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Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure

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Abstract

Literature analysis and chemical considerations of biological phosphate solubilization have shown that the commonly used selection factor for this trait, tricalcium phosphate (TCP), is relatively weak and unreliable as a universal selection factor for isolating and testing phosphate-solubilizing bacteria (PSB) for enhancing plant growth. Most publications describing isolation of PSB employed TCP. The use of TCP usually yields many (up to several thousands per study) isolates “supposedly” PSB. When these isolates are further tested for direct contribution of phosphorus to the plants, only a very few are true PSB. Other compounds are also tested, but on a very small scale. These phosphates (P), mainly Fe-P, Al-P, and several Ca-P, are even less soluble than TCP in water. Because soils greatly vary by pH and several chemical considerations, it appears that there is no metal-P compound that can serve as the universal selection factor for PSB. A practical approach is to use a combination of two or three metal-P compounds together or in tandem, according to the end use of these bacteria—Ca-P compounds (including rock phosphates) for alkaline soils, Fe-P and Al-P compounds for acidic soils, and phytates for soils rich in organic P. Isolates with abundant production of acids will be isolated. This approach will reduce the number of potential PSB from numerous isolates to just a few. Once a potential isolate is identified, it must be further tested for direct contribution to P plant nutrition and not necessarily to general growth promotion, as commonly done because promotion of growth, even by PSB, can be the outcome of other mechanisms. Isolates that do not comply with this general sequence of testing should not be declared as PSB.

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References

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    Article  PubMed  CAS  Google Scholar 

  • Ahn PM (1993) Tropical soils and fertilizer use. Intermediate tropical agriculture series. Longman, Essex

    Google Scholar 

  • Alikhani HA, Saleh-Rastin N, Antoun H (2006) Phosphate solubilization activity of rhizobia native to Iranian soils. Plant Soil 287:35–41

    Article  CAS  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, 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

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Babana AH, Antoun H (2005) Biological system for improving the availability of Tilemsi phosphate rock for wheat (Triticum aestivum L) cultivated in Mali. Nutr Cycl Agroecosyst 72:147–157

    Article  Google Scholar 

  • Babana AH, Antoun H (2006) Effect of Tilemsi phosphate rock-solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L) in Mali. Plant Soil 287:51–58

    Article  CAS  Google Scholar 

  • Bache BW (1963) Aluminium and iron phosphate studies relating to soils. I. Solution and hydrolysis of variscite and strengite. J Soil Sci 14:113–123

    Article  Google Scholar 

  • Baig KS, Arshad M, Shaharoona B, Khalid A, Ahmed I (2012) Comparative effectiveness of Bacillus spp. possessing either dual or single growth-promoting traits for improving phosphorus uptake, growth and yield of wheat (Triticum aestivum L.). Ann Microbiol. doi:10.1007/s13213-011-0352-0

  • Bardiya MC, Gaur AC (1974) Isolation and screening of microorganisms dissolving low-grade rock phosphate. Folia Microbiol 19:386–389

    Article  CAS  Google Scholar 

  • Barret M, Morrissey JP, O'Gara F (2011) Functional genomics analysis of plant-growth promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE (2005) Bacteria/Plant growth-promotion. In: Hillel D (ed) Encyclopedia of soils in the environment. Vol. 1. Elsevier, Oxford, pp 103–115

    Google Scholar 

  • Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bationo A, Ayuk E, Ballo D, Kone M (1997) Agronomic and economic evaluation of Tilemsi phosphate rock in different agroecological zones of Mali. Nutr Cycl Agrosyst 48:179–189

    Article  Google Scholar 

  • Belimov AA, Safronova VI, Mimura T (2002) Response of spring rape (Brassica napus var. oleifera L.) to inoculation with plant growth promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase depends on nutrient status of the plant. Can J Microbiol 48:189–199

    Article  PubMed  CAS  Google Scholar 

  • Ben Farhat M, Farhat A, Bejar W, Kammoun R, Bouchaala K, Fourati A, Antoun H, Bejar S, Chouayekh H (2009) Characterization of the mineral phosphate solubilizing activity of Serratia marcescens CTM 50650 isolated from the phosphate mine of Gafsa. Arch Microbiol 191:815–824

