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Effect of a phosphate-solubilizing fungus and an arbuscular mycorrhizal fungus on leucaena seedlings in tropical soils with contrasting phosphate sorption capacity

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Abstract

Background and aims

A greenhouse experiment was conducted to determine the effects of a rock phosphate-solubilizing fungus (Mortierella sp.) and an arbuscular mycorrhizal fungus (Claroideoglomus claroideum (N. C. Schenck & G. S. Sm.) C. Walker & A. Schüßler comb. nov.) on enhancing plant phosphate (P) uptake and growth of Leucaena leucocephala (Lam.) in three tropical soils that exhibited contrasting soil P sorption capacities.

Methods

For this purpose, the three soils (Mollisol, Oxisol and Andisol) were amended with Huila rock phosphate (RP) at a P rate of 300 mg kg−1 and inoculated with neither, one, or both fungi.

Results

The results indicate that a three-way interaction occurred for all variables studied and that the effectiveness of the PSM in increasing plant P uptake and growth was limited by the soil P sorption. For instance, PSM inoculation was ineffective in the Andisol (very high P sorption capacity) even when the mycorrhizal association was present, while in the Oxisol (medium P sorption) the PSM was only effective when the plant was concomitantly inoculated with the AMF (dual inoculation). In contrast, both individual PSM inoculation and individual AMF inoculation were effective in promoting plant P uptake and growth in the Mollisol (low soil P sorption); however, the effect was even higher in the presence of both (dual inoculation).

Conclusions

Although the PSM effect was limited by soil P sorption, this limitation likely was overcome by the mycorrhizal association, which permitted a more efficient capture of the P released from RP dissolution.

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References

  • Anderson BH, Magdoff FR (2005) Autoclaving soil samples affects algal-available phosphorus. J Environ Qual 34:1958–1963. doi:10.2134/jeq2005.0024

    Article  CAS  PubMed  Google Scholar 

  • Asea PEA, Kucey RMN, Stewart JWB (1988) Inorganic phosphate solubilisation by 2 Penicillium species in solution culture and soil. Soil Biol Biochem 20:459–464. doi:10.1016/0038-0717(88)90058-2

    Article  CAS  Google Scholar 

  • Barber SA (1995) Soil Nutrient Bioavailability. A Mechanistic Approach. Wiley, New Yor

  • Barea JM, Toro M, Orozco M, Campos E, Azcon R (2002) The Application of isotopic (32P and 15N) dilution technique to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops. Nutr Cycl Agroecosyst 63:35–42. doi:10.1023/A:1020589732436

    Article  CAS  Google Scholar 

  • Bhatti TM, Yawar W (2010) Bacterial solubilization of phosphorus from phosphate rock containing sulfur-mud. Hydrometallurgy 103:54–59. doi:10.1016/j.hydromet.2010.02.019

    Article  CAS  Google Scholar 

  • Cabello M, Irrazabal G, Bucsinszky AM, Saparrat M, Schalamuk S (2005) Effect of an arbuscular mycorrhizal fungus, Glomus mosseae, and a rock-phosphate-solubilizing fungus, Penicillium thomii, on Mentha piperita growth in a soilless medium. J Basic Microbiol 45:182–289. doi:10.1002/jobm.200410409

    Article  PubMed  Google Scholar 

  • Carter DO, Yellowlees D, Tibbett M (2007) Autoclaving kills soil microbes yet soil enzymes remain active. Pedobiologia 51:295–299. doi:10.1016/j.pedobi.2007.05.002

    Article  CAS  Google Scholar 

  • Chien SH, Hammond LL (1978) A comparison of various laboratory methods for predicting the agronomic potential of phosphate rocks for direct application. Soil Sci Soc Am J 42:935–939. doi:10.2136/sssaj1978.03615995004200060022x

    Article  CAS  Google Scholar 

  • Delvasto P, Valverde A, Ballester A, Igual JM, Munoz JA, Gonzalez F, Blazquez ML, Garcia C (2006) Characterization of brushite as a recrystallization product formed during bacterial solubilization of hydroxyapatite in batch cultures. Soil Biol Biochem 38:2645–2654. doi:10.1016/j.soilbio.2006.03.020

    Article  CAS  Google Scholar 

  • Duponnois R, Kisa M, Plenchette C (2006) Phosphate-solubilizing potential of the nematophagous fungus Arthrobotrys oligospora. J Plant Nutr Soil Sci 169:280–282. doi:10.1002/jpln.200520551

    Article  CAS  Google Scholar 

  • Fox RL, Kamprath E (1970) Phosphate sorption isotherms for evaluating phosphorus requirements of soils. Soil Sci Soc Am Proc 34:902–907. doi:10.2136/sssaj1970.03615995003400060025x

    Article  CAS  Google Scholar 

  • Gaur A, Rana J, Jalali B, Chand H (1990) Role of VA mycorrhizae, phosphate solubilizing bacteria and their interactions on growth and uptake of nutrients by wheat crops. In: Trends in Mycorrhizal Research. Proceedings of the National Conference on Mycorrhizae, Hisar, India, pp 105–106

