Abstract
Phosphate (P)-solubilizing microorganisms as a group form an important part of the microorganisms, which benefit plant growth and development. Growth promotion and increased uptake of phosphate are not the only mechanisms by which these microorganisms exert a positive effect on plants. Microbially mediated solubilization of insoluble phosphates through release of organic acids is often combined with production of other metabolites, which take part in biological control against soilborne phytopathogens. In vitro studies show the potential of P-solubilizing microorganisms for the simultaneous synthesis and release of pathogen-suppressing metabolites, mainly siderophores, phytohormones, and lytic enzymes. Further trends in this field are discussed, suggesting a number of biotechnological approaches through physiological and biochemical studies using various microorganisms.
This is a preview of subscription content, access via your institution.
References
Altomare C, Norvell WA, Bjorkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant growth promoting and biocontrol fungus Trichoderma harzianum rifai 1295-22. Appl Environ Microbiol 65:2926–2933
Azcon R, Azcon C, Barea JM (1978) Effects of plant hormones present in bacterial cultures on the formation and response to VA endomycorrhiza. New Phytol 80:359–364
Bano N, Musarrat J (2003a) Isolation and characterization of phorate degrading soil bacteria of environmental and agronomic significance. Lett Appl Microbiol 36:349–353
Bano N, Musarrat J (2003b) Characterization of a new Pseudomonas aeruginosa strain NJ-15 as a potential biocontrol agent. Curr Microbiol 46:324–328
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
Belanger RR, Benyagoub M (1997) Challenges and prospects for integrated control of powdery mildews in the greenhouse. Can J Plant Pathol 19:310–314
Brown AE, Hamilton JTG (1993) Indole-3-ethanol produced by Zygorrhynchusmoelleri, and indole-3-acetic acid analogue with antifungal activity. Mycol Res 96:71–74
Butler MJ, Gardiner RB, Day AW (2005) Degradation of melanin or inhibition of its synthesis: are these a significant approach as a biological control of phytopathogenic fungi? Biol Control 32:326–336
Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1680
Chernin I, Ismailov Z, Haran S, Chet I (1995) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl Environ Microbiol 61:1720–1726
Chien SH, Sompongee D, Henao J, Hellums DT (1987) Greenhouse evaluation of phosphorus availability from compacted phosphate rocks with urea or with urea and triple superphosphate. Fertil Res 14:245–256
Dalla GC (1986) Esperienze di lotta biologicacontrola fusariosi vascolare del garofano (Trials on the biological control of vascular kilt of carnations). Ann Inst Sper Floric 17:3012
Dar Gh Hassan, Zargar MY, Beigh GM (1997) Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microb Ecol 34:74–80
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 24:358–364
Del Campillo SE, Van der Zee SEATM, Torrent J (1999) Modelling long-term phosphorus leaching and changes in phosphorus fertility in excessively fertilized acid sandy soils. Eur J Soil Sci 50:391–399
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. Microbiol Res 159:371–394
Droog F (1997) Plant glutathione S-transferases, a tale of theta and tau. J Plant Growth Regul 16:95–107
Duffy B, Defago G (1999) Trace mineral amendments in agriculture for optimizing the biocontrol activity of plant-associated bacteria. In: Berthelin P, Huang M, Bollag JM, Andreux F (eds) Effect of mineral-organic-microorganism interactions on soil and freshwater environments. Kluwer Academic & Plenum, New York, pp 295–304
Dugassa GD, von Alten H, Schonbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182
Dunn C, Crowley JJ, Moenne-Loccoz Y, Dowling DN, de Bruijn FJ, O’Gara F (1997) Biological control of Pythium ultinum by Stenotrophomonasmaltophilia W18 is mediated by an extracellular proteolytic activity. Microbiology 143:3921–3931
Fenice M, Selbmann L, Federici F, Vassilev N (2000) Application of encapsulated Penicillium variabile P16 in solubilization of rock phosphate. Biores Technol 73:157–162
Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533
Fravel DR, Roberts DP (1991) In situ evidence for the role of glucose oxidase in the biocontrol of Verticillium wilt by Talaromyces flavus. Biocontrol Sci Technol 1:91–99
Gerhardson B (2002) Biological substitutes for pesticides. Trends Biotechnol 20:338–343
Gildon A, Tinker PB (1983) Interactions of vesicular-arbuscular mycorrhizal infection and heavy metals in plants. I. The effects of heavy metals on the development of vesicular-arbuscular mycorrhizae. New Phytol 95:247–261
Goldstein AH (1986) Bacterial solubilization of mineral phosphates: historical perspective and future prospects. Am J Altern Agric 1:51–57
Goldstein AH (2000) Bioprocessing of rock phosphate ore: essential technical considerations for the development of a successful commercial technology. IFA Technical Conference, New Orleans, LA, pp 1–21. http://goldsteinlab.alfred.edu/publications.html
Goldstein AH, Rogers RD (1999) Biomediated continuous release phosphate fertilizer. US Patent 5,912,398
Guerinot ML, Meidl EJ, Plessner O (1990) Citrate as a siderophore in Bradyrhizobium japonicum. J Bacteriol 172:3298–3303
Hahn K, Strittmatter (1994) Pathogen-defence gene prp1-1 from potato encodes an auxin-responsive glutathione S-transferase. Eur J Biochem 226:619–626
Hamill JD (1993) Alterations in auxin and cytokinin metabolism of higher plants due to expression of specific genes from pathogenic bacteria: a review. Aust J Plant Physiol 20:405–423
Harman GE, Bjorkman T (1998) Potential and existing uses of Trichoderma and Gliocladium for plant disease control and plant growth enhancement. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium, vol 2. Taylor and Francis, London, UK, pp 229–265
Harman GE, Hayes CK, Lorito M, Broadway RM, Di Pietro A, Peterbaues C, Tronsmo A (1993) Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase. Phytopathology 83:313–318
Hoitink HAJ, Kraus MS, Han DY (2001) Spectrum and mechanisms of plant disease control with composts. In: Stoffela PJ, Kahn BA (eds) Compost utilization in horticultural cropping systems. Lewis, Boca Raton, FL, pp 263–273
Iyamuremye F, Dick RP (1996) Organic amendments and phosphorus sorption by soils. Adv Agron 56:139–185
Jeffries P, Gianinazzi S, Perotto S, Turnau K (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16
Johansson J, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 1:1–13
Khan MR, Khan SM (2001) Biomanagement of Fusarium wilt of tomato by the soil application of certain phosphate-solubilizing microorganisms. Int J Pest Manag 47:227–231
Khan MR, Khan SM (2002) Effect of root-dip treatment with certain phosphate-solubilizing microorganisms on the Fusarium wilt of tomato. Biores Technol 85:213–215
Kloepper JW, Lifshitz K, Zablotovicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–43
Kpomblekou K, Tabatabai MA (1994) Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci 158:442–453
Kpomblekou K, Chien SH, Henao J, Hill WA (1991) Greenhouse evaluation of phosphate fertilizers produced from Togo phosphate rocks. Commun Soil Sci Plant Anal 22:63–73
Krishnaraj PU, Goldstein AH (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
Kucey RMN, Jansen HH, Leggett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42:199–228
Lambais MR, Mehdy MC (1995) Suppression of endochitinase, beta-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol Plant-Microb Interact 6:75–83
Lehinos V (1994) Effects of pH and glucose on auxin production of phosphate-solubilizing rhizobacteria in vitro. Microbiol Res 149:135–138
Lehinos V, Vacek O (1994) Biosynthesis of auxin by phosphate-solubilizing rhizobacteria from wheat (Triticum aestivum) and rye (Secale cereale). Microbiol Res 149:31–35
Lemanceau P, Alabouvette C, Meyer JM (1985) Production of fusarinine and iron assimilation by pathogenic and non-pathogenic Fusarium. In: Swinburne TR (ed) Iron, siderophores and plant diseases. Plenum, London, pp 251–259
Machuca A, Napoleao D, Milagres AMF (2001) Detection of metal-chelating compounds from wood-rotting fungi Trametes versicolor and Wolfiporia cocos. World J Microbiol Biotechnol 17:687–690