    Article  PubMed  CAS  Google Scholar 

  • Brosheer JC, Lenfesty FA, Anderson JF Jr (1954) Solubility in the system aluminum phosphate–phosphoric acid–water. J Am Chem Soc 76:5951–5956

    Article  CAS  Google Scholar 

  • Castagno LN, Estrella MJ, Sannazzaro AI, 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 110:151–1165

    Article  CAS  Google Scholar 

  • Cawthray GR (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J Chromatogr 1011:233–240

    Article  CAS  Google Scholar 

  • Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarium biovar phaseoli. Plant Soil 184:311–321

    Article  CAS  Google Scholar 

  • Chang C-H, Yang S-S (2009) Thermo-tolerant phosphate-solubilizing microbes for multi-functional biofertilizer preparation. Bioresour Technol 100:1648–1658

    Article  PubMed  CAS  Google Scholar 

  • Chen YP, Rekha PD, Arunshen AB, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41

    Article  Google Scholar 

  • Chung H, Park M, Madhaiyan M, Seshadri S, Song J, Cho H, Sa T (2005) Isolation and characterization of phosphate solubilizing bacteria from the rhizosphere of crop plants of Korea. Soil Biol Biochem 37:1970–1974

    Article  CAS  Google Scholar 

  • Collavino MM, Sansberro PA, Mroginski LA, Aguilar OM (2010) Comparison of in vitro solubilization activity of diverse phosphate-solubilizing bacteria native to acid soil and their ability to promote Phaseolus vulgaris growth. Biol Fertil Soils 46:727–738

    Article  Google Scholar 

  • de Freitas JR, Banerjee NR, Germida JJ (1997) Phosphate solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fertil Soils 24:358–364

    Article  Google Scholar 

  • de-Bashan LE, Bashan Y (2004) Recent advances in removing phosphorus from wastewater and its future use as fertilizer (1997–2003). Water Res 38:4222–4246

    Article  PubMed  CAS  Google Scholar 

  • Dorozhkin SV (2009) Calcium orthophosphate-based biocomposites and hybrid biomaterials. J Mater Sci 44:2343–2387

    Article  CAS  Google Scholar 

  • Dorozhkin SV (2011) Calcium orthophosphates. Occurrence, properties, biomineralization, pathological calcification and biomimetic applications. Biomatter 1:121–164

    Article  PubMed  Google Scholar 

  • Duffield JR, Edwards K, Evans DA, Morrish DM, Vobe RA, Williams DR (1991) Low molecular mass aluminum complex speciation in biofluids. J Coord Chem 23:277–290

    Article  CAS  Google Scholar 

  • El-Tarabily KA, Youssef T (2010) Enhancement of morphological, anatomical and physiological characteristics of seedlings of the mangrove Avicennia marina inoculated with a native phosphate-solubilizing isolate of Oceanobacillus picturae under greenhouse conditions. Plant Soil 332:147–162

    Article  CAS  Google Scholar 

  • Evans WG, Pierce AG (1981) Calcium-phytate complex formation studies. J Am Oil Chem Soc 58:850–851

    Article  CAS  Google Scholar 

  • Fankem H, Ngo Nkot L, Deubel A, Quinn J, Merbach W, Etoa F-X, Nwaga D (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 

  • Fernández LA, Zalba P, Gómez 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ghassemi M, Recht HL (1971) Phosphate precipitation with ferrous iron. Project No. 17010 EKI. US Environmental Protection Agency, Washington, DC, 69 pp

    Google Scholar 

  • Gillis MB, Edwards HM Jr, Young RJ (1962) Studies on the availability of calcium orthophosphates to chickens and turkeys. J Nutr 78:155–161

    PubMed  CAS  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

    Article  Google Scholar 

  • Goldstein AH (2007) Future trends in research on microbial phosphate solubilization: one hundred years of insolubility. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Developments in plant and soil sciences, Vol. 102. Springer, Dordrecht, pp 91–96