  • Giovanneti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection of roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  • Gururaj R, Mallikarjunaiah R (1995) Interactions among Azotobacter chroococcum, Penicillium glaucum and Glomus fasciculatum and their effect on the growth and yield of sunflower. Helia 18:73–84

    Google Scholar 

  • Habte M (2006) The roles of arbuscular mycorrhizas in plant and soil health. In: Uphoff N et al (eds) Biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 129–147

    Chapter  Google Scholar 

  • Habte M, Manjunath A (1987) Soil solution phosphorus status and mycorrhizal dependency in Leucaena leucocephala. Appl Environ Microbiol 53:797–801

    PubMed Central  CAS  PubMed  Google Scholar 

  • Habte M, Osorio NW (2001) Arbuscular mycorrhizas: producing and applying arbuscular mycorrhizal inoculum. University of Hawaii, Honolulu

    Google Scholar 

  • Habte M, Fox RL, Huang RS (1987) Determining vesicular-arbuscular mycorrhizal effectiveness by monitoring P status of subleaflets of an indicator plant. Commun Soil Sci Plant Anal 18:1403–1420. doi:10.1080/00103628709367907

    Article  CAS  Google Scholar 

  • Hallman J, Berg G, Schulz B (2006) Isolation procedures for endophytic microorganisms. In: Shulz B, Boyle C, Sieber T (eds) Microbial root endophytes. Springer, Berlin, pp 299–319

    Chapter  Google Scholar 

  • Hamdali H, Smirnov A, Esnault C, Ouhdouch Y, Virolle MJ (2010) Physiological studies and comparative analysis of rock phosphate solubilization abilities of actinomycetales originating from Moroccan phosphate mines and of Streptomyces lividans. Appl Soil Ecol 44:24–31. doi:10.1016/j.apsoil.2009.09.001

    Article  Google Scholar 

  • He ZL, Bian W, Zhu J (2002) Screening and identification of microorganisms capable of utilizing phosphate adsorbed by goethite. Commun Soil Sci Plant Anal 33:647–663. doi:10.1081/CSS-120003057

    Article  CAS  Google Scholar 

  • Hue NV, Fox RL (2010) Predicting plant phosphorus requirements for Hawaii soils using a combination of phosphorus sorption isotherms and chemical extraction methods. Commun Soil Sci Plant Anal 41:133–143. doi:10.1080/00103620903426949

    Article  Google Scholar 

  • Juo ASR, Fox RL (1977) Phosphate sorption characteristics of some benchmark soils of West Africa. Soil Sci 124:370–376. doi:10.1097/00010694-197712000-00010

    Article  CAS  Google Scholar 

  • Kageyama SA, Mandyam KG, Jumpponen A (2008) Diversity, function and potential applications of the root-associated endophytes. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, ecophysiology, structure and systemetics. Springer, Berlin, pp 29–59

    Chapter  Google Scholar 

  • Kim KY, Jordan D, McDonald GA (1998) Effect of phosphate solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26:79–87. doi:10.1007/s003740050347

    Article  CAS  Google Scholar 

  • Kucey RMN (1988) Effect of Penicillium bilaii on the solubility and uptake of P and micronutrients from soil by wheat. Can J Soil Sci 68:261–270. doi:10.4141/cjss88-026

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Manjunath A, Habte M (1991) Root morphological characteristics of host species having distinct mycorrhizal dependency. Can J Bot 69:671–676. doi:10.1139/b91-089

    Article  Google Scholar 

  • Miyasaka SC, Habte M (2001) Plant mechanisms and mycorrhizal symbioses to increase phosphorus uptake efficiency. Commun Soil Sci Plant Anal 32:1101–1147. doi:10.1081/CSS-100104105

    Article  CAS  Google Scholar 

  • Msolla MM, Semoka JMR, Borggaard OK (2005) Hard Minjingu phosphate rock. An alternative P source for maize production on acid soils in Tanzania. Nutr Cycl Agroecosyst 72:299–308. doi:10.1007/s10705-005-6081-7

    Article  CAS  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–35. doi:10.1016/S0003-2670(00)88444-5

    Article  CAS  Google Scholar 

  • Muthkumar T, Udaiyan K, Rajeshkannan V (2001) Response of neem to indigenous arbuscular mycorrhizal fungi, phosphate solubilizing and asymbiotic nitrogen-fixing bacteria under tropical nursery conditions. Biol Fertil Soils 34:417–426. doi:10.1007/s00374-001-0425-5

    Google Scholar 

  • Narisawa K, Tokumasu S, Hashiba T (1998) Suppression of club root formation in chinese cabbage by the root endophytic fungus, Heteroconium chaetospira. Plant Pathol 47:206–210. doi:10.1046/j.1365-3059.1998.00225.x

    Article  Google Scholar 

  • Oberson A, Bunemann EK, Friesen DK, Rao IM, Smithson PC, Turner BL, Frossard E (