Skip to main content
SpringerLink
Log in

Phosphorus Cycling: Prospects of Using Rhizosphere Microorganisms for Improving Phosphorus Nutrition of Plants

  • Chapter
  • First Online:
Book cover Geomicrobiology and Biogeochemistry

Part of the book series: Soil Biology ((SOILBIOL,volume 39))

Abstract

Phosphorus (P) is the second most essential nutrient after nitrogen for plant growth and development. The available form of P is generally low even in fertile soils throughout the world due to high reactivity of soluble P with calcium, iron, or aluminum. Thus, major portion of applied phosphatic fertilizers in the soil is fixed into insoluble unavailable forms and the availability of P in the rhizosphere is limited. Organic matter is another important reservoir of immobilized P that accounts for 20–80 % of soil P. Phosphate-solubilizing bacteria and fungi convert insoluble fixed phosphates (both organic and inorganic) into a plant utilizable HPO4 2− and H2PO4 − form. The mechanisms of phosphorus solubilization are production of organic/inorganic acids and H+ excretion by microorganisms. For mineralization of organic compounds in the soil, nonspecific acid phosphatases, phytases, and C–P lyases enzymes are involved. Inoculation of these phosphate-solubilizing bacteria in soil has been found to increase uptake of inorganic phosphorus, plant growth, and grain yield of different crop plants. Some of the bacterial genes involved in phosphate solubilization and mineralization of organic P sources have been characterized. The genetic engineering of bacterial strains to enhance phosphate solubilizing capacity will help in further improving the efficacy of biofertilizer inoculants for increasing crop productivity in sustainable agriculture.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abd-Alla MH (1994) Use of organic phosphorus by Rhizobium leguminosarum biovar viceae phosphatases. Biol Fertil Soils 18:216–218

    Google Scholar 

  • Achat DL, Bakker MR, Augusto L, Saur E, Dousseron L, Morel C (2009a) Evaluation of the phosphorus status of P-deficient podzols in temperate pine stands: combining isotopic dilution and extraction methods. Biogeochemistry 92:183–200

    Google Scholar 

  • Achat DL, Bakker MR, Morel C (2009b) Process-based assessment of phosphorus availability in a low phosphorus sorbing forest soil using isotopic dilution methods. Soil Sci Soc Am J 73:2131–2142

    Google Scholar 

  • Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240

    Google Scholar 

  • Agasimani CA, Mudalagiriyappa MV, Sreenivasa MH (1994) Response of groundnut to phosphate solubilizing microorganisms. Groundnut News 6:5–7

    Google Scholar 

  • Agnihotri VP (1970) Solubilization of insoluble phosphates by some soil fungi isolated from nursery seed beds. Can J Microbiol 16:877–880

    Google Scholar 

  • Arcand MM, Schneider KD (2006) Plant-and microbial-based mechanisms to improve the agronomic effectiveness of phosphate rock: a review. An Acad Bras Cienc 78:791–807

    Google Scholar 

  • Asea PEA, Kucey RWN, Stewart JWB (1988) Inorganic phosphate solubilization by two Penicillium species in solution culture and soil. Soil Biol Biochem 20:459–464

    Google Scholar 

  • Azziz G, Bajsa N, Haghjou T, Taule C, Valverde A, Igual JM, Arias A (2012) Abundance, diversity and prospecting of culturable phosphate solubilizing bacteria on soils under crop–pasture rotations in a no-tillage regime in Uruguay. Appl Soil Ecol 61:320–326

    Google Scholar 

  • Babu-khan S, Yeo C, Martin WL, Duron MR, Rogers R, Goldstein A (1995) Cloning of a mineral phosphate solubilizing gene from Pseudomonas cepacia. Appl Environ Microbiol 61:972–978

    Google Scholar 

  • Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20:642–650

    Google Scholar 

  • Bagyaraj DJ, Krishanaraj PU, Khanuja SPS (2000) Mineral phosphate solubilization: agronomic implications, mechanism and molecular genetics. Proc Indian Natl Sci Acad B 66:69–82

    Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Google Scholar 

  • Banger KC, Yadav KS, Mishra MM (1985) Transformation of rock phosphate during composting and the effect of humic acid. Plant Soil 85:259–266

    Google Scholar 

  • Banik S, Dey BK (1981) Solubilization of inorganic phosphate and production of organic acids by microorganisms isolated in sucrose-tricalcium phosphate agar plates. Zentralbl Microbiol 136:478–486

    Google Scholar 

  • Banik S, Dey BK (1983a) Alluvial soil microorganisms capable of utilizing insoluble aluminium phosphates as a sole source of phosphorus. Zentralbl Microbiol 138:437–442

    Google Scholar 

  • Banik S, Dey BK (1983b) Available phosphate content of an alluvial soil as influenced by inoculation of some isolated phosphate solubilizing microorganisms. Plant Soil 69:353–364

    Google Scholar 

  • Banik S, Dey BK (1983c) Phosphate solubilizing potentiality of microorganisms capable of utilizing aluminium phosphate as a sole phosphate source. Zentralbl Microbiol 138:17–23

    Google Scholar 

  • Bano N, Musarrat J (2004) Characterization of a novel carbofuran degrading Pseudomonas sp. with collateral biocontrol and plant growth promoting potential. FEMS Microbiol Lett 231:13–17

    Google Scholar 

  • Bardiya MC, Gaur AC (1972) Rock phosphate dissolution by bacteria. Indian J Microbiol 12:269–271

    Google Scholar 

  • Barea JM, Navarro E, Montoya E (1976) Production of plant growth regulators by rhizosphere phosphate solubilizing bacteria. J Appl Bacteriol 40:129–134

    Google Scholar 

  • Barriuso J, Ramos Solano B, Fray RG, Camara M, Hartmann A, Gutiérrez Manero FJ (2008) Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria. Plant Biotechnol J 6:442–452

    Google Scholar 

  • Bashan Y, Moreno M, Troyo E (2000) Growth promotion of the sea-water irrigated oil seed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp. Biol Fertil Soils 32:265–272

    Google Scholar 

  • Baskanova G, Macaskie LE (1997) Microbially-enhanced chemisorption of nickel into biologically-synthesized hydrogen uranyl phosphate: a novel system for the removal and recovery of metals from aqueous solutions. Biotechnol Bioeng 54:319–329

    Google Scholar 

  • Beacham IR (1980) Periplasmic enzymes in Gram negative bacteria. Int J Biochem 10:877–883