    Chapter  Google Scholar 

  • Goldstein AH, Krishnaraj PU (2007) Phosphate solubilizing microorganisms vs. phosphate mobilizing microorganisms: what separates a phenotype from a trait? In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Developments in plant and soil sciences, vol. 102. Springer, Dordrecht, pp 203–213

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Goldstein AH, Braverman K, Osorio N (1999) Evidence for mutualism between a plant growing in a phosphate-limited desert environment and a mineral phosphate solubilizing (MPS) rhizobacterium. FEMS Microbiol Ecol 30:295–300

    Article  PubMed  CAS  Google Scholar 

  • Greaves JE (1922) Influence of salts on bacterial activities of soil. Bot Gaz 73:161–180

    Article  CAS  Google Scholar 

  • Grynspan F, Cheryan M (1983) Calcium phytate: effect of pH and molar ratio on in vitro solubility. J Am Oil Chem Soc 60:1761–1764

    Article  CAS  Google Scholar 

  • Gulati A, Rahi P, Vyas P (2008) Characterization of phosphate-solubilizing fluorescent pseudomonads from the rhizosphere of seabuckthorn growing in the cold deserts of Himalayas. Curr Microbiol 56:73–79

    Article  PubMed  CAS  Google Scholar 

  • Gulati A, Sharma N, Vyas P, Sood S, Rahi P, Pathania V, Prasad R (2010) Organic acid production and plant growth promotion as a function of phosphate solubilization by Acinetobacter rhizosphaerae strain BIHB 723 isolated from the cold deserts of the trans-Himalayas. Arch Microbiol 192:975–983

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Hameeda B, Harini G, Rupela OP, Wani SP, Reddy G (2008) Growth promotion of maize by phosphate solubilizing bacteria isolated from composts and macrofauna. Microbiol Res 163:234–242

    Article  PubMed  CAS  Google Scholar 

  • Harris JN, New PB, Martin PM (2006) Laboratory tests can predict beneficial effects of phosphate-solubilising bacteria on plants. Soil Biol Biochem 38:1521–1526

    Article  CAS  Google Scholar 

  • Haynes RJ (1982) Effects of liming on phosphate availability in acid soils. Plant Soil 68:289–308

    Article  CAS  Google Scholar 

  • He Z, Ohno T, Cade-Menun BJ, Erich MS, Honeycutt CW (2006) Spectral and chemical characterization of phosphates associated with humic substances. Soil Sci Soc Am J 70:1741–1751

    Article  CAS  Google Scholar 

  • Hill JE, Kysela D, Elimelech M (2007) Isolation and assessment of phytate-hydrolysing bacteria from the DelMarVa Peninsula. Environ Microbiol 9:3100–3107

    Article  PubMed  CAS  Google Scholar 

  • Hoffland E (1992) Quantitative evaluation of the role of organic acid exudation in the mobilization of rock phosphate by rape. Plant Soil 140:279–289

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Illmer P, Barbato A, Schinner F (1995) Solubilization of hardly-soluble AlPO4 with P-solubilizing microorganisms. Soil Biol Biochem 27:265–270

    Article  CAS  Google Scholar 

  • Iqbal U, Jamil N, Ali I, Hasnain S (2010) Effect of zinc-phosphate-solubilizing bacterial isolates on growth of Vigna radiate. Ann Microbiol 60:243–248

    Article  Google Scholar 

  • Ishio S, Kuwahara M, Nakawaga H (1986) Conversion of AlPO4-P to Fe-bound P in sea sediments. B Jpn Soc Sci Fish 52:901–911

    Article  CAS  Google Scholar 

  • Jiang J-Q, Graham NJD (1998) Pre-polymerised inorganic coagulants and phosphorus removal by coagulation—a review. Water SA 24:237–244

    CAS  Google Scholar 

  • Johri JK, Surange S, Nautiyal CS (1999) Occurrence of salt, pH, and temperature-tolerant, phosphate-solubilizing bacteria in alkaline soils. Curr Microbiol 39:89–93

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257

    Article  CAS  Google Scholar 

  • Jorquera MA, Hernandez MT, Rengel Z, Marschner P, Mora ML (2008) Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil. Biol Fertil Soils 44:1025–1034

