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Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria

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Abstract

Plant growth-promoting bacteria (PGPB) are soil and rhizosphere bacteria that can benefit plant growth by different mechanisms. The ability of some microorganisms to convert insoluble phosphorus (P) to an accessible form, like orthophosphate, is an important trait in a PGPB for increasing plant yields. In this mini-review, the isolation and characterization of genes involved in mineralization of organic P sources (by the action of enzymes acid phosphatases and phytases), as well as mineral phosphate solubilization, is reviewed. Preliminary results achieved in the engineering of bacterial strains for improving capacity for phosphate solubilization are presented, and application of this knowledge to improving agricultural inoculants is discussed.

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References

  • Armarger N (2002) Genetically modified bacteria in agriculture. Biochimie 84:1061–1072

    Article  Google Scholar 

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

    PubMed  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 

  • Baskanova G, Macaskie L E (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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Deng S, Summers M L, Kahn M L, McDermontt T R (1998) Cloning and characterization of a Rhizobium. meliloti nonspecific acid phosphatase. Arch. Microbiol. 170:18–26

    Article  PubMed  CAS  Google Scholar 

  • Deng S, Elkins J G, Da L H, Botero L M, McDermott T R (2001) Cloning and characterization of a second acid phosphatase from Sinorhizobium meliloti strain 104A14. Arch. Microbiol. 176:255–263

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Glick B R (1995) The enhancement of plant growth by free living bacteria. Can. J. Microbiol. 41:109–117

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Goldstein A H (1996) Involvement of the quinoprotein glucose dehydrogenase in the solubilization of exogenous phosphates by Gram-negative bacteria. In: Torriani-Gorini A, Yagil E, Silver S (eds) Phosphate in Microorganisms: Cellular and Molecular Biology. ASM Press, Washington, DC, pp. 197–203

    Google Scholar 

  • Golovan S, Wang G, Zhang J, Forsberg C W (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

    Article  PubMed  CAS  Google Scholar 

  • Iddris E E, 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 effect. Microbiology 148:2097–2109

    Google Scholar 

  • Igual J M, Valverde A, Cervantes E, Velázquez E (2001) Phosphate-solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie 21:561–568

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kerovuo J, Lauraeus 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

    PubMed  CAS  Google Scholar 

  • Kim K Y, McDonald G A, Jordan D (1997) Solubilization of hydroxypatite by Enterobacter agglomerans and cloned Escherichia coli in culture medium. Biol. Fert. Soils 24:347–352

    Article  CAS  Google Scholar 

  • Kim Y O, Lee J K, Kim H K, Yu J H, Oh T K (1998a) Cloning of the thermostable phytase gene (phy) from Bacillus sp. DS11 and its overexpression in Escherichia coli. FEMS Microbiol. Lett. 162:185–191

    Article  CAS  Google Scholar 

  • Kim K Y, Jordan D, Krishnan H B (1998b) 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 

  • Krishnaraj P U, Goldstein A H (2001) Cloning of a Serratia marcescens DNA fragment that induces quinoprotein glucose dehydrogenase-mediated gluconic acid production in Escherichia coli in the presence of stationary phase Serratia marcescens. FEMS Microbiol. Lett. 205:215–220

    Article  PubMed  CAS  Google Scholar 

  • Krishnaraj P U, Sadasivam K V, Khanuja S PS (1999) Mineral phosphate soil defective mutants of Pseudomonas sp. express pleiotropic phenotypes. Curr. Sci. (Bangalore, India) 76:1032–1034

    Google Scholar 

  • Lei X G, Stahl C H (2001) Biotechnological development of effective phytases for mineral nutrition and environmental protection. Appl. Microbiol. Biotechnol. 57:474–481

    Article  PubMed  CAS  Google Scholar 

  • Liu S T, Lee L Y, Taj C Y, Hung C H, Chang Y S, Wolfrang J H, Rogers R, Goldstein A H (1992) Cloning of an Erwinia herbicola gene necessary for gluconic acid production and enhanced mineral phosphate solubilization in Escherichia coli HB101: nucleotide sequence and probable involvement in biosynthesis of the coenzyme Pyrroloquinoline Quinone. J. Bacteriol. 174:5814–5819