    Google Scholar 

  • Bianco C, Defez R (2010) Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl Environ Microbiol 76:4626–4632

    Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport and phosphate availability. Annu Rev Plant Physiol 24:225–252

    Google Scholar 

  • Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631

    Google Scholar 

  • Bonthrone KM, Baskanova G, Lin F, Macaskie LE (1996) Bioaccumulation of nickel by intercalation into polycrystalline hydrogen uranyl phosphate deposited via an enzymatic mechanism. Nat Biotechnol 14:635–638

    Google Scholar 

  • Bünemann EK (2008) Enzyme additions as a tool to assess the potential bioavailability of organically bound nutrients. Soil Biol Biochem 40:2116–2129

    Google Scholar 

  • Bünemann EK, Marschner P, McNeill AM, McLaughlin MJ (2007) Measuring rates of gross and net mineralisation of organic phosphorus in soils. Soil Biol Biochem 39:900–913

    Google Scholar 

  • Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95

    Google Scholar 

  • Bϋnemann EK, Heenan DP, Marschner P, McNeill AM (2006) Long term effects of crop rotation, stubble management and tillage on soil phosphorus dynamics. Aust J Soil Res 44:611–618

    Google Scholar 

  • Carrillo AE, Li CY, Bashan Y (2002) Increased acidification in the rhizosphere of cactus seedlings induced by Azospirillum brasilense. Naturewissenschaften 89:428–432

    Google Scholar 

  • Castagno LN, Estrella MJ, Sannazzaro AL, Grassano AE, Ruiz OA (2011) Phosphate solubilization mechanism and in vitro plant growth promotion activity mediated by Pantoea eucalypti isolated from Lotus tenuis rhizosphere in the Salado river basin (Argentina). J Appl Microbiol 110:1151–1165

    Google Scholar 

  • Cattelan AJ, Hartel PG, Furhmann FF (1999) Screening of plant growth promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1680

    Google Scholar 

  • Chandra K, Mukherjee PK, Karmakar JB, Sharma BK (1995) Effect of phosphate solubilizing bacteria on rhizobial symbiosis in soybean at rainfed conditions of Manipur. Environ Ecol 13:436–438

    Google Scholar 

  • Chen CR, Condron LM, Davis MR, Sherlock RR (2002) Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol Biochem 34:487–499

    Google Scholar 

  • Cheng WX (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801

    Google Scholar 

  • Chookietwattana K, Maneewan K (2012) Screening of efficient halotolerant phosphate solubilizing bacterium and its effect on promoting plant growth under saline conditions. World Appl Sci J 16(8):1110–1117

    Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Change 19:292–305

    Google Scholar 

  • Correll DL (1998) The role of phosphorus in the eutrophication of receiving waters: a review. J Environ Qual 27:261–266

    Google Scholar 

  • de Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fertil Soils 27:358–364

    Google Scholar 

  • Deng S, Summers ML, Kahn ML, Mc Dermontt TR (1998) Cloning and characterization of a Rhizobium meliloti nonspecific acid phosphatase. Arch Microbiol 170:18–26

    Google Scholar 

  • Deng S, Elkins JG, Da LH, Botero LM, McDermontt TR (2001) Cloning and characterization of second acid phosphatase from Sinorhizobium meliloti strain 104A14. Arch Microbiol 176:255–263

    Google Scholar 

  • Deubel A, Merbach W (2005) Influence of microorganisms on phosphorus bioavailability in soils. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions. Springer, Berlin, pp 177–191

    Google Scholar 

  • Deubel A, Gransee A, Merbach W (2000) Transformation of organic rhizodepositions by rhizosphere bacteria and its influence on the availability of tertiary calcium phosphate. J Plant Nutr Soil Sci 163:387–392

    Google Scholar 

  • Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Micobiol Res 159:371–394

    Google Scholar 

  • Dubey SK (1997) Coinoculation of phosphate solubilizing bacteria with Bradyrhizobium japonicum to increase phosphate availability to rainfed soybean on vertisol. J Indian Soc Soil Sci 45:506–509

    Google Scholar 

  • Dubey SK (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 

  • Dugan P, Lundgren DG (1965) Energy supply for the chemoautotroph Ferrobacillus ferrooxidans. J Bacteriol 89:825–834

    Google Scholar 

  • Dye C (1995) Effect of citrate and tartrate on phosphate absorption by amorphous ferric hydroxide. Fert Res 40:129–134

    Google Scholar 

  • Ekin Z (2010) Performance of phosphate solubilizing bacteria for improving growth and yield of sunflower (Helianthus annuus L.) in the presence of phosphorus fertilizer. Afr J Biotechnol 9(25):3794–3800

    Google Scholar 

  • El Komy HMA (2005) Coimmobilization of Azospirillum lipoferum and Bacillus megaterium for successful phosphorus and nitrogen nutrition of wheat plants. Food Technol Biotechnol 43:19–27

    Google Scholar 

  • El Sayed SAM (1999) Influence of Rhizobium and phosphate solubilizing bacteria on nutrient and yield of lentil in New Valley (Egypt). Egypt J Soil Sci 39:175–186

    Google Scholar 

  • Esberg C, du Toit B, Olsson R, Ilstedt U, Giesler R (2010) Microbial responses to P addition in six South African forest soils. Plant Soil 329:209–225

    Google Scholar 

  • Fankem H, Nwaga D, Deubel A, Dieng L, Merbach W, Etoa FX (2006) Occurrence and functioning of phosphate solubilizing microorganisms from oil palm tree (Elaeis guineensis) rhizosphere in Cameroon. Afr J Biotechnol 5:2450–2460

    Google Scholar 

  • Fernandez LA, Zalba P, Gomez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol Fertil Soils 43:805–809

    Google Scholar 

  • Fraga R, Rodriguez H, Gonzalez T (2001) Transfer of the gene encoding the NapA acid phosphatase from Morganella marganii to a Burkholderia cepacia strain. Acta Biotechnol 21:359–369

    Google Scholar 

  • Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23

    Google Scholar 

  • Gadagi RS, Tongmin SA (2002) New isolation method for microorganisms solubilizing iron and aluminium phosphates using dyes. Soil Sci Plant Nutr 48:615–618

    Google Scholar 

  • Gaind S, Gaur AC (1990) Influence of temperature on the efficacy of phosphorus solubilizing microorganisms. Indian J Microbiol 30:305–310

