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Rock phosphate-solubilizing Actinomycetes: screening for plant growth-promoting activities

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Abstract

In order to select Actinobacteria that could improve plant growth and thus agricultural yield, we assessed different plant growth promoting (PGP) abilities of eight rock phosphate (RP)-solubilizing Actinomycete isolates originating from Moroccan phosphate mines. Six of these strains were able to grow on root exudates of the wheat plant as sole nutrient sources and were efficiently releasing soluble phosphate from RP. These strains also inhibited the growth of potentially phytopathogenic fungi, bacteria (Gram +/−) or yeasts. Five of these strains produced indoleacetic acid and four showed endophytic properties. When these strains were grown, in the presence of the wheat plant, in a synthetic minimum medium (SMM) containing insoluble RP as unique phosphate source or in soil experiment, the most active RP-solubilizing strains had the highest stimulatory effect on the production of plant biomass. The most efficient strain Streptomyces griseus-related strain (BH7), stimulated aerial growth of the plant more than 70% in test tubes and more than 30% in RP soil compared to the non-inoculated control treatment. This study demonstrated that our selected Actinomycete strains could be used for the development of novel, non-polluting; farming practices by entering in the formulation of novel biofertilizer and biocontrol products constituted by spores and/or mycelium of the ad hoc Actinobacteria in association with pulverized RP.

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References

  • Alexander M (1977) Introduction to soil microbiology, 2nd edn. Wiley, New York, 467 pp

  • Bacilio-Jimenez M, Aguilar-Flores S, Ventura-Zapata E, Perez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277. doi:10.1023/A:1022888900465

    Article  CAS  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. doi:10.1016/S0378-1097(03)00894-2

    Article  CAS  Google Scholar 

  • Bauer AW, Kirby M, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–497

    CAS  Google Scholar 

  • Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538

    CAS  Google Scholar 

  • Cakmakci R, Donmez F, Aydin A, Sahin F (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38:1482–1487. doi:10.1016/j.soilbio.2005.09.019

    Article  CAS  Google Scholar 

  • Cao L, Qiu Z, You J, Tan H, Zhou S (2004) Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett Appl Microbiol 39:425–430. doi:10.1111/j.1472-765X.2004.01606.x

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Azcon R, Parlade J, Torres P, Roldan A (2005) Establishment of two ectomycorrhizal shrub species in a semiarid site after “in situ” amendment with sugar beet, rock phosphate and Aspergillus niger. Microb Ecol 49:73–82. doi:10.1007/s00248-003-0131-y

    Article  CAS  Google Scholar 

  • Chater KF (1993) Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47:685–713. doi:10.1146/annurev.mi.47.100193.003345

    Article  CAS  Google Scholar 

  • Conn VM, Walker AR, Franco CMM (2008) Endophytic actinobacteria induce defence pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218. doi:10.1094/MPMI-21-2-0208

    Article  CAS  Google Scholar 

  • Coombs JT, Franco CM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608. doi:10.1128/AEM.69.9.5603-5608.2003

    Article  CAS  Google Scholar 

  • Crawford DL, Kowalski M, Roberts MA, Merrell G, Deobald LA (2005) Discovery, development, and commercialization of a microbial antifungal biocontrol agent, Streptomyces lydicus WYEC108: history of a decade long endeavor. Soc Ind Microbiol News 55:88–95

    Google Scholar 

  • Cross JV, Polonenko DR (1996) An industry perspective on registration and commercialization of biocontrol agents in Canada. Can J Plant Pathol 18:446–454

    CAS  Google Scholar 

  • De Araujo JM, da Silva AC, Azevedo JL (2000) Isolation of endophytic actinomycetes from roots and leaves of maize (Zea mays L.). Braz Arch Biol Technol 434:447–451

    Google Scholar 

  • De Giudici P (1985) Contribution à l’étude de la solubilisation microbienne d’un phosphate naturel en modèle rhizosphérique. PhD thesis. Institut National Polytechnique de Lorraine France, 125 pp

  • Duponnois R, Colombet A, Hien V, Thioulouse J (2005) The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea. Soil Biol Biochem 37:1460–1468. doi:10.1016/j.soilbio.2004.09.016

    Article  CAS  Google Scholar 

  • Errakhi R, Bouteau F, Lebrihi A, Barakate M (2007) Evidences of biological control capacities of Streptomyces spp. against Sclerotium rolfsii responsible for damping-off disease in sugar beet (Beta vulgaris L.). World J Microbiol Biotechnol 23:1503–1509. doi:10.1007/s11274-007-9394-7

    Article  CAS  Google Scholar 

  • Fabre B, Armau E, Etienne G, Legendre F, Tiraby G (1988) A simple screening method for insecticidal substances from actinomycetes. J Antibiot (Tokyo) 41:212–219

    CAS  Google Scholar 

  • Firakova S, Sturdikova M, Muckova M (2007) Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia (Bratisl) 62:251–257. doi:10.2478/s11756-007-0044-1

