Growth and nutrient status of citrus plants as influenced by mycorrhiza and phosphorus application, Plant Soil 131, 11–19.Google Scholar
  8. Asea P.E.A., Kucey R.M.N., Stewart J.W.B. (1988) Inorganic Phosphate solubilization by two Penicillium species in solution culture and soil, Soil Biol. Biochem. 20, 459–464.CrossRefGoogle Scholar
  9. Azaizeh H.A., Marshner A., Romheld V., Wittenmayer L. (1995) Effects of a vesicular-arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil grown maize plants, Mycorrhiza 5, 321–327.CrossRefGoogle Scholar
  10. Azcon-Aguilar C., Diaz-Rodriguez R., Barea J.M. (1986) Effect of soil microorganisms on spore germination and growth on the vesicular arbuscular mycorrhizal fungus (Glomus moseae), Trans. Brit. Mycol. Soc. 86, 337–340.CrossRefGoogle Scholar
  11. Babu-Khan S., Yeo T.C., Martin W.I., Duron M.R., Rogers R.D., Goldstein A.H. (1995) Cloning of a mineral phosphate solubilizing gene from Pseudomonas cepacia, Appl. Environ. Microbiol. 61, 972–978.PubMedGoogle Scholar
  12. Bagyaraj D.J. (1984). Biological interaction with VA mycorrhizal fungi, in: Powell C.L., Bagyaraj D.J. (Eds.), VA mycorrhiza, CRC Press, Boca Raton, pp. 131–153.Google Scholar
  13. Banik S., Dey B.K. (1982) Available phosphate content of an alluvial soil as influenced by inoculation of some isolated phosphate solubilizing microorganisms, Plant Soil 69, 353–364.CrossRefGoogle Scholar
  14. Banik S., Dey B.K. (1983) Phosphate solubilizing potentiality of the microorganisms capable of utilizing aluminium phosphate as a sole phosphate source, Zbl. Microbiol. 138, 17–23.Google Scholar
  15. Barber S.A. (1984) Soil nutrient bioavailability, John Wiley, New York, USA.Google Scholar
  16. Barea J.M., Azcon R., Azcon-Aguilar C. (1983) Interaction between phosphate solubilizing bacteria and VA mycorrhiza to improve the utilization of rock phosphate by plants in non acidic soils, Third Inter. Congress on Phosphorus Compounds, Brussels, pp. 127–152.Google Scholar
  17. Barea J.M., El-Atrach F., Azcon R. (1991) The role of VA mycorrhizas in improving plant N acquisition from soil as assessed with 15N. The use of stable isotopes in plant nutrition, in: Fitton C. (Ed.), Soil Fertility and Enviornmental Studies, Joint AIEA, FAO, Division, Vienna, pp. 677–808.Google Scholar
  18. Bar-Yosef B., Rogers R.D., Wolfram J.H., Richman E. (1999) Pseudomonas cepacia mediated rock phosphate solubilization in kaolinite and montmorillonite suspensions, Soil Sci. Soc. Am. J. 63, 1703–1708.CrossRefGoogle Scholar
  19. Bashan Y., Puente M.E., Rodriquea M.N., Toledo G., Holguin G., Ferrera-Cerrato R., Pedrin S. (1995) Survival of Azorhizobium brasilense in the bulk soil and rhizosphere of 23 soil types, Appl. Environ. Microbiol. 61, 1938–1945.PubMedGoogle Scholar
  20. Bethlenfalvay G.J. (1994) Sustainability and rhizoorganisms in an ecosystem, Sociedad Maxicana de la Ciencia del Suelo. 4, 9–10.Google Scholar
  21. Bolan N.S. (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plant, Plant Soil 134, 189–207.CrossRefGoogle Scholar
  22. Bolan N.S., Robson A.D., Barrow N.I. (1987) Effect of vesicular arbuscular mycorrhiza on availability of iron phosphates to plants, Plant Soil 99, 401–410.CrossRefGoogle Scholar
  23. Burgstaller W., Stxaser H., Shinner F. (1992) Solubilization of zinc oxide from filter dust with Penicillium simplicissimum: bioreactor, leaching and stoichiometry, Environ. Sci. Technol. 26, 340–346.CrossRefGoogle Scholar