    Google Scholar 

  • Gaind S, Gaur AC (1991) Thermotolerant phosphate solubilizing microorganisms and their interaction with mungbean. Plant Soil 133:141–149

    Google Scholar 

  • Galar ML, Bolardi JL (1995) Evidence for a membrane bound pyrrolquinoline quinine-linked glucose dehydrogenase in Acetobacter diazotrophicus. Appl Environ Microbiol 43:713–716

    Google Scholar 

  • Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390

    Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Google Scholar 

  • Gaur AC (1990) Phosphate solubilizing microorganisms as biofertilizer. Omega Scientific Publications, New Delhi, p 176

    Google Scholar 

  • Gaur AC, Madan M, Ostwal KP (1973) Solubilization of phosphatic compounds by native microflora of rock phosphates. Indian J Exp Biol 11:427–429

    Google Scholar 

  • Geelhoed JS, van Riemsdijk WH, Findenegg GR (1999) Simulation of the effect of citrate exudation from roots on the plant availability of phosphate adsorbed on goethite. Eur J Soil Sci 50:379–390

    Google Scholar 

  • George TS, Richardson AE, Smith JB, Hadobas PA, Simpson RJ (2005) Limitations to the potential of transgenic Trifolium subterraneum L. plants that exude phytase when grown in soils with a range of organic P content. Plant Soil 278:263–274

    Google Scholar 

  • George TS, Simpson RJ, Hadobas PA, Marshall DJ, Richardson AE (2007) Accumulation and phosphatase-lability of organic phosphorus in fertilised pasture soils. Aust J Agric Res 58:47–55

    Google Scholar 

  • George TS, Richardson AE, Li SM, Gregory PJ, Daniell TJ (2009) Extracellular release of a heterologous phytase from roots of transgenic plants: does manipulation of rhizosphere biochemistry impact microbial community structure? FEMS Microbiol Ecol 70:433–445

    Google Scholar 

  • Gerke J (1992) Phosphate, aluminium and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Zeitsch Pflanz Bodenk 155:339–343

    Google Scholar 

  • Gerretson FC (1948) The influence of microorganisms on the phosphate intake by the plants. Plant Soil 1:51–81

    Google Scholar 

  • Ghosh G, Poi SC (1990) Response of Rhizobium, phosphate solubilizing bacteria and mycorrhizal organisms in legume crops. Environ Ecol 16:607–610

    Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    Google Scholar 

  • Gilvert N (2009) The disappearing nutrient. Science 461:716–718

    Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 32:145–148

    Google Scholar 

  • Goldstein AH (1986) Bacterial solubilization of microbial phosphates: historical perspective and future prospects. Am J Altern Agric 1:51–57

    Google Scholar 

  • Goldstein AH (1995) Recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by Gram-negative bacteria. Biol Agric Hortic 12:185–193

    Google Scholar 

  • Goldstein AH (1996) Involvement of the quinoprotein glucose dehydrogenase in the solubilization of exogenous phosphates by Gram-negative bacteria. In: Toriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 197–203

    Google Scholar 

  • Goldstein AH (2007) Future trends in research on microbial phosphate solubilization: one hundred years of insolubility. In: Velazquez E, Roderguez-Barrueco C (eds) Proceedings of the first international meeting on microbial phosphate solubilization. Springer, Berlin, pp 91–96

    Google Scholar 

  • Goldstein AH, Liu ST (1987) Molecular cloning and regulation of a mineral phosphate solubilizing gene from Erwinia herbicola. Biotechnology 5:72–74

    Google Scholar 

  • Goldstein AH, Rogers RD, Mead G (1993) Separating phosphate from ores via bioprocessing. Biotechnology 11:1250–1254

    Google Scholar 

  • Golovan S, Wang G, Zhang J, Forsberg CW (2000) Characterization and overproduction of the Escherichia coli appA encoded bifunctional enzyme that exhibits both phytase and acid phosphatase activities. Can J Microbiol 46:59–71

    Google Scholar 

  • Grimes HD, Mount MS (1984) Influence of Pseudomonas putida on nodulation of Phaseolus vulgaris. Soil Biol Biochem 16:27–30

    Google Scholar 

  • Gupta R, Singal R, Shankar A, Kuhad RC, Saxena RK (1993) Modified plate assay for screening of phosphate solubilizing microorganisms. J Gen Appl Microbiol 40:255–260

    Google Scholar 

  • Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    Google Scholar 

  • Halder AK, Mishra AK, Chakrabarty PK (1991) Solubilizing of inorganic phosphates by Bradyrhizobium. Indian J Exp Biol 29:28–31

    Google Scholar 

  • Han Y, Wilson DB, Lei XG (1999) Expression of an Aspergillus niger phytase gene (phyA) in Saccharomyces cerevisiae. Appl Environ Microbiol 65:1915–1918

    Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Google Scholar 

  • Harvey PR, Warren RA, Wakelin S (2009) Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere. Crop Pasture Sci 60:144–151

    Google Scholar 

  • Hasan R (1994) Phosphorus fertility status of soils in India. Phosphorus research in India. In: Dev G (ed) Proceedings of group discussion, Indian Agricultural Research Institute, New Delhi. Principal Publications, Gurgaon, pp 8–12

    Google Scholar 

  • Hassan HM, Marschner P, McNeill A, Tang C (2012) Growth, P uptake in grain legumes and changes in rhizosphere soil P pools. Biol Fertil Soils 48:151–159

    Google Scholar 

  • Hebbara M, Suseeladevi L (1990) Effect of phosphorus solubilizing bacteria (PSB) on phosphorus availability to groundnut from rock phosphate. Curr Res 19:56–57

    Google Scholar 

  • Henri F, Laurette NN, Annette D, John Q, Wolfgang M, François-Xavier E, Dieudonné N (2008) Solubilization of inorganic phosphates and plant growth promotion by strains of Pseudomonas fluorescens isolated from acidic soils of Cameroon. Afr J Microbiol Res 2:171–178

    Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Google Scholar 

  • Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root mediated pH changes in the rhizosphere and their response to environmental constraints: a review. Plant Soil 248:43–59

    Google Scholar 

  • Holford ICR (1997) Soil phosphorus: its measurement and its uptake by plants. Aust J Soil Res 35:227–239

    Google Scholar 

  • Huelett FM, Sun G, Liu W (2007) The Pho regulon of Bacillus subtilis is regulated by sequential action of two genetic switches. In: Toriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 50–54