    PubMed  CAS  Google Scholar 

  • López-Bucio J, de la Vega O M, Guevara-García A, Herrera-Estrella L (2000) Enhanced phophorus uptake in transgenic tobacco plants that overproduce citrate. Nat. Biotechnol. 18:450–453

    Article  PubMed  Google Scholar 

  • Macaskie L E, Yong P, Doyle T C, Roig M G, Díaz M, Manzano T (1997) Bioremediation of uranium-bearing wastewater: biochemical and chemical factors affecting bioprocess application. Biotechnol. Bioeng. 53:100–109

    Article  CAS  PubMed  Google Scholar 

  • Morrissey J P, Walsh U F; O’Donnell A, Moenne-Loccoz Y, O’Gara F (2002) Exploitation of genetically modified inoculants for industrial ecology applications. Antonie van Leeuwenhoek 81:599–606

    Article  PubMed  CAS  Google Scholar 

  • Reilly T J, Baron G S, Nano F, Kuhlenschmidt M S (1996) Characterization and sequencing of a respiratory burst-inhibiting acid phosphatase from Francisella tularensis. J. Biol. Chem. 271:10973–10983

    Article  PubMed  CAS  Google Scholar 

  • Richardson A E (1994) Soil microorganisms and phosphorous availability. In: Pankhurst CE, Doube BM, Gupta VVSR (Eds) Soil Biota: Management in Sustainable Farming Systems. CSIRO, Victoria, Australia pp. 50–62

    Google Scholar 

  • Richardson A E, Hadobas P A, Hayes J E (2001a) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorous from phytate. Plant J 25:641–649

    Article  CAS  Google Scholar 

  • Richardson A E, Hadobas P A, Hayes J E, O’Hara C P, Simpson R J (2001b) Utilization of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil micro-organisms. Plant Soil 229:47–56

    Article  CAS  Google Scholar 

  • Rodríguez E, Han Y, Lei X G (1999) Cloning, sequencing and expression of an Escherichia. coli acid phopshatase/phytase gene (appA2) isolated from pig colon. Biochem. Biophys. Res. Comm. 257:117–123

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rossolini G M, Shipa S, Riccio M L, Berlutti F, Macaskie L E, Thaller M C (1998) Bacterial non-specific acid phosphatases: physiology, evolution, and use as tools in microbial biotechnology. Cell Mol. Life Sci. 54:833–850

    Article  PubMed  CAS  Google Scholar 

  • Tarafdar J C, Jung A (1987) Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus. Biol. Fertil. Soils 3:199–204

    Article  CAS  Google Scholar 

  • Tarafdar J C, Claassen N (1988) Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biol. Fertil. Soils 5:308–312

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Thaller M C, Berlutti F, Schippa S, Iori P, Passariello C, Rossolini G M (1995a) Heterogeneous patterns of acid phosphatases containing low-molecular-mass polypeptides in members of the family Enterobacteriaceae. Int. J. Syst. Bacteriol. 4:255–261

    Article  Google Scholar 

  • Thaller M C, Lombardi G, Berlutti F, Schippa S, Rossolini G M (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 

  • Tye A J, Siu F K, Leung T Y, Lim B L (2002) Molecular cloning and the biochemical characterization of two novel phytases from Bacillus subtilis 168 and Bacillus licheniformis. Appl. Microbiol. Biotechnol. 59:190–197

    Article  PubMed  CAS  Google Scholar 

  • Wanner B L (1996) Phosphorus assimilation and control of the phosphate regulon. In: Niedhardt FC, Curtiss III R, 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, 2 1, ASM Press, Washington, DC, pp 1357–1381

    Google Scholar 

  • Yanming H, Wilson D B, Lei X G (1999) Expression of an Aspergillus niger phytase gene (phyA) in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 65:15–18

    Google Scholar 

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Acknowledgements

H.R. received support from Consejo Nacional de Ciencia y Tecnología of Mexico (CONACyT Catedra Patrimonial de Excelencia grant EX-000580). We thank Ira Fogel at CIB for editing the English text.

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Rodríguez, H., Fraga, R., Gonzalez, T. et al. Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287, 15–21 (2006). https://doi.org/10.1007/s11104-006-9056-9

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