  24. Burkert B., Robson A. (1994) Zn uptake in subterranean clover (Trifolium subterraneum 1.) by three vesicular-arbuscular mycorrhizal fungi in a root free sandy soil, Soil Biol. Biochem. 26, 1117–1124.CrossRefGoogle Scholar
  25. Chabot R., Anton H., Cescas M.P. (1996): Growth promotion of maize and lettuce by phosphate solubilizing Rhizobium leguminosarum biovar phaseoli, Plant Soil 184, 311–321.CrossRefGoogle Scholar
  26. Colbert S.F., Hendson M., Ferri M., Schroth M.N. (1993) Enhanced growth and activity of a biocontrol bacterium genetically engineered to utilize salicylate, Appl. Microbiol. 59, 2071–2076.Google Scholar
  27. Cooper J.E., Bjourson A.J., Streit W., Werner D. (1998) Isolation of unique nucleic acid sequence from rhizobia by genomic subtraction: Application in microbial ecology and symbiotic gene analysis, Plant Soil 204, 47–55.CrossRefGoogle Scholar
  28. Cruz R.E. de la., Manalo M.Q., Aggangan N.S., Tambalo J.D. (1988) Growth of three legume trees inoculated with VA mycorrhizal fungi and Rhizobium, Plant Soil 108, 111–115.CrossRefGoogle Scholar
  29. Cunningham J.E., Kuiack C. (1992) production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium bilaji, Appl. Environ. Microbiol. 58, 1451–1458.PubMedGoogle Scholar
  30. Downey J., Van Kessel C. (1990) Dual inoculation of Pisum sativum with Rhizobium leguminosarum and Penicillium bilaji, Biol. Fert. Soils 10, 194–196.Google Scholar
  31. Dubey S.K. (1996) Response of soybean to rock phosphate applied with Pseudomonas striata in a typic chromustert, J. Ind. Soc. Soil Sci. 44, 252–255.Google Scholar
  32. Dubey S.K., Billore S.D. (1992) Phosphate solubilizing microorganisms (PSM) as inoculant and their role in augmenting crop productivity in India, Crop Res. 5, 11.Google Scholar
  33. Dudeja S.S., Khurana A.L., Kundu B.S. (1981) Effect of Rhizobium and phosphomicroorganism on yield and nutrient uptake in chickpea, Curr. Sci. 50, 503.Google Scholar
  34. Dubey S.K. (2001) Associative effect of nitrogen fixing and phosphate solubilizing bacteria in rainfed soybean (Glycine max) grown in vertisols, Indian J. Agric. Sci. 71, 476–479.Google Scholar
  35. Duponnois R., Colombet A., Hien V., Thioulouse J. (2005) The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea, Soil Biol. Biochem. 37, 1460–1468.CrossRefGoogle Scholar
  36. Duponnois R., Kisa M., Plenchette C. (2006) Phosphate solubilizing potential of the nematofungus Arthrobotrys oligospora, J. Plant Nutr. Soil Sci. 169, 280–282.CrossRefGoogle Scholar
  37. Elgala H.M., Ishac Y.Z., Abdel-Monem M., El-Ghandour I.A.I., Hang P.M., Berthelin J., Bollag J.M., McGill W.B., Page A.I. (1995) Effect of single and combined inoculation with Azotobacter and VA mycorrhizal fungi on growth and nutrient content of maize and wheat plants, Environ. Impact Soil Component Interactions. 2, 109–116.Google Scholar
  38. Frederic B.G., Estefania A., Jordi B.F., Charles A.A., Dolors M.B., Manel P. (2000) Assessment of microbial community structure changes by amplified rhibosomal DNA restriction analysis (ARDRA), Int. Microbiol. 3, 103–106.Google Scholar
  39. Gaume A. (2000) Low P tolerance of various maize cultivars; the contribution of the root exudation, Ph.D. dissertation, Swiss Federal institute of Technology, Zurich, Switzerland.Google Scholar
  40. Gaur A.C. (1990) Phosphate solubilizing microorganisms as biofertilizers, Omega Scientific Publisher, New Delhi, p. 176.Google Scholar
