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Plant and Soil

, Volume 287, Issue 1–2, pp 15–21 | Cite as

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

  • H. RodríguezEmail author
  • R. Fraga
  • T. Gonzalez
  • Y. Bashan
Article

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.

Keywords

genetically modified microorganisms organic acids phosphatases phosphorus solubilization phytases plant growth promoting bacteria 

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Notes

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.

References

  1. Armarger N (2002) Genetically modified bacteria in agriculture. Biochimie 84:1061–1072CrossRefGoogle Scholar
  2. 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. 61:972–978PubMedGoogle Scholar
  3. 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 32:265–272CrossRefGoogle Scholar
  4. 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. 54:319–329CrossRefGoogle Scholar
  5. Beacham I R (1980) Periplasmic enzymes in Gram-negative bacteria. Int. J. Biochem. 10:877–883CrossRefGoogle Scholar
  6. 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. 14:635–638PubMedCrossRefGoogle Scholar
  7. 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. 172:6568–6572PubMedGoogle Scholar
  8. Deng S, Summers M L, Kahn M L, McDermontt T R (1998) Cloning and characterization of a Rhizobium. meliloti nonspecific acid phosphatase. Arch. Microbiol. 170:18–26PubMedCrossRefGoogle Scholar
  9. 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. 176:255–263PubMedCrossRefGoogle Scholar
  10. 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. 21:359–369CrossRefGoogle Scholar
  11. Glick B R (1995) The enhancement of plant growth by free living bacteria. Can. J. Microbiol. 41:109–117CrossRefGoogle Scholar
  12. Goldstein A H, Liu S T (1987) Molecular cloning and regulation of a mineral phosphate solubilizing gene from Erwinia herbicola. Biotechnology 5:72–74CrossRefGoogle Scholar
  13. 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. 197–203Google Scholar
  14. 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. 46:59–71PubMedCrossRefGoogle Scholar
  15. 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 148:2097–2109Google Scholar
  16. 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 21:561–568CrossRefGoogle Scholar
  17. Illmer P, Shinnera F (1995) Solubilization of inorganic calcium phosphates. Solubilization mechanisms. Soil Biol. Biochem. 27:257–263CrossRefGoogle Scholar
  18. 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. 64:2079–2085PubMedGoogle Scholar
  19. 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 24:347–352CrossRefGoogle Scholar
  20. 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. 162:185–191CrossRefGoogle Scholar
  21. 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. 159:121–127Google Scholar
  22. 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. 205:215–220PubMedCrossRefGoogle Scholar
  23. 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) 76:1032–1034Google Scholar
  24. Lei X G, Stahl C H (2001) Biotechnological development of effective phytases for mineral nutrition and environmental protection. Appl. Microbiol. Biotechnol. 57:474–481PubMedCrossRefGoogle Scholar
  25. 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. 174:5814–5819PubMedGoogle Scholar
  26. 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. 18:450–453PubMedCrossRefGoogle Scholar
  27. 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. 53:100–109CrossRefPubMedGoogle Scholar
  28. 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 81:599–606PubMedCrossRefGoogle Scholar
  29. 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. 271:10973–10983PubMedCrossRefGoogle Scholar
  30. 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. 50–62Google Scholar
  31. 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 25:641–649CrossRefGoogle Scholar
  32. 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 229:47–56CrossRefGoogle Scholar
  33. 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. 257:117–123PubMedCrossRefGoogle Scholar
  34. Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17:319–339PubMedCrossRefGoogle Scholar
  35. Rodríguez H, Gonzalez T, Selman G (2000b) Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. J. Biotechnol. 84:155–161CrossRefGoogle Scholar
  36. 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. 40:362–366CrossRefGoogle Scholar
  37. 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. 54:833–850PubMedCrossRefGoogle Scholar
  38. Tarafdar J C, Jung A (1987) Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus. Biol. Fertil. Soils 3:199–204CrossRefGoogle Scholar
  39. 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 5:308–312CrossRefGoogle Scholar
  40. 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 140:1341–1350PubMedCrossRefGoogle Scholar
  41. 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. 4:255–261CrossRefGoogle Scholar
  42. 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 140:147–151Google Scholar
  43. 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. 59:190–197PubMedCrossRefGoogle Scholar
  44. 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 1357–1381Google Scholar
  45. Yanming H, Wilson D B, Lei X G (1999) Expression of an Aspergillus niger phytase gene (phyA) in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 65:15–18Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • H. Rodríguez
    • 1
    • 2
    Email author
  • R. Fraga
    • 1
  • T. Gonzalez
    • 1
  • Y. Bashan
    • 2
  1. 1.Dept. of MicrobiologyCuban Research Institute on Sugar Cane By-Products (ICIDCA)HavanaCuba
  2. 2.Environmental Microbiology GroupCenter for Biological Research of the Northwest (CIB)La Paz B.C.S.Mexico

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