    Google Scholar 

  • Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borris R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant growth promoting effects. Microbiology 148:2097–2109

    Google Scholar 

  • Igual JM, Valverde A, Ceravantes E, Velazquez E (2001) Phosphate solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie 21:561–568

    Google Scholar 

  • Illmer P, Schinner F (1992) Solubilization of inorganic phosphates by microorganisms isolated from forest soils. Soil Biol Biochem 24:389–395

    Google Scholar 

  • Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates: solubilization mechanisms. Soil Biol Biochem 27:257–263

    Google Scholar 

  • Jain LK, Singh P (2003) Growth and nutrient uptake of chickpea (Cicer arietinum L.) as influenced by biofertilizers and phosphorus nutrition. Crop Res 25:410–413

    Google Scholar 

  • Jakobsen I, Leggett ME, Richardson AE (2005) Rhizosphere microorganisms and plant phosphorus uptake. In: Sims JT, Sharpley AN (eds) Phosphorus: agriculture and the environment. American Society for Agronomy, Madison, WI, pp 437–494

    Google Scholar 

  • Jisha MS, Alagawadi AR (1996) Nutrient uptake and yield of sorghum (Sorghum bicolor L. Moench) inoculated with phosphate solubilizing bacteria and cellulolytic fungus in cotton stalk amended vertisol. Microbiol Res 151:1–5

    Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44

    Google Scholar 

  • Jones DL, Oburger E (2011) Phosphorus in action. Soil Biol 100:169–198

    Google Scholar 

  • Juriank JJ, Dudley LM, Allen MF, Knight WG (1986) The role of calcium oxalate in the availability of phosphorus in soils of semiarid regions: thermodynamic study. Soil Sci 142:255–261

    Google Scholar 

  • Kamh M, Horst W, Amer F, Mostafa H, Maier P (1999) Mobilization of soil and fertilizer phosphate by cover crops. Plant Soil 211:19–27

    Google Scholar 

  • Karamanos RE, Flore NA, Harapiak JT (2010) Re-visiting use of Penicillium bilaii with phosphorus fertilization of hard red spring wheat. Can J Plant Sci 90:265–277

    Google Scholar 

  • Katznelson H, Bose B (1959) Metabolic activity and phosphate dissolving activity of bacterial isolates from wheat roots, rhizosphere and non-rhizosphere soil. Can J Microbiol 5:79–85

    Google Scholar 

  • Kerovuo J, Lauracus M, Nurminen P, Kalkinen N, Apajalahti J (1998) Isolation, characterization, molecular gene cloning and sequencing of a novel phytase from Bacillus subtilis. Appl Environ Microbiol 64:2079–2085

    Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2006) Role of phosphate solubilizing microorganisms in sustainable agricultural – a review. Agron Sustain Dev 26:1–15

    Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2007) Role of phosphate solubilizing microorganisms in sustainable agriculture – a review. Agron Sustain Dev 27:29–43

    Google Scholar 

  • Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi – current perspective. Arch Agron Soil Sci 56:73–98

    Google Scholar 

  • Khandelwal A, Sindhu SS (2012) Expression of 1-aminocyclopropane-1-carboxylate deaminase in rhizobia promotes nodulation and plant growth of clusterbean (Cyamopsis tetragonoloba L.). Res J Microbiol 7:158–170

    Google Scholar 

  • Kim KY, McDonald GA, Jordan D (1997) Solubilization of hydroxyapatite by Enterobacter agglomerans and cloned Escherichia coli in culture medium. Biol Fertil Soils 24:347–352

    Google Scholar 

  • Kim KY, Jordan D, Krishnan HB (1998a) Expression of genes from Rahnella aquatilis that are necessary for mineral phosphate solubilization in Escherichia coli. FEMS Microbiol Lett 159:121–127

    Google Scholar 

  • Kim KY, Jordan D, McDonald GA (1998b) Effect of phosphate solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26:79–87

    Google Scholar 

  • Kim KY, Jordan D, McDonald GA (1998c) Enterobacter agglomerans, phosphate solubilizing bacteria and microbial diversity in soil: effect of carbon sources. Soil Biol Biochem 30:995–1003

    Google Scholar 

  • Kim YO, Lee JK, Kim HK, Yu JH, Oh TK (1998d) Cloning of thermostable phytase gene (phy) from Bacillus sp. DS11 and its overexpression in Escherichia coli. FEMS Microbiol Lett 162:185–191

    Google Scholar 

  • Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomus JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58:169–188

    Google Scholar 

  • Kole SC, Hazra JN (1998) Occurrence and acidity of tricalcium phosphate and rock phosphate solubilizing microorganisms in mechanical compost plants of Calcutta and an alluvial soil of West Bengal. Environ Ecol 16:344–349

    Google Scholar 

  • Krishanaraj PU (1987) Studies on beneficial microorganisms in crop plants. M.Sc. thesis, UAS, Bangalore

    Google Scholar 

  • Krishanaraj PU (1996) Genetic characterization of mineral phosphate solubilization in Pseudomonas sp. Ph.D. thesis, IARI, New Delhi

    Google Scholar 

  • Krishanaraj PU, Goldstein AH (2001) Cloning of a Serratia marcescens DNA fragment that induces quino-protein glucose dehydrogenase-mediated gluconic acid production in Escherichia coli in the presence of Serratia marcescens. FEMS Microbiol Lett 205:215–220

    Google Scholar 

  • Krishanaraj PU, Sadasivam KV, Khanuja PS (1999) Mineral phosphate solubilization defective mutants of Pseudomonas sp. express pleiotropic phenotypes. Curr Sci 76:1032–1034

    Google Scholar 

  • Kucey RMN (1987) Increased phosphorus uptake by wheat and field beans inoculated with a phosphorus solubilizing Penicillium bilaji strain and vesicular arbuscular mycorrhizal fungi. Appl Environ Microbiol 53:2699–2703

    Google Scholar 

  • Kucey RMN (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

    Google Scholar 

  • Kucey RMN, Janzen HH, Legett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42:198–228

    Google Scholar 

  • Kumrawat B, Dighe JM, Sharma RA, Katti GV (1997) Response of soybean to biofertilizer in black clay soils. Crop Res 14:209–214

    Google Scholar 

  • Kundu BS, Gaur AC (1980a) Effects of phosphobacteria on yield and phosphate uptake by potato crop. Curr Sci 48:159