  41. Giand S., Gaur A.C. (1991) Thermotolerant phosphate solubilizing microorganisms and their interactions in mungbean, Plant Soil 133, 141–149.CrossRefGoogle Scholar
  42. Glick B.R., Bashan Y. (1997) Genetic manipulation of plant growth promoting bacteria to enhance biocontrol of phytopathogens, Biotechnol. Adv. 15, 353–378.PubMedCrossRefGoogle Scholar
  43. Goldstein A.H., Rogers R.D., Mead G. (1993) Mining by microbe, Bio. Technol. 11, 1250–1254.Google Scholar
  44. Gupta R.R., Singal R., Shanker A., Kuhad R.C., Saxena R.K. (1994) A modified plate assay for secreening phosphate solubilizing microorganisms, J. Gen. Appl. Microbiol. 40, 255–260.CrossRefGoogle Scholar
  45. Guissou T., Bâ A.M., Guinko S., Plenchette C., Duponnois R. (2001) Mobilisation des phosphates naturels de kodijari par des jujubiers (Ziziphus mauritiana Lam.) mycorhizes dans un sol acidifié avec de la tourbe, Fruits 56, 261–269.CrossRefGoogle Scholar
  46. Gull M., Hafeez F.Y., Saleem M., Malik K.A. (2004) Phosphorus uptake and growth promotion of chickpea by co-inoculation of mineral phosphate solubilizing bacteria and a mixed rhizobial culture, Aust. J. Exp. Agr. 44, 623–628.CrossRefGoogle Scholar
  47. Gunasekaran S., Pandiyarajan P. (1995) Dual inoculation of Rhizobium and phosphobacteria with two forms of phosphorus in pigeonpea, in: Microbiology Abstracts. XXXVI. Annual conference of the Association of Microbiologists of India, Hissar, Nov. 8–10, p. 111.Google Scholar
  48. Gyaneshwar P., Naresh K.G., Parekh L.J. (1998a) Effect of buffering on the phosphate solubilizing ability of microorganisms, World J. Microb. Biot. 14, 669–673.CrossRefGoogle Scholar
  49. Gyaneshwar P., Naresh Kumar G., Parekh L.J. (1998b) Cloning of mineral phosphate solubilizing genes from Synechocystis PCC 6803, Curr. Sci. India 74, 1097–1099.Google Scholar
  50. Gyaneshwar P., Parekh L.J., Archana G., Podle P.S., Collins M.D., Hutson R.A., Naresh K.G. (1999) Involvement of a phosphate starvation inducible glucose dehydrogenase in soil phosphate solubilization by Enterobacter asburiae, FEMS Microbiol. Lett. 171, 223–229.CrossRefGoogle Scholar
  51. Halder A.K., Chakrabarty P.K. (1993) Solubilization of inorganic phosphate by Rhizobium., Folia Microbiol. 38, 325–330.CrossRefGoogle Scholar
  52. Haider A.K., Misra A.K., Chakrabarty P.K. (1991) Solubilization of inorganic phosphates by Bradyrhizobium, Ind. J. Exp. Biol. 29, 28–31.Google Scholar
  53. Hayman D.S. (1983) The physiology of vesicular-arbuscular endomycorrhizal symbiosis, Can. J. Bot. 61, 944–963.CrossRefGoogle Scholar
  54. Hobbie S.E. (1992) Effects of plant species on nutrient cycling, Trends Ecol. Evol. 7, 336–339.PubMedCrossRefGoogle Scholar
  55. Holben W.E., Noto K., Sumino T., Suwa Y. (1998) Molecular analysis of bacterial communities in a three compartment granular activated sludge system indicates community-level control by incompatible nitrification process, Appl. Environ. Microbiol. 64, 2528–2532.PubMedGoogle Scholar
  56. Ho W.C., Ko W.H. (1985) Effect of environmental edaphic factors, Soil Biol. Biochem. 17, 167–170.CrossRefGoogle Scholar
  57. Hoon H., Park R.D., Kim Y.W., Rim Y.S., Park K.H., Kim T.H., Such J.S., Kim K.Y. (2003) 2-ketogluconic acid production and phosphate solubilization by Enterobacter intermedium, Current Microbiol. 47, 87–92.CrossRefGoogle Scholar
  58. Hugenholtz P., Goebel B.M., Pace N.R. (1998) Impact of culture independent studies on the emerging phylogenetic view of bacterial diversity, J. Bacteriol. 180, 4765–4774.PubMedGoogle Scholar