    Article  CAS  Google Scholar 

  • Katiyar V, Goel R (2003) Solubilization of inorganic phosphate and plant growth promotion by cold tolerant mutants of Pseudomonas fluorescens. Microbiol Res 158:163–168

    Article  PubMed  CAS  Google Scholar 

  • Kelley WP (1912) The effects of calcium and magnesium carbonates on some biological transformations of nitrogen in soils. Univ Calif Publ Agric Sci 1:39–49

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Kpomblekou AK, Tabatabai MA (1994) Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci 158:442–453

    Article  Google Scholar 

  • Kucey RMN, Janzen HH, Leggett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42:199–228

    Article  CAS  Google Scholar 

  • Kumar V, Narula N (1999) Solubilization of inorganic phosphates and growth emergence of wheat as affected by Azotobacter chroococcum mutants. Biol Fertil Soils 28:301–305

    Article  CAS  Google Scholar 

  • Linu MS, Stephen J, Jisha MS (2009) Phosphate solubilizing Gluconacetobacter sp., Burkholderia sp. and their potential interaction with cowpea (Vigna unguiculata (L.) Walp.). Int J Agri Res 4:79–87

    CAS  Google Scholar 

  • Liu H, Wu XQ, Ren JH, Ye JR (2011) Isolation and identification of phosphobacteria in poplar rhizosphere from different regions of China. Pedosphere 21:90–97

    Article  Google Scholar 

  • Lobartini JC, Tan KH, Pape C (1998) Dissolution of aluminum and iron phosphate by humic acids. Commun Soil Sci Plant Anal 29:535–544

    Article  CAS  Google Scholar 

  • Lopez BR, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the Southern Sonoran Desert. Arch Microbiol 193:527–541

    Article  PubMed  CAS  Google Scholar 

  • Lopez BR, Tinoco-Ojanguren C, Bacilio M, Mendoza A, Bashan Y (2012) Endophytic bacteria of the rock-dwelling cactus Mammillaria fraileana affect plant growth and mobilization of elements from rocks. Environ Exp Bot 81:26–36

    Article  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  PubMed  CAS  Google Scholar 

  • Mamta Rahi P, Pathania V, Gulati A, Singh B, Bhanwra RK, Tewari R (2010) Stimulatory effect of phosphate-solubilizing bacteria on plant growth, stevioside and rebaudioside-A contents of Stevia rebaudiana Bertoni. Appl Soil Ecol 46:222–229

    Article  Google Scholar 

  • Martin RB (1997) The importance of aluminium chemistry for biological systems. In: Zatta PF, Alfrey AC (eds) Aluminium toxicity in infants’ health and disease. World Scientific, Singapore, pp 3–15

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Merbach W, Fankem H, Deubel A (2009) Influence of rhizosphere bacteria of African oil palm (Elaeis guineensis) on calcium, iron, and aluminum phosphate in vitro mobilization. In: International symposium “Root Research and Applications”, 2–4 September 2009. BOKU, Vienna, Austria. URL: http://asrr.boku.ac.at/fileadmin/files/RRcd/session03/poster/042.pdf

  • Merbach W, Deubel A, Gransee A, Ruppel S, Klamroth A-K (2010) Phosphorus solubilization in the rhizosphere and its possible importance to determine phosphate plant availability in soil. A review with main emphasis on German results. Arch Agron Soil Sci 56(2):119–138

    Article  CAS  Google Scholar 

  • Middleton VG (ed) (2003) Encyclopedia of sediments and sedimentary rocks. Encyclopedia of earth sciences series. Kluwer, Dordrecht

    Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Oberson A, Frossard E (eds) Phosphorus in action. Soil biology vol. 26. Springer, Berlin, pp 215–241

    Chapter  Google Scholar 

  • Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    Article  PubMed  CAS  Google Scholar 

  • Naz I, Bano A (2010) Biochemical, molecular characterization and growth promoting effects of phosphate solubilizing Pseudomonas sp. isolated from weeds grown in salt range of Pakistan. Plant Soil 334:199–207

    Article  CAS  Google Scholar 

  • Ogut M, Er F, Kandemir N (2010) Phosphate solubilization potentials of soil Acinetobacter strains. Biol Fertil Soils 46:707–715