    Google Scholar 

  • Kundu BS, Gaur AC (1980b) Effect of nitrogen fixing and phosphate solubilising microorganisms as single and composite inoculants on cotton. Indian J Microbiol 20:225–229

    Google Scholar 

  • Kundu BS, Gaur AC (1980c) Establishment of nitrogen and phosphate solubilizing bacteria in rhizosphere and their effect on yield and nutrient uptake of wheat crop. Plant Soil 57:223–230

    Google Scholar 

  • Kundu BS, Gaur AC (1982) Yield increase of wheat after inoculation with A. chroococcum and phosphobacteria. Curr Sci 51:291–293

    Google Scholar 

  • Kundu BS, Gaur AC (1984) Rice response to inoculation with nitrogen fixing bacteria and PSM. Plant Soil 78:227–234

    Google Scholar 

  • Larsen S (1967) Soil phosphorus. Adv Agron 19:151–210

    Google Scholar 

  • Lei XG, Ku PK, Miller ER, Yokoyama MT, Ullrey DE (1993) Supplementing corn-soybean meal diets with microbial phytase maximizes phytate P utilization by winling pigs. J Anim Sci 71:3368–3375

    Google Scholar 

  • Lifschitz R, Kloepper JW, Kozlowski M, Simonson C, Carlson J, Tipling EM, Zaleska T (1987) Growth promotion of canola (rape seed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Can J Microbiol 33:390–395

    Google Scholar 

  • Lim BL, Yeung P, Cheng C, Hill JE (2007) Distribution and diversity of phytate-mineralizing bacteria. ISME J 1:321–330

    Google Scholar 

  • Lindsay WLP, Vlek LG, Chien SH (1989) Phosphate minerals. In: Dixon JB, Weed SB (eds) Minerals in soil environment, 2nd edn. Soil Science Society of America, Madison, WI, pp 1089–1130

    Google Scholar 

  • Liu ST, Lee LY, Jai CY, Hung CH, Chang YS, Wolfram JH, Rogers B, Goldstein AH (1992) Cloning of an Erwinia herbicola gene necessary for gluconic acid production and enhanced mineral phosphate solubilization in E. coli HB101: nucleotide sequence and probable involvement in biosynthesis of the co-enzyme pyrrolquinoline quinine. J Bacteriol 174:5814–5819

    Google Scholar 

  • Lopez-Bucio J, de la Vega OM, Guevara-Garcia A, Herreera-Estrella I (2000) Enhanced phosphate uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453

    Google Scholar 

  • Lorenzo V, Herrero M, Jakubjik U, Timmis KN (1990) Mini-Tn5 transposon derivatives for transposon mutagenesis, promoter probing and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172:6568–6572

    Google Scholar 

  • Macaskie LE, Young P, Doyle TC, Roig MG, Diaz M, Monzano T (1997) Bioremediation of uranium-bearing waste water: biochemical and chemical factors affecting bioprocess application. Biotechnol Bioeng 53:100–109

    Google Scholar 

  • Macklon AES, Grayston SJ, Shand CA, Sim A, Sellars S, Ord BG (1997) Uptake and transport of phosphorus by Agrostis capillaris seedlings from rapidly hydrolysed organic sources extracted from P32-labelled bacterial cultures. Plant Soil 190:163–167

    Google Scholar 

  • Maheshkumar KS (1997) Studies on microbial diversity and their activity in soil under bamboo plantations. M.Sc. thesis, UAS, Dharwad

    Google Scholar 

  • Maheshkumar KS, Krishanraj PU, Alagawadi AR (1999) Mineral phosphate solubilizing activity of Acetobacter diazotrophicus: a bacterium associated with sugarcane. Curr Sci 76:874–875

    Google Scholar 

  • Makino K, Amemura M, Kim SK, Nakata A, Shinagawa H (2007) Mechanism of transcriptional activation of the phosphate regulon in Eschericia coli. In: Toriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 5–12

    Google Scholar 

  • Malik DK, Sindhu SS (2011) Production of indole acetic acid by Pseudomonas sp.: Effect of coinoculation with Mesorhizobium sp. Cicer on nodulation and plant growth of chickpea (Cicer arietinum). Physiol Mol Biol Plants 17:25–32

    Google Scholar 

  • Mehta S, Nautiyal SC (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56

    Google Scholar 

  • Miller SH, Browne P, Prigent-Combaret C, Combes-Meynet E, Morrissey JP, O'Gara F (2010) Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ Microbiol Rep 2:403–411

    Google Scholar 

  • Mishra MM, Kapoor KK, Yadav KS (1982) Effect of compost enriched with Mussorie rock phosphate on crop yield. Indian J Agric Sci 52:674–678

    Google Scholar 

  • Monod SPI, Gupta DN, Chavan AS (1989) Enhancement of phosphate availability and phosphorus uptake in rice by phosphate solubilizing culture. J Maharastra Agric Univ 14:178–181

    Google Scholar 

  • Mortensen JL (1963) Complexing of metals by soil organic matter. Soil Sci Soc Am Proc 27:179–186

    Google Scholar 

  • Naik PR, Raman G, Narayanan KB, Sakthivel N (2008) Assessment of genetic and functional diversity of phosphate solubilizing fluorescent pseudomonads isolated from rhizospheric soil. BMC Microbiol 8:230–243

    Google Scholar 

  • Nautiyal CS (1990) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    Google Scholar 

  • Norrish K, Rosser H (1983) Mineral phosphate. In: Lenaghan JJ, Katsantoni G (eds) Soils, An Australian view point. CSIRO, Melbourne, Academic Press, London, pp 335–361

    Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2005a) Phosphorus uptake by grain legumes and subsequently grown wheat at different levels of residual phosphorus fertilizer. Aust J Agric Res 56:1041–1047

    Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2005b) Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant Soil 271:175–187

    Google Scholar 

  • Nziguheba G, Merckx R, Palm CA, Rao MR (2000) Organic residues affect phosphorus availability and maize yields in a Nitisol of western Kenya. Biol Fertil Soils 32:328–339

    Google Scholar 

  • Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI, Wallingford, pp 133–164

    Google Scholar 

  • Oehl F, Oberson A, Probst M, Fliessback A, Roth HR, Frossard E (2001) Kinetics of microbial phosphorus uptake in cultivated soils. Biol Fertil Soils 34:31–41