  59. Illmer P., Schinner F. (1992) Solubilization of inorganic phosphates by microorganisms isolated from forest soil, Soil Biol. Biochem. 24, 389–395.CrossRefGoogle Scholar
  60. Illmer P.A., Barbato A., Schinner F. (1995) Solubilization of hardly soluble A1PO4 with P-solubilizing microorganisms, Soil Biol. Biochem. 27, 260–270.Google Scholar
  61. Jeffries P. (1987) Use of mycorrhizae in agriculture, CRC Crit. Rev. Biotechnol. 5, 319–357.CrossRefGoogle Scholar
  62. Johri J.K., Surange S., Nautiyal C.S. (1999) Occurrence of salt, pH and temperature tolerant phosphate solubilizing bacteria in alkaline soils, Curr. Microbiol. 39, 89–93.PubMedCrossRefGoogle Scholar
  63. Kang S.C., Ha C.G., Lee T.G., Maheshwari D.K. (2002) Solubilization of insoluble inorganic phosphates by a soil-inhabiting fungus Fomitopsis sp. PS 102, Curr. Sci. 82, 439–442.Google Scholar
  64. Khan M.S., Aamil M., Zaidi A. (1997) Associative effect of Bradyrhizobium sp. (vigna) and phosphate solubilizing bacteria on moongbean [Vigna radiata (L.) wilczek], Biojournal. 10, 101–106.Google Scholar
  65. Khan M.S., Aamil M., Zaidi A. (1998) Moongbean response to inoculation with nitrogen fixing and phosphate solubilizing bacteria, in: Deshmukh A.M. (Ed.), Biofertilizers and biopesticides, Technoscience Publications, Jaipur, pp. 40–48.Google Scholar
  66. Kim K.Y., Jordan D., McDonald G.A. (1997) Solubilization of hydroxyapatite by Enterobacter agglomerons and cloned Escherichia coli in culture medium, Biol. Fert. Soils 24, 347–352.CrossRefGoogle Scholar
  67. Kim K.Y., Jordan D., McDonald G.A. (1998) Enterobacter agglomerons, phosphate solubilizing bacteria and microbial activity in soil: Effect of carbon sources, Soil Biol Biochem. 30, 995–1003.CrossRefGoogle Scholar
  68. Kloepper J.W., Schroth M.N., Miller T.D. (1980) Effects of rhizosphere colonization by plant growth promoting rhizobacteria on potato plant development and yield, Phytopathol. 70, 1078–1082.CrossRefGoogle Scholar
  69. Koide T.R., Shreinner P.R. (1992) Regulation of vesicular arbuscular mycorrhizal symbiosis, Ann. Rev. Plant Physiol. Plant Mol. Biol. 43, 557–581.CrossRefGoogle Scholar
  70. Kucey R.M.N. (1983) Phosphate solubilizing bacteria and fungi in various cultivated and virgin Alberta soils, Can. J. Soil Sci. 63, 671–678.CrossRefGoogle Scholar
  71. Kucey R.M.N. (1987) Increased P uptake by wheat and field beans inoculated with a phosphorus solubilizing Penicillium bilaji strain and with vesicular arbuscular mycorrhizal fungi, Appl. Environ. Micobiol. 53, 2699–2703.Google Scholar
  72. Kucey R.M.N. (1988) Effect of Penicillium bilaji on the solubility and uptake of P and micronutrients from soil by wheat, Can. J. Soil Sci. 68, 261–270.CrossRefGoogle Scholar
  73. Kucey R.M.N., Janzen H.H., Legget M.E. (1989) Microbial mediated increases in plant available phosphorus, Adv. Agron. 42, 199–228.CrossRefGoogle Scholar
  74. Kumar V., Behl R.K., Narula N. (2001) Establishment of phosphate solubilizing strains of Azotobacter chroococcum in the rhizosphere and their effect on wheat cultivars under greenhouse conditions, Microbiol. Res. 156, 87–93.PubMedCrossRefGoogle Scholar
  75. Kundu B.S., Gaur A.C. (1980) Effect of nitrogen fixing and phosphate solubilizing microorganism as single and composite inoculants on cotton, Ind. J. Microbiol. 20, 225–229.Google Scholar