Martinez Noel GMA, Madrid EA, Botín R, Lamattina L (2001) Indole acetic acid attenuates disease severity in potato-Phytophthora infestans interaction and inhibits the pathogen growth in vitro. Plant Physiol Biochem 39:815–823
Milagres AMF, Machuca A, Napoleao D (1999) Detection of siderophore production from several fungi and bacteria by a modification of chrome azurol S (CAS) agar plate assay. J Microbiol Methods 37:1–6
Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant Soil 185:241–251
Norlaeny N, Marschner H, Gerge E (1996) Effects of liming and mycorrhizal colonization on soil phosphate depletion and phosphate uptake by maize (Zea mays L.) and soybean (Glycine max L.) grown in two tropical acid soils. Plant Soil 181:275–285
Ordentlich A, Elad Y, Chet I (1988) The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology 78:48–88
Pal KK, Tilak VBP, Saxena AK, Dey R, Singh CS (2001) Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiol Res 156:209–223
Patidar P, Agrawal D, Banerjee T, Patil S (2005) Optimization of process parameters for chitinase production by soil isolates of Penicillium chrysogenum under solid substrate fermentation. Proc Biochem 40:2962–2967
Petruccioli M, Federici F, Bucke C, Keshavarz T (1999) Enhancement of glucose oxidase production by Penicillium variabile P16. Enzyme Microb Technol 24:397–401
Postma J, Montanari M, van der Boogert PHJF (2003) Microbial enrichment to enhance the disease suppressive activity of compost. Eur J Soil Biol 39:157–163
Pozo M, Azcon C, Barea J, Dumas-Gaudot E (1998) Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophtora parasitica. J Exp Bot 49:1729–1739
Prabhu V, Biolchini PF, Boyer GL (1996) Detection and identification of ferricrocin produced by ectendomycorrhizal fungi in the genus Wilcoxina. BioMetals 9:229–234
Rajan SSS, Watkinson JH (1993) Unacidulated and partially acidulated phosphate rocks. Agronomic effectiveness and the rate of dissolution of phosphate rock. Fertil Res 33:267–277
Rattanakit N, Plikomol A, Yano S, Wakayama M, Tachiki T (2002) Utilization of shrimp shellfish waste as a substrate for solid-state cultivation of Aspergillus sp. S1–13: evaluation of a culture based on chitinase formation which is necessary for chitin-assimilation. J Biosci Bioeng 93:550–556
Rausher MD (2001) Co-evolution and plant resistance to natural enemies. Nature 411:857–864
Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906
Roco A, Perez LM (2001) In vitro biocontrol activity of Trichoderma harzianum on Alternaria alternata in the presence of growth regulators. Electron J Biotechnol 4. http://www.ejbiotechnology.info/content/vol4/issue2/full/1/
Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339
Rogers D,Wolfram JH (1993) Microbial solubilization of phosphate. US Patent 5,256,544
Sattar MA, Gaur AC (1987) Production of auxins and gibberellins by phosphate-dissolving microorganisms. Zentralbl Mikrobiol 142:393–395
Segall I (1995) Marketing compost as a pest control product. Biocycle 36:65–67
Shapira R, Ordentlich A, Chet I, Openheim AB (1989) Control of plant diseases by chitinase expressed from cloned DNA in Escherichia coli. Phytopathology 79:1246–1249
Sinclair A, Dyson CB (1988) An interim report on the MAF National Series forms of phosphate fertilizer trials, herbage dry matter production for growing seasons 1982/83 to 1987/8 inclusive. MAFTech, Wellington
Smith SE, Gianinazzi-Pearson V (1988) Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annu Rev Plant Physiol Plant Mol Biol 39:211–244
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, San Diego
Smith SE, St. John BJ, Smith FA, Nicholas DJD (1985) Activity of glutamine synthetase and glutamate dehydrogenase in Trifolium subterraneum L. and Allium cepa L.: effects of mycorrhizal infection and phosphate nutrition. New Phytol 99:211–227
Stleger RJ, Cooper RM, Charnley AK (1986) Cuticle degrading enzyme of entomopathogenic fungi: cuticle degradation in vitro by enzymes from entomopathogens. J Invertebr Pathol 47:167–177