    Google Scholar 

  • Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675

    Google Scholar 

  • Ogawa N, Hayashi N, Salto H, Noguchi K, Yamashita Y, Oshima Y (2007) Regulatory circuit for phosphatase genes in Saccharomyces cerevisiae: specific cis-acting sites in Pho promoters for binding the Pho4p. In: Toriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 56–62

    Google Scholar 

  • Ostwal KP, Bhide VP (1972) Solubilization of tricalcium phosphate by soil Pseudomonas. Indian J Exp Biol 10:153–154

    Google Scholar 

  • Otani T, Ae N, Tanaka H (1996) Phosphorus (P) uptake mechanisms of crops grown in soils with low P status: II. Significance of organic acids in root exudates of pigeonpea. J Soil Sci Plant Nutr 42:553–560

    Google Scholar 

  • Panhar QA, Othman R, Rahman ZA, Meon S, Ismail MR (2012) Isolation and characterization of phosphate-solubilizing bacteria from aerobic rice. Afr J Biotechnol 11:2711–2719

    Google Scholar 

  • Panhwar QA, Radziah O, Zaharah AR, Sariah M, Razi IM (2011) Role of phosphate solubilizing bacteria on rock phosphate solubility and growth of aerobic rice. J Environ Biol 32:607–612

    Google Scholar 

  • Parks EJ, Olson GJ, Brickman PE, Baldi F (1990) Characterization of high performance liquid chromatography (HPLC) of the solubilization of phosphorus in iron ore by a fungus. Indian J Microbiol 5:83–190

    Google Scholar 

  • Prabhakar M, Saraf CS (1990) Dry matter accumulation and distribution in chickpea as influenced by genotype, P source and irrigation level. Indian J Agric Sci 60:204–206

    Google Scholar 

  • Prasanna A, Deepa V, Balkrishna Murthy P, Deecaraman M, Sridhar R, Dhandapani P (2011) Insoluble phosphate solubilization by bacterial strains isolated from rice rhizosphere soils from Southern India. Intern J Soil Sci 6:34–141

    Google Scholar 

  • Puente ME, Bashan Y, Li CY, Lebsky VK (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. Root colonization and weathering of igneous rocks. Plant Biol 6:629–642

    Google Scholar 

  • Qureshi MA, Ahmad ZA, Akhtar N, Iqbal A, Mujeeb F, Shakir MA (2012) Role of phosphate solubilizing bacteria (PSB) in enhancing P availability and promoting cotton growth. J Anim Plant Sci 22:204–210

    Google Scholar 

  • Rachewad SN, Raut RS, Malewar GU, Ganure CK (1992) Effects of phosphate solubilizing biofertilizer on biomass production and uptake of phosphorus by sunflower. J Maharastra Agric Univ 17:480–481

    Google Scholar 

  • Rajarathinam K, Balamurugan T, Kulasekarapandian R, Veersami S, Jayabalan M (1995) Isolation and screening of phosphate solubilizers from soil of Kamarajar district (Tamil Nadu). J Exotoxicol Environ Monit 5:155–157

    Google Scholar 

  • Rashid M, Khalil S, Ayub N, Alam S, Latif M (2004) Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms (PSM) under in vitro conditions. Pakistan J Biol Sci 7:187–196

    Google Scholar 

  • Reilly TJ, Baron GS, Nano F, Kuhlenschmidt MS (1996) Characterization and sequence of a respiratory burst-inhibiting acid phosphatase from Francisella tularensis. J Biol Chem 271:10973–10983

    Google Scholar 

  • Reyes I, Bernier L, Simard RR, Tanguay P, Antoun H (1999) Characteristics of phosphate solubilization by an isolate of a tropical Penicillium rugulosum and two UV-induced mutants. FEMS Microbiol Ecol 28:291–295

    Google Scholar 

  • Reyes I, Baziramakenga R, Bernier L, Antoun H (2001) Solubilization of phosphate rocks and minerals by a wild-type strain and two UV-induced mutants of Penicillium rugulosum. Soil Biol Biochem 33:1741–1747

    Google Scholar 

  • Richardson AE (1994) Soil microorganisms and phosphorus availability. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Soil biota: management in sustainable farming systems. CSIRO, Highett, VIC, pp 50–62

    Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE (2001a) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649

    Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE, O’Hara CP, Simpson RJ (2001b) Utilization of phosphorus by pasteur plants supplied with meso-inositol hexaphosphate is enhanced by the presence of soil microorganisms. Plant Soil 229:47–56

    Google Scholar 

  • Richardson AE, George TS, Hens M, Simpson RJ (2005) Utilization of soil organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI, Wallingford, pp 165–184

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009a) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Google Scholar 

  • Richardson AE, Hocking PJ, Simpson RJ, George TS (2009b) Plant mechanisms to optimize access to soil phosphorus. Crop Pasture Sci 60:124–143

    Google Scholar 

  • Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Google Scholar 

  • Rodriguez E, Han Y, Lei XG (1999) Cloning, sequencing and expression of an Escherichia coli acid phosphatase/phytase gene (appA2) isolated from pig colon. Biochem Biophys Res Commun 257:117–123

    Google Scholar 

  • Rodriguez H, Gonzalez T, Selman G (2000a) Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. J Biotechnol 84:155–161

    Google Scholar 

  • Rodriguez H, Rossolini GM, Gonzalez T, Jiping L, Glick BR (2000b) Isolation of a gene from Burkholderia cepacia IS-16 encoding a protein that facilitates phosphatase activity. Curr Microbiol 40:362–366

    Google Scholar 

  • Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555

    Google Scholar 

  • Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth promoting bacteria. Plant Soil 287:15–21

    Google Scholar 

  • Rossolini GM, Schippa S, Riccio ML, Berlutti F, Macaskie LE, Thallar MC (1998) Bacterial non-specific acid phosphatases: physiology, evolution and use as tools in microbial biotechnology. Cell Mol Life Sci 54:833–850

    Google Scholar 

  • Roychaudhary P, Kaushik BD (1989) Solubilization of Mussoorie rock phosphate by cyanobacteria. Curr Sci 58:569–570

    Google Scholar 

  • Ryan PR, Delhaise E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Google Scholar 

  • Sanchez PA, Shepherd KD, Soule MJ, Place FM, Buresh RJ, Izac AN (1997) Soil fertility replenishment in Africa: an investment in natural resources capital. In: Replenishing soil fertility in Africa, Indianapolis. Proceedings, SSSA Special Publication No. 51, American Society of Agronomy, Madison, WI, pp 1–46