  76. Kundu B.S., Gaur A.C. (1981) Effect of single and composite cultures on rock phosphate solubilization, Haryana Agric. Univ. J. Res. 11, 559–562.Google Scholar
  77. Lapeyrie F., Ranger J., Varelles D. (1991) Phosphate solubilizing activity of ectomycorhhizal fungi in vitro, Can. J. Bot. 69, 342–346.CrossRefGoogle Scholar
  78. Lapeyrie F. (1988) Oxalate synthesis from soil bicarbonate by the mycorrhizal fungus Paxillus involutus, Plant Soil 110, 3–8.CrossRefGoogle Scholar
  79. Leisinger K.M. (1999) Biotechnology and food security, Curr. Sci. India 76, 488–500.Google Scholar
  80. Leopold H., Hofner W. (1991) Improvement of clover yield and quality by inoculation with VAM fungi and Rhizobium bacteria, Angew. Bot. 65, 23–33.Google Scholar
  81. Lindsay W.L., Vlek P.L.G., Chien S.H. (1989) Phosphate minerals, in: Dixon J.B., Weed S.B., Soil environment, 2nd ed., Soil Sci. Soc. America, Madison, pp. 1089–1130.Google Scholar
  82. Lynch J.M. (1983). Soil Biotechnology: Microbiological factors in crop productivity, Blackwell, Scientific Publications, Oxford.Google Scholar
  83. Maliha R., Samina K., Najma A., Sadia A., Farooq L. (2004) Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms under in vitro conditions, Pakistan J. Biol. Sci. 7, 187–196.CrossRefGoogle Scholar
  84. Marshner P., Crowley D.E., Higashi M. (1997) Root exudation and physiological status of a root colonizing fluorescent Pseudomonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annum L.), Plant Soil 189, 11–20.CrossRefGoogle Scholar
  85. Martinez-Murcia A.J., Acinas S.G., Rodriguez-Valera F. (1995) Evaluation of prokaryotic diversity by restrictase digestion of 16S rDNA directly amplified from hipersaline environments, FEMS Microbiol. Ecol. 17, 247–256.Google Scholar
  86. Mehana T.A., Wahid O.A.A. (2002) Associative effect of phosphate dissolving fungi, Rhizobium and phosphate fertilizer on some soil properties, yield components and the phosphorus and nitrogen concentration and uptake by Vicia faba L. under field conditions, Pakistan J. Biol. Sci. 5, 1226–1231.CrossRefGoogle Scholar
  87. Motsara M.R., Bhattacharyya P.B., Srivastava B. (1995) Biofertilizerstheir description and characteristics, in: Biofertilizer Technology, Marketing and Usage, A sourcebook-cum-Glossary, Fertilizer development and consultation organisation 204–204, A Bhanot Corner, 1-2 Pamposh Enclave, New Delhi, 110048, India, pp. 9–18.Google Scholar
  88. Moyer C.L., Dobbs F.C., Karl D.M. (1994) Estimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S r RNA genes from a microbial mat at an active, hydrothermal vent system, Loithi Seamount, Hawaii, Appl. Environ. Microb. 60, 871–879.Google Scholar
  89. Mukherjee P.K., Rai R.K. (2000) Effect of vesicular arbuscular mycorrhizae and phosphate solubilizing bacteria on growth, yield and phosphorus uptake by wheat (Triticum aestivum) and chickpea (Cicer arietinum), Indian J. Agron. 45, 602–607.Google Scholar
  90. Nahas E. (1996) Factors determining rock phosphate solubilization by microorganism isolated from soil, World J. Microb. Biot. 12, 18–23.Google Scholar
  91. Narula N., Kumar V., Behl R.K., Duebel A.A., Gransee A., Merbach W. (2000) Effect of P solubilizing Azotobacter chroococcum on N, P, K uptake in P responsive wheat genotypes grown under green house conditions, J. Plant Nutr. Soil Sci. 163, 393–398.CrossRefGoogle Scholar