    Article  CAS  Google Scholar 

  • Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–375. doi:10.1111/j.1469-8137.2005.01436.x

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216. doi:10.1146/annurev.mi.37.100183.001201

    Article  CAS  Google Scholar 

  • Graham JH, Lkonard RT, Menge JA (1981) Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular arbuscular mycorrhiza formation. Plant Physiol 68:548–552

    Article  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. doi:10.1023/A:1020663916259

    Article  CAS  Google Scholar 

  • Hamdali H, Bouizgarne B, Hafidi M, Lebrihi A, Virolle MJ, Ouhdouch Y (2008) Screening for rock phosphate-solubilizing Actinomycetes from Moroccan phosphate mines. Appl Soil Ecol 38:12–19. doi:10.1016/j.apsoil.2007.08.007

    Article  Google Scholar 

  • Hameeda B, Reddy HK, Rupela OP, Kumar GN, Reddy G (2006a) Effect of carbon substrates on rock phosphate solubilization by bacteria from composts and macrofauna. Curr Microbiol 53:298–302. doi:10.1007/s00284-006-0004-y

    Article  CAS  Google Scholar 

  • Hameeda B, Rupela OP, Reddy G, Satyavani K (2006b) Application of plant growth-promoting bacteria associated with composts and macrofauna for growth promotion of Pearl millet (Pennisetum glaucum L.). Biol Fertil Soils 43:221–227. doi:10.1007/s00374-006-0098-1

    Article  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constrains: a review. Plant Soil 248:43–59. doi:10.1023/A:1022371130939

    Article  CAS  Google Scholar 

  • Hsu SC, Lockwood JL (1975) Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29:422–426

    CAS  Google Scholar 

  • Ikeda T (2003) Pharmacological effects of ivermectin, an antiparasitic agent for intestinal strongyloidiasis: its mode of action and clinical efficacy. Nippon Yakurigaku Zasshi 122:527–538. doi:10.1254/fpj.122.527

    CAS  Google Scholar 

  • Indiragandhi P, Anandham R, Madhaiyan M, Sa TM (2008) Characterization of plant growth promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Putellidae). Curr Microbiol. doi:10.1007/s00284-007-9086-4

  • Jain PK, Jain PC (2007) Isolation, characterization and antifungal activity of Streptomyces sampsonii GS 1322. Indian J Exp Biol 45:203–206

    CAS  Google Scholar 

  • Jones KL (1949) Fresh isolates of Actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141–145

    Google Scholar 

  • Khan MS, Zaidi A (2007) Synergistic effects of the inoculation with plant growth promoting rhizobacteria and an arbuscular mycorrhizal fungus on the performance of wheat. Turk J Agric For 31:355–362

    CAS  Google Scholar 

  • Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In: Proceedings of the 4th International Conference on Plant Pathogenic Bacteria, Angers, pp 879–882

  • Kucey RMN, Jenzen HH, Leggett ME (1989) Microbially mediated increases in plant available phosphorus. Adv Agron 42:199–228. doi:10.1016/S0065-2113(08)60525-8

    Article  CAS  Google Scholar 

  • Lehr NA, Schrey SD, Hampp R, Tarkka MT (2008) Root inoculation with a forest soil streptomycete leads to locally and systemically increased resistance against phytopathogens in Norway spruce. New Phytol. doi: 10.1111/j.1469-8137.2007.02322.x

  • Martinez-Noel GMA, Madrid EA, Bottini 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. doi:10.1016/S0981-9428(01)01298-0

    Article  CAS  Google Scholar 

  • Matthijs S, Tehrani KA, Laus G, Jackson RW, Cooper RM, Cornelis P (2007) Thioquinolobactin, a Pseudomonas siderophore with antifungal and anti-Pythium activity. Environ Microbiol 9:425–434. doi:10.1111/j.1462-2920.2006.01154.x

    Article  CAS  Google Scholar 

  • Mclaughlin BR, Russell PR, Carroll DJ (1988) Cogen plant includes 12-acre greenhouse, oyster farm. Power Eng 92:40–42

    Google Scholar 

  • Meunchang S, Panichsakpatana S, Weaver RW (2006) Tomato growth in soil amended with sugar mill by-products compost. Plant Soil 280:171–176. doi:10.1007/s11104-005-2949-1

    Article  CAS  Google Scholar 

  • Nasholm T, Huss-Danell K, Hogberg P (2001) Uptake of glycine by field grown wheat. New Phytol 150:59–63. doi:10.1046/j.1469-8137.2001.00072.x

    Article  CAS  Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeny DR (eds) Methods of Soil Analysis, Part 2. American Society of Agronomy, Madison, pp 403–430

    Google Scholar 

  • Pandey A, Trivedi P, Kumar B, Palni LMS (2006) Characterization of a phosphate-solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a sub-alpine location in the Indian central Himalaya. Curr Microbiol 53:102–107. doi:10.1007/s00284-006-4590-5