    Google Scholar 

  • Santhi V (1998) Mechanism of mineral phosphate solubilization and growth promotion by diverse bacteria. M. Sc. thesis, University of Agricultural Sciences, Dharwad

    Google Scholar 

  • Saraf CS, Shivkumar BG, Patil RR (1997) Effect of phosphorus, sulphur and seed inoculation on performance of chickpea (Cicer arietinum). Indian J Agron 42:323–328

    Google Scholar 

  • Sarawgi SK, Tiwari PK, Tripathi RS (1999) Uptake and balance sheet of nitrogen and phosphorus in gram (Cicer arietinum) as influenced by phosphorus biofertilizers and micronutrients under rain-fed conditions. Indian J Agron 44:768–772

    Google Scholar 

  • Sarawgi SK, Tiwari PK, Tripathi RS (2000) Growth, nodulation and yield of chickpea as influenced by phosphorus, bacterial culture and micronutrients under rain-fed conditions. Madras Agric J 86:181–185

    Google Scholar 

  • Seeling B, Zasoski RJ (1993) Microbial effects in maintaining organic and inorganic solution phosphorus concentrations in a grassland topsoil. Plant Soil 148:277–284

    Google Scholar 

  • Shahid M, Hameed S, Imran A, Ali S, van Elsas JD (2012) Root colonization and growth promotion of sunflower (Helianthus annuus L.) by phosphate solubilizing Enterobacter sp. Fs-11. World J Microbiol Biotechnol 28(8):2749–2758

    Google Scholar 

  • Sharma SN (2003) Effect of phosphate solubilizing bacteria on the efficacy of Mussoorie rock phosphate in rice (Oryza sativa) – wheat (Triticum aestivum) cropping system. Indian J Agric Sci 73:478–481

    Google Scholar 

  • Sharpley AN (1985) Phosphorus cycling in unfertilized and fertilized agricultural soils. Soil Sci Soc Am J 49:905–911

    Google Scholar 

  • Sheshardri S, Kumaraswamy R, Lakshminarasimhan C, Ignacimuthu S (2000) Solubilization of inorganic phosphate by Azospirillum halopraeferans. Curr Sci 79:565–567

    Google Scholar 

  • Sindhu SS, Dadarwal KR (2000) Competition for nodulation among rhizobia in Rhizobium-legume symbiosis. Indian J Microbiol 40:211–246

    Google Scholar 

  • Sindhu SS, Verma MK, Mor S (2009) Molecular genetics of phosphate solubilization in rhizosphere bacteria and its role in plant growth promotion. In: Khan MS, Zaidi A (eds) Phosphate solubilizing microbes and crop productivity. Nova Science, Hauppauge, NY, pp 199–228

    Google Scholar 

  • Sindhu SS, Dua S, Verma MK, Khandelwal A (2010) Growth promotion of legumes by inoculation of rhizosphere bacteria. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer-Wien, NewYork, pp 195–235

    Google Scholar 

  • Singh CP, Mishra MM, Yadav KS (1980) Solubilization of insoluble phosphates by thermophilic fungi. Ann Microbiol (Inst Pasteur) 131:289–296

    Google Scholar 

  • Singh HP, Pareek RP, Singh PA (1984) Solubilization of rock phosphate by phosphate solubilizers in broth. Curr Sci 53:1212–1213

    Google Scholar 

  • Singh AV, Chandra R, Goel R (2012) Phosphate solubilization by Chryseobacterium sp. and their combined effect with N and P fertilizers on plant growth promotion. Arch Agron Soil Sci 58:1–11

    Google Scholar 

  • Sonboir HL, Sarawgi SK (2000) Nutrients uptake, growth and yield of chickpea as influenced by phosphorus, Rhizobium and phosphate solubilizing bacteria. Madras Agric J 87:149–151

    Google Scholar 

  • Sperber JI (1958) Solution of apatite by soil microorganisms producing organic acids. Aust J Agric Res 9:778–781

    Google Scholar 

  • Srivastava TK, Ahalwat LPS, Panwar JDS (1998) Effect of phosphorus, molybdenum and biofertilizers on productivity of pea. Indian J Plant Physiol 3:237–239

    Google Scholar 

  • Stalstorm VA (1903) Beitrag, Zur Kenntrusder einwinsking sterilizer and in garung befindlieher strife any dil Loslishkerd der phosphorus are destrical cum phosphorus. Zentralb Bakteriol Abt 11:724–732

    Google Scholar 

  • Surange S, Kumar N (1993) Phosphate solubilization under varying pH by Rhizobium from tree legumes. Indian J Exp Biol 31:427–429

    Google Scholar 

  • Taha SM, Mahamood SAZ, Halim EI, Damaty A, Hafez AM (1969) Activity of phosphate dissolving bacteria in Egyptian soils. Plant Soil 31:149–160

    Google Scholar 

  • Tallapragada P, Seshachala U (2012) Phosphate-solubilizing microbes and their occurrence in the rhizospheres of Piper betel in Karnataka, India. Turk J Biol 36:25–35

    Google Scholar 

  • Tang C, Fang RY, Raphael C (1998) Factors affecting soil acidification under legumes II. Effect of phosphorus supply. Aust J Agric Res 49:657–664

    Google Scholar 

  • Tarafdar JC, Yadav RS, Meena SC (2001) Comparative efficiency of acid phosphatase originated from plant and fungal sources. J Plant Nutr Soil Sci 164:279–282

    Google Scholar 

  • Tarafder JC, Claassen N (2003) Organic phosphorus utilization by wheat plants under sterile conditions. Biol Fertil Soils 39:25–29

    Google Scholar 

  • Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116

    Google Scholar 

  • Thakkar J, Narsian V, Patel HH (1993) Inorganic phosphate solubilization by certain soil bacteria: solubilization of natural rock phosphates and pure insoluble inorganic phosphate by Aspergillus awamorii. Indian J Exp Biol 31:743–747

    Google Scholar 

  • Thallar MC, Berlutti F, Schippa S, Lombardi G, Rossolini GM (1994) Characterization and sequence of PhoC, the principal phosphatase-irrepressible acid phosphatase of Morganella morganii. Microbiology 140:1341–1350