Strack D, Fester T, Hause B, Schliemann W, Walter H (2003) Arbuscular mycorrhiza: biological, chemical and molecular aspects. J Chem Ecol 29:1955–1979
Stuvier MH, Custers JHHV (2001) Engineering disease resistance in plants. Nature 411:865–868
Sylvia D (1998) Activity of external hyphae of vesicular-arbuscular mycorrhizal fungi. Soil Biol Biochem 20:39–43
Traquair JA (1995) Fungal biocontrol of root diseases: endomycorrhizal suppression of cylindrocarpon root rot. Can J Bot 73:S89–S95
Vassilev N, Vassileva M (2003) Biotechnological solubilization of rock phosphate on media containing agro-industrial wastes. Appl Microbiol Biotechnol 61:435–440
Vassilev N, Vassileva M (2004) Multifunctional properties of a plant growth promoting bacterium entrapped in k-carrageenan. In: Pedraz JL, Orive G, Poncelet D (eds) XII international workshop on bioencapsulation, Vitoria, Univ Pais Vasco, 24–26 September 2004, pp 162–166
Vassilev N, Fenice M, Federici F (1996) Rock phosphate solubilization with gluconic acid produced by immobilized Penicillium variabile P16. Biotechnol Tech 10:585–588
Vassilev N, Vassileva M, Azcon R (1997a) Solubilization of rock phosphate by immobilized cells of Aspergillus niger. Biores Technol 59:1–4
Vassilev N, Fenice M, Federici F (1997b) Olive mill waste water treatment by immobilized cells of Aspergillus niger and its enrichment with soluble phosphate. Proc Biochem 32:617–620
Vassilev N, Toro M, Vassileva M (1997c) Rock phosphate solubilization by immobilized cells of Enterobacter sp. in fermentation and soil conditions. Biores Technol 61:29–32
Vassilev N, Vassileva M, Fenice M, Federici F (2001) Immobilized cell technology applied in solubilization of insoluble inorganic (rock) phosphates and P plant acquisition. Biores Technol 79:263–271
Vassilev N, Nikolaeva I, Vassileva M (2005a) Biocontrol properties of microbially-treated sugar beet wastes in presence of rock phosphate. J Biotechnol 118S1:S177
Vassilev N, Nikolaeva I, Vassileva M (2005b) Polymer-based preparation of soil inoculants: applications to arbuscular mycorrhizal fungi. Rev Environ Sci Biotechnol 4:235–243
Vassilev N, Medina A, Vassileva M (2006a) Microbial solubilization of rock phosphate on media containing agro-industrial wastes and effect of the resulting products on plant growth and P uptake. Plant Soil (in press)
Vassilev N, Nikolaeva I, Vassileva M (2006b) Phosphate ore solubilization and simultaneous indole-3-acetic acid production by a gel-entrapped bacterium in fermentation conditions. Chem Eng Commun (in press)
Vassileva M, Azcon R, Barea JM, Vassilev N (1998) Application of encapsulated filamentous fungus in solubilization of inorganic phosphate. J Biotechnol 63:67–72
Vassileva M, Azcon R, Barea JM, Vassilev N (2000) Rock phosphate solubilization by free and encapsulated cells of Yarrowia lipolytica. Proc Biochem 35:693–697
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151
Winkelmann G (1979) Surface polymers and hydroxyl acids. A model of iron supply in sideramine-free fungi. Arch Microbiol 121:43–51
Winkelmann G (1991) Importance of siderophores in fungal growth, sporulation and spore germination. In: Hawksworth DL (ed) Frontiers in mycology. CAB International, Wallingford, pp 49–65
Yao Q, Li X, Feng G, Christie P (2001) Mobilization of sparingly soluble inorganic phosphates by the external mycelium of an arbuscular mycorrhizal fungus. Plant Soil 230:279–285
Zayed G, Abdel-Motaal H (2005) Bio-active composts from rice straw enriched with rock phosphate and their effect on the phosphorous nutrition and microbial community in rhizosphere of cowpea. Biores Technol 96:929–935
Acknowledgements
This work is supported by Project MEC CTM2005-06955 and R&C Programme.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vassilev, N., Vassileva, M. & Nikolaeva, I. Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71, 137–144 (2006). https://doi.org/10.1007/s00253-006-0380-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-006-0380-z
Keywords
- Arbuscular Mycorrhizal
- Rock Phosphate
- Soluble Phosphate
- Siderophore Production
- Biocontrol Activity