    Article  CAS  Google Scholar 

  • Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP, Guimarães CT, Schaffert RE, Sà NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 4:1782–1787

    Article  CAS  Google Scholar 

  • Park K-H, Lee O-M, Jung H-I, Jeong J-H, Jeon Y-D, Hwang D-Y, Lee C-Y, Son H-J (2010) Rapid solubilization of insoluble phosphate by a novel environmental stress-tolerant Burkholderia vietnamiensis M6 isolated from ginseng rhizospheric soil. Appl Microbiol Biotechnol 86:947–955

    Article  PubMed  CAS  Google Scholar 

  • Peix A, Rivas R, Mateos PF, Martinez-Molina E, Rodriguez-Barrueco C, Velazquez E (2003) Pseudomonas rhizosphaerae sp. nov., a novel species that actively solubilizes phosphate in vitro. Int J Syst Evol Microbiol 53:2067–2072

    Article  PubMed  CAS  Google Scholar 

  • Peix A, Rivas R, Santa-Regina I, Mateos PF, Martinez-Molina E, Rodriguez-Barrueco C, Velazquez E (2004) Pseudomonas lutea sp. nov., a novel phosphate-solubilizing bacterium isolated from the rhizosphere of grasses. Int J Syst Evol Microbiol 54:847–850

    Article  PubMed  CAS  Google Scholar 

  • Pérez E, Sulbarán M, Ball MM, Yarzábal LA (2007) Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biol Biochem 39:2905–2914

    Article  CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphates in soil in relation with vital activity of some microbial species. Mikrobiologiya 17:362–370 (in Russian)

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2004b) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. II. Growth promotion of cactus seedlings. Plant Biol 6:643–650

    Article  PubMed  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2009a) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401

    Article  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2009b) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408

    Article  CAS  Google Scholar 

  • Rajan SSS, Watkinson JH, Sinclair AG (1996) Phosphate rocks for direct application to soils. Adv Agron 57:77–159

    Article  CAS  Google Scholar 

  • Rajapaksha RMCP, Herath D, Senanayake AP, Senevirathne MGTL (2011) Mobilization of rock phosphate phosphorus through bacterial inoculants to enhance growth and yield of wetland rice. Commun Soil Sci Plant Anal 42:301–314

    Article  CAS  Google Scholar 

  • Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748

    Article  PubMed  CAS  Google Scholar 

  • Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312

    Article  PubMed  CAS  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 33:1741–1746

    Article  CAS  Google Scholar 

  • Reyes I, Valery A, Valduz Z (2006) Phosphate-solubilizing microorganisms isolated from rhizospheric and bulk soils of colonizer plants at an abandoned rock phosphate mine. Plant Soil 287:69–75

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Sackett WG, Patten AJ, Brown CV (1908) The solvent action of soil bacteria upon the insoluble phosphates of raw bonemeal and natural raw rock phosphate. Centralbl Bakteriol 202:688–703

    Google Scholar 

  • Schwab AP (1989) Manganese-phosphate solubility relationships in an acid soil. Soil Sci Soc Am J 53:1654–1660

    Article  CAS  Google Scholar 

  • Selvakumar G, Joshi P, Nazim S, Mishra PK, Bisht JK, Gupta HS (2009) Phosphate solubilization and growth promotion by Pseudomonas fragi CS11RH1 (MTCC 8984), a psychrotolerant bacterium isolated from a high altitude Himalayan rhizosphere. Biologia 64:239–245

    Article  CAS  Google Scholar 

  • Son H-J, Park G-T, Cha M-S, Heo M-S (2006) Solubilization of insoluble inorganic phosphates by a novel salt- and pH-tolerant Pantoea agglomerans R-42 isolated from soybean rhizosphere. Bioresour Technol 97:204–210

    Article  PubMed  CAS  Google Scholar 

  • Song O-R, Lee S-J, Lee Y-S, Lee S-C, Kim K-K, Choi Y-L (2008) Solubilization of insoluble inorganic phosphate by Burkholderia cepacia DA23 isolated from cultivated soil. Braz J Microbiol 39:151–156