    Google Scholar 

  • Thallar MC, Berlutti F, Schippa S, Lori P, Passariello C, Rossolini GM (1995a) Heterogenous patterns of acid phosphatases containing low molecular mass polypeptides in members of the family Enterobacteriaceae. Int J System Bacteriol 4:255–261

    Google Scholar 

  • Thallar MC, Lombardi G, Berlutti F, Schippa S, Rossolini GM (1995b) Cloning and characterization of the NapA acid phosphatase/phosphotransferase of Morganella morganii. Identification of a new family of bacterial acid phosphatase encoding genes. Microbiology 140:147–151

    Google Scholar 

  • Tilak KVBR, Saxena AK, Sadasivan KV (1995) Synergistic effects of phosphate solubilizing bacterium Pseudomonas striata and arbuscular mycorrhizae on soybean. In: Sujan Singh, Adholya A (eds) Mycorrhizae: biofertilizers for the future. Tata Energy Research Institute, New Delhi, pp 224–226

    Google Scholar 

  • Tomar M (2005) Biodiversity of mineral phosphate solubilizing bacteria from chickpea, mustard and wheat rhizosphere. Ph.D. thesis submitted to CCS HAU, Hisar

    Google Scholar 

  • Toro M, Azcon R, Barea JM (1997) Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate solubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl Environ Microbiol 63:4408–4412

    Google Scholar 

  • Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity – magnitude, dynamics, and controlling factors. Science 296:1064–1066

    Google Scholar 

  • Turan M, Ataoglu N, Sahin F (2006) Evaluation of the capacity of phosphate solubilizing bacteria and fungi on different forms of phosphorus in liquid culture. J Sustain Agric 28:99–108

    Google Scholar 

  • Turner BL (2007) Inositol phosphates in soil: amounts, forms and significance of the phosphorylated inositol stereoisomers. In: Tuner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates; linking agriculture and the environment. CABI, Wallingford, pp 186–206

    Google Scholar 

  • Turner BL, Haygarth PM (2001) Biogeochemistry – phosphorus solubilization in rewetted soils. Nature 411:258

    Google Scholar 

  • Tye AJ, Siu FK, Leung TY, Lim BL (2002) Molecular cloning and the biochemical characterization of two novel phytases from Bacillus subtilis 168 and Bacillus licheniformis. Appl Environ Microbiol 59:190–197

    Google Scholar 

  • van Schie BJ, Hellingwerf KE, Vandijkan JP, Elferink MGL, Van Diji JM, Kuenen JG, Konigns N (1985) Energy transduction by electron transfer via a pyrroquinoline quinine dependent glucose dehydrogenase in Escherichia coli, Pseudomonas aeruginosa and Acinetobacter calcoaceticum (var. Lowoffi). J Bacteriol 163:493–499

    Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Google Scholar 

  • Varsha N, Patel HH (1995) Inorganic phosphate solubilization by some yeast. Indian J Microbiol 35:127–132

    Google Scholar 

  • Varsha N, Thakkar J, Patel HH (1994) Isolation and screening of phosphate solubilizing fungi. Indian J Microbiol 34:113–118

    Google Scholar 

  • Venkateswarlu B, Rao AV, Raina P (1984) Evaluation of phosphorus solubilization by microorganisms isolated from arid soils. J Indian Soc Soil Sci 32:273–277

    Google Scholar 

  • Vessey JK, Heisinger KG (2001) Effect of Penicillium bilaii inoculation and phosphorus fertilisation on root and shoot parameters of field-grown pea. Can J Plant Sci 81:361–366

    Google Scholar 

  • Viruel E, Lucca ME, Sineriz F (2011) Plant growth promotion traits of phosphobacteria isolated from Puna, Argentina. Arch Microbiol 193:489–496

    Google Scholar 

  • Vu DT, Tang C, Armstrong RD (2008) Changes and availability of P fraction following 65 years of P application to a calcareous soil in a Mediterranean climate. Plant Soil 304:21–33

    Google Scholar 

  • Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fertil Soils 40:36–43

    Google Scholar 

  • Wall DH, Virginia RA (1999) Control of soil biodiversity – in sight from extreme environments. Appl Soil Ecol 13:137–150

    Google Scholar 

  • Wanner BL (1996) Phosphorus assimilation and control of the phosphate regulon. In: Niedhardt FC, Curtis R III, Ingraham JL, Lin EC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. IASM Press, Washington, DC, pp 1357–1381

    Google Scholar 

  • 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 125:155–166

    Google Scholar 

  • Xie XN, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117

    Google Scholar 

  • Yadav BN, Singh D, Singh SM (2004) Performance of barley (Hordeum vulgare L.) varieties under varying fertilizer levels and microbial inoculation. Agric Sci Digest 24:148–150

    Google Scholar 

  • Yousefi AA, Khavazi K, Moezi AA, Rejali F, Nadian HA (2011) Phosphate solubilizing bacteria and arbuscular mycorrhizal fungi impacts on inorganic phosphorus fractions and wheat growth. World Appl Sci J 15:1310–1318

    Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hungarica 56:263–284

    Google Scholar 

  • Zhao XR, Lin QM (2001) A review of phosphate-dissolving microorganisms. Soil Fertil 3:7–11

    Google Scholar 

  • Zhu F, Qu L, Hong X, Sun X (2011) Isolation and characterization of a phosphate-solubilizing halophilic bacterium Kushneria sp. YCWA18 from Daqiao saltern on the coast of Yellow sea of China. Evid Based Complem Altern Med, Article ID 615032, p 6

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, CCS Haryana Agricultural University, Hisar, 125004, Haryana, India

    Satyavir S. Sindhu, Manisha Phour, Sita Ram Choudhary & Deepika Chaudhary

Authors
  1. Satyavir S. Sindhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manisha Phour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sita Ram Choudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deepika Chaudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Satyavir S. Sindhu .

Editor information

Editors and Affiliations

  1. Department of Chemistry & Biology, Ryerson University, Toronto, Ontario, Canada

    Nagina Parmar

  2. Lystek International Inc., Cambridge, Ontario, Canada

    Ajay Singh

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Sindhu, S.S., Phour, M., Choudhary, S.R., Chaudhary, D. (2014). Phosphorus Cycling: Prospects of Using Rhizosphere Microorganisms for Improving Phosphorus Nutrition of Plants. In: Parmar, N., Singh, A. (eds) Geomicrobiology and Biogeochemistry. Soil Biology, vol 39. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-41837-2_11

Download citation

Publish with us

Policies and ethics

Search

Navigation