  92. Nautiyal C.S. (1999) An efficient microbiological growth medium for screening of phosphate solubilizing microorganisms, FEMS Microbiol. Lett. 170, 265–270.PubMedCrossRefGoogle Scholar
  93. Norrish K., Rosser H. (1983) Mineral phosphate, in: Soils, an Australian viewpoint, Academic press, Melbourne, CSIRO/London, UK, Australia, pp. 335–361.Google Scholar
  94. Natarajan T., Subrammanian P. (1995) Response of phosphobacteria along with Rhizobium at two levels of phosphorus on groundnut, in: Microbiology Abstracts, XXXVI Annual Conference of the Association of Microbiologists of India, Hissar, Nov. 8–10, p. 111.Google Scholar
  95. Nozawa M., Hu H.Y., Fujie K., Tanaka H., Urano K. (1998) Quantitative detection of Enterobacter cloacae strai HO-I In bioreactor for chromate wastewater treatment using polymerase chain reaction (PCR), Water Res. 32, 3472–3476.CrossRefGoogle Scholar
  96. Omar S.A. (1998) The role of rock phosphate solubilizing fungi and vesicular arbuscular mycorrhiza (VAM) in growth of wheat plants fertilized with rock phosphate, World J. Microb. Biot. 14, 211–219.CrossRefGoogle Scholar
  97. Ozanne P.G. (1980) Phosphate nutrition of plants — general treatise. The role of phosphorus in agriculture, in: Khasawneh F.E., Sample E.C., Kamprath E.J. (Eds.), American Soc. Agron. Crop Sci. Soc. America, Soil Sci. Soc. America, Madison, WI, USA, pp. 559–589.Google Scholar
  98. Parks E.J., Olson G.J., Brinckman F.E., Baldi F. (1990) Characterization by high performance liquid chromatography (HPLC) of the solubilization of phosphorus in iron ore by a fungus, J. Ind. Microbiol. Biot. 5, 183–189.Google Scholar
  99. Perveen S., Khan M.S., Zaidi A. (2002) Effect of rhizospheric microorganisms on growth and yield of greengram (Phaseolus radiatus), Indian J. Agr. Sci. 72, 421–423.Google Scholar
  100. Piccini A., Azcon R. (1987) Effect of phosphate solubilizing bacteria and vesicular arbuscular mycorrhizal fungi on the utilization of Bayovar rock phosphate by alfalfa plants using a sand vermiculite medium, Plant Soil 101, 45–50.CrossRefGoogle Scholar
  101. Pikovskaya R.I. (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species, Microbiology 17, 362–370.Google Scholar
  102. Poi S.C., Ghosh G., Kabi M.C. (1989) Response of chickpea (Cicer aeritinum L.) to combined inoculation with Rhizobium, phosphobacteria and mycorrhizal organisms, Zbl. Microbiol. 114, 249–253.Google Scholar
  103. Ponmurugan P., Gopi C. (2006) In vitro production of growth regulators and phosphatase activity by phosphate solubilizing bacteria, African J. Biotechnol. 5, 348–350.Google Scholar
  104. Prabakaran J., Ravi K.B., Srinivasan K. (1996) Response of Vamban-1 Blackgram to N2 fixer and P mobilizers in acid soil, in: Microbiology Abstracts, XXXVII Annual Conference of the Microbiologists of India, IIT, Chennai, Dec, 4–6, p. 120.Google Scholar
  105. Pradhan N., Sukla L.B. (2005) Solubilization of inorganic phosphate by fungi isolated from agriculture soil, African J. Biotechnol. 5, 850–854.Google Scholar
  106. Remy W., Taylor T.N., Hass H., Kerp H. (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae, Proceedings of the National Academy of Sciences, USA 91, pp. 11841–11843.Google Scholar
  107. Reyes I., Bernier L., Simard R.R., Antoun H. (1999) Effect of nitrogen source on the solubilization of different inorganic phosphates by an isolate of Penicillium rugulosum and two UV induced mutants, FEMS Micobiol. Ecol. 28, 281–290.CrossRefGoogle Scholar
  108. Roos W., Luckner M. (1984) Relationships between proton extrusion and fluxes of ammonium ions and organic acid in Penicillium cyclopium, J. Gen. Microbiol. 130, 1007–1014.Google Scholar
  109. Saber M.S.M., Kabesh M.O. (1990) Utilization of biofertilizers in field crop production. II. A comparison study on the effect of biofertilization or sulphur application on yield and nutrient uptake by lentil plants, Egyptian J. Soil Sci. 30, 415–422.Google Scholar
  110. Saber K., Nahla L., Ahmed D., Chedly A. (2005) Effect of P on nodule formation and N fixation in bean, Agron. Sustain. Dev. 25, 389–393.CrossRefGoogle Scholar
  111. Sarojini V., Verma S., Mathur R.S. (1990) The effects of microbial inoculations on the yield of wheat when grown in straw amended soil, Biol. Wastes 33, 9–16.CrossRefGoogle Scholar
  112. Sarojini V., Verma S., Mathur M.S. (1989) Biocoenotic association between nitrogen fixing and phosphate solubilizing microorganisms, Curr. Sci. India 59, 1099–1100.Google Scholar
  113. Satizabal E.J.H., Saif U.S.R. (1987) Interaction between vesicular arbuscular mycorrhiza and leguminous Rhizobium in an oxisol of the eastern plains of Colombia, Acta Agron. 7–21.Google Scholar
  114. Sattar M.A., Gaur A.C. (1987) Production of auxins and gibberellins by phosphate dissolving microorganisms, Zbl. Mikrobiol. 142, 393–395.Google Scholar
  115. Schreiner R.P., Mishra R.L., Mc Daniel K.L., Benthlenfalvay G.J. (2003) Mycorrhizal fungi influence plant and soil functions and interactions, Plant Soil 188, 199–209.CrossRefGoogle Scholar
  116. Shachar-Hill Y., Pfeffer P.E., Douds D., Osman S.F., Doner L.W., Ratcliffe R.G. (1995) Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leeks, Plant Physiol. 108, 7–15.PubMedGoogle Scholar
  117. Singal R., Gupta R., Saxena R.K. (1994) Rock phosphate solubilization under alkaline conditions by Aspergillus japonicus and A. foetidus, Folia 39, 33–36.CrossRefGoogle Scholar
  118. Singh H.P. (1990) Response of dual inoculation with Bradyrhizobium and VAM mycorrhiza or phosphate solubilizer on soybean in mollisol, in: Jalali B.L., Chand H. (Eds.), Trends in mycorrhiza. Research Proceedings of the National conference on Mycorrhiza, HAU, Hisar, India, Feb. 14–16.Google Scholar
  119. Singh H.P., Singh T.A. (1993) The interaction of rock phosphate, Bradyrhizobium, vesicular arbuscular mycorrhizae and phosphate solubilizing microbes on soybean grown in a sub-Himalyan mollisol, Mycorrhiza 4, 37–43.CrossRefGoogle Scholar
  120. Son C.L., Smith S.E. (1995) Mycorrhizal growth responses: interaction between photon irradiance and phosphorus nutrition, New Phytol. 108, 305–314.CrossRefGoogle Scholar
  121. Snaidr J., Amann R., Huber I., Ludwiig W., Schleifer K.H. (1998) Phylogenetic analysis and in situ identification of bacteria in activated sludge, Appl. Environ. Microb. 63, 2884–2896.Google Scholar
  122. Stevenson F.J. (1986) Cycles of soil carbon, nitrogen, phosphorus, sulphur micronutrients, Wiley, New York.Google Scholar
  123. Subha Rao N.S. (1982) Advances in Agricultural Microbiology, in: Subha Rao N.S. (Ed.), Oxford and IBH Publ. Co., pp. 229–305.Google Scholar
  124. Tinker P.B. (1980) The role of phosphorus in Agriculture, in: Khasawneh F.E., Sample E.C., Kamprath E.J. (Eds.), Soil Sci. Soc. Am. Madison, WI.Google Scholar
  125. Tisdall J.M. (1994) Possible role of soil microorganisms in aggregation in soils, Plant Soil 159, 115–121.Google Scholar
  126. Thiagrajan T.R., Ames R.N., Ahmad M.H. (1992) Response of cowpea (Vigna unguiculata) to inoculated with co-selected vesicular arbuscular mycorrhizal fungi and Rhizobium strains in field trials, Can. J. Microbiol. 38, 573–576.CrossRefGoogle Scholar
  127. Tomar S.S., Pathan M.A., Gupta K.P., Khandkar U.R. (1993) Effect of phosphate solubilizing bacteria at different levels of phosphate on black gram (Phaseolus mungo), Indian J. Agron. 38, 131–133.Google Scholar
  128. Trappe J.M. (1987) Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint, in: Safir G.R. (Ed.), Ecophysiology of VA mycorrhizal plants, Boca Raton, FL, CRC Press, USA, pp. 5–25.Google Scholar
  129. Van Elsas J.D., Van Overbeek L.S., Fouchier R. (1991) A specific marker pat for studying the fate of introduced bacteria and their DNA in soil using a combination of detection techniques, Plant Soil 138, 49–60.CrossRefGoogle Scholar
  130. Vassilev N., Fenice M., Federici F. (1996) Rock phosphate solubilization with gluconic acid produced by immobilized Penicillium variable P16, Biotechnol. Tech. 20, 585–588.CrossRefGoogle Scholar
  131. Venkateswarlu B., Rao A.V., Raina P., Ahmad N. (1984) Evaluation of phosphorus solubilization by microorganisms isolated from arid soil, J. Ind. Soc. Soil Sci. 32, 273–277.Google Scholar
  132. Van Veen J.A., Leonard S., Van Overbeek L.S., Van Ellsas J.D. (1997) Fate and activity of microorganisms introduced into soil, Microbiol. Mol. Biol. R. 61, 121–135.Google Scholar
  133. Vasil I.K. (1998) Biotechnology and Food security for 21st century: A real world perspective, Nat. Biotechnol. 16, 399–400.PubMedCrossRefGoogle Scholar
  134. Vazquez P., Holguin G., Puente M., Elopez Cortes A., Bashan Y. (2000) Phosphate solubilizing microorganisms associated with the rhizosphere of mangroves in a semi arid coastal lagoon, Biol. Fert. Soils 30, 460–468.CrossRefGoogle Scholar
  135. Wahid O.A., Mehana T.A. (2000) Impact of phosphate solubilizing fungi on the yield and phosphorus uptake by wheat and faba bean plants, Microbiol. Res. 155, 221–227.PubMedGoogle Scholar
  136. Whitelaw M.A., Harden T.J., Helyar K.R. (1999) Phosphate solubilization in solution culture by the soil fungus penicillium radicum, Soil Biol. Biochem. 32, 655–665.CrossRefGoogle Scholar
  137. Whitelaw M.A. (2000) Growth promotion of plants inoculated with phosphate solubilizing fungi, Adv. Agron. 69, 99–151.CrossRefGoogle Scholar
  138. Zaidi A. (1999) Synergistic interactions of nitrogen fixing microorganisms with phosphate mobilizing microorganisms, Ph.D. Thesis, Aligarh Muslim University, Aligarh.Google Scholar
  139. Zaidi A., Khan M.S. (2005) Interactive effect of rhizospheric microorganisms on growth, yield and nutrient uptake of wheat, J. Plant Nutr. 28, 2079–2092.CrossRefGoogle Scholar
  140. Zaidi A., Khan M.S., Amil M. (2003) Interactive effect of rhizotrophic microorganisms on yield and nutrient uptake of chickpea (Cicer arietinum L.), Eur. J. Agron. 19, 15–21.CrossRefGoogle Scholar
  141. Zaidi A., Khan M.S., Aamil M. (2004) Bio-associative effect of rhizospheric microorganisms on growth, yield and nutrient uptake of greengram, J. Plant Nutr. 27, 599–610.CrossRefGoogle Scholar

Copyright information

© INRA, EDP Sciences 2006

Authors and Affiliations

  • Mohammad Saghir Khan
    • 1
  • Almas Zaidi
    • 1
  • Parvaze A. Wani
    • 1
  1. 1.Department of Agricultural Microbiology, Faculty of Agricultural SciencesAligarh Muslim UniversityAligarh U.P.India

Personalised recommendations