    Article  Google Scholar 

  • Srinivasan R, Alagawadi AR, Yandigeri MS, Meena KK, Saxena AK (2012) Characterization of phosphate-solubilizing microorganisms from salt-affected soils of India and their effect on growth of sorghum plants [Sorghum bicolor (L.) Moench]. Ann Microbiol 62:93–105

    Article  CAS  Google Scholar 

  • Stumm W, Morgan JJ (1996) Aquatic chemistry, 3rd edn. Wiley, New York

    Google Scholar 

  • Szymkiewicz-Dabrowska D, Lachacz A, Huszcza-Ciolkowska G (2002) The contribution of soil solution CO2 (HCO 3 ) to incorporation of sparingly soluble phosphates to the pool of phosphates available for plants. Zeszyty Problemowe Postepow Nauk Rolniczych, no. 484, pp. 701-709 (URL: http://psjc.icm.edu.pl/psjc/cgi-bin/getdoc.cgi?AAAA00721)

  • Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Ludueña L, Pena D, Ibáñez F, Fabra A (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431

    Article  CAS  Google Scholar 

  • Trivedi P, Sa T (2008) Pseudomonas corrugata (NRRL B-30409) mutants increased phosphate solubilization, organic acid production, and plant growth at lower temperatures. Curr Microbiol 56:140–144

    Article  PubMed  CAS  Google Scholar 

  • Unno Y, Okubo K, Wasaki J, Shinano T, Osaki M (2005) Plant growth promotion abilities and microscale bacterial dynamics in the rhizosphere of lupin analysed by phytate utilization ability. Environ Microbiol 7:396–404

    Article  PubMed  Google Scholar 

  • Vassilev N, Toro M, Vassileva M, Azcon R, Barea JM (1997) Rock phosphate solubilization by immobilized cells of Enterobacter sp. in fermentation and soil conditions. Bioresour Technol 61:29–32

    Article  CAS  Google Scholar 

  • Vazquez P, Holguin G, Puente ME, Lopez-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Nancollas GH (2008) Calcium orthophosphates: crystallization and dissolution. Chem Rev 108:4628–4669

    Article  PubMed  CAS  Google Scholar 

  • Welch SA, Taunton AE, Banfield JF (2002) Effect of microorganisms and microbial metabolites on apatite dissolution. Geomicrobiol J 19:343–367

    Article  CAS  Google Scholar 

  • Whitelaw MA (1999) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151

    Article  Google Scholar 

  • Xiang W-L, Liang H-Z, Liu S, Luo F, Tang J, Li M-Y, Che Z-M (2011) Isolation and performance evaluation of halotolerant phosphate solubilizing bacteria from the rhizospheric soils of historic Dagong brine well in China. World J Microbiol Biotechnol 27:2629–2637

    Article  CAS  Google Scholar 

  • Xiao CQ, Chi RA, Li WS, Zheng Y (2011) Biosolubilization of phosphorus from rock phosphate by moderately thermophilic and mesophilic bacteria. Miner Eng 24:956–958

    Article  CAS  Google Scholar 

  • Yu X, Liu X, Zhu TH, Liu GH, Mao C (2011) Isolation and characterization of phosphate-solubilizing bacteria from walnut and their effect on growth and phosphorus mobilization. Biol Fertil Soils 47:437–446

    Article  CAS  Google Scholar 

  • Zou K, Binkley D, Doxtader KG (1992) A new method for estimating gross phosphorus mineralization and immobilization rates in soils. Plant Soil 147:243–250

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Prof. Hani Antoun from Laval University, Quebec, Canada for proposing the type of evaluations that were needed for this essay. Ira Fogel of CIBNOR provided editorial services. Preparation of this essay was supported by The Bashan Foundation, USA.

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Correspondence to Yoav Bashan.

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This study is dedicated to the memory of the German/Spanish mycorrhizae researcher Dr. Horst Vierheilig (1964–2011) of CSIC, Spain.

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Bashan, Y., Kamnev, A.A. & de-Bashan, L.E. Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49, 465–479 (2013). https://doi.org/10.1007/s00374-012-0737-7

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  • DOI: https://doi.org/10.1007/s00374-012-0737-7

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