    Article  CAS  Google Scholar 

  • Prévost K, Couture G, Shipley B, Brzezinski R, Beaulieu C (2006) Effect of chitosan and a biocontrol streptomycete on field and potato tuber bacterial communities. Biocontrol 51:533–546. doi:10.1007/s10526-005-4240-z

    Article  CAS  Google Scholar 

  • Reddy MS, Kumar S, Babita K, Reddy MS (2002) Biosolubilization of poorly soluble rock phosphates by Aspergillus tubingensis and Aspergillus niger. Biores Technol 84:187–189

    Article  CAS  Google Scholar 

  • Rodriguez H, Fraga R (1999) Phosphate-solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. doi:10.1016/S0734-9750(99)00014-2

    Article  CAS  Google Scholar 

  • Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216. doi:10.1111/j.1469-8137.2005.01518.x

    Article  CAS  Google Scholar 

  • Shigaki F, Sharpley AN, Prochnow LI (2006) Animal-based agriculture, phosphorus and management and water quality in Brazil: options for the future. Sci Agric 63:194–209

    Article  CAS  Google Scholar 

  • Taechowisan T, Peberdy JF, Lumyong S (2004) PCR cloning and heterologous expression of chitinase gene of endophytic Streptomyces aureofaciens CMUAc130. J Gen Appl Microbiol 50:177–182. doi:10.2323/jgam.50.177

    Article  CAS  Google Scholar 

  • Tahvonen RT, Avikainen H (1987) The biological control of seed-borne Alternaria brassicicola of cruciferous plants with a powdery preparation of Streptomyces sp. J Agric Sci Finl 59:199–208

    Google Scholar 

  • Te-Hsiu M (1999) The international program on plant bioassays and the report of the follow-up study after the hands-on workshop in China. Mutat Res 426:103–106

    Google Scholar 

  • Thirup L, Johnsen K, Winding A (2001) Succession of indigenous Pseudomonas spp. and actinomycetes on barley roots affected by the antagonistic strain Pseudomonas fluorescens DR54 and the fungicide imazalil. Appl Environ Microbiol 67:1147–1153. doi:10.1128/AEM.67.3.1147-1153.2001

    Article  CAS  Google Scholar 

  • Thomas-Bauzon D, Weinhard P, Villecourt P, Balandreau J (1982) The spermosphere model-its use in growing, counting and isolationg N2-fixing bacteria from the rhizosphere of rice. Can J Microbiol 28:922–928

    Article  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 (P-32) and nutrient cycling. Appl Environ Microbiol 63:4408–4412

    CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un systéme radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionelle. In: Mycorrhizae: Physiology and genetics-Les mycorhizes: physiologie et génétique. Proceedings of the 1st ESM/1er SEM, Dijon, 1–5 July 1985, INRA, Paris, pp 217–221

  • Tuomi T, Heino M, Rosenqvist H, Nordström K, Laakso S (2001) Fiber fractions from processing of barley in production and conservation of a biologic control agent. Appl Biochem Biotechnol 94:135–145. doi:10.1385/ABAB:94:2:135

    Article  CAS  Google Scholar 

  • Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144. doi:10.1007/s00253-006-0380-z

    Article  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. doi:10.1023/A:1026037216893

    Article  CAS  Google Scholar 

  • Vivas A, Barea JM, Biro B, Azcon R (2006) Effectiveness of autochthonous bacterium and mycorrhizal fungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminated soil. J Appl Microbiol 100:587–598. doi:10.1111/j.1365-2672.2005.02804.x

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) Chromium reduction, plant growth-promoting potentials and metal solubilization by Bacillus sp. isolated from alluvial soil. Curr Microbiol 54:237–243. doi:10.1007/s00284-006-0451-5

    Article  CAS  Google Scholar 

  • Welch SA, Taunton AE, Banfield JF (2002) Effect of microorganisms and microbial metabolites on apatite dissolution. Geomicrobiol J 19:343–367. doi:10.1080/01490450290098414

    Article  CAS  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    CAS  Google Scholar 

  • Whitelaw MA (1999) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–144. doi:10.1016/S0065-2113(08)60948-7

    Article  Google Scholar 

  • Xiao K, Samac DA, Kinkel LL (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol Control 23:285–295. doi:10.1006/bcon.2001.1015

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by a Franco-Moroccan cooperation (CMIFM Volubilis PAI No MA/04/109F) financed by the Foreign Affairs Ministries of France and Morocco as well as by the French CNRS, the University Paris Sud 11 (Orsay, France) and the University Cadi Ayyad (Marrakech, Morocco). I thank M.E.S.M. for the attribution of the bourse 03/032.

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Correspondence to Yedir Ouhdouch.

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Hamdali, H., Hafidi, M., Virolle, M.J. et al. Rock phosphate-solubilizing Actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24, 2565–2575 (2008). https://doi.org/10.1007/s11274-008-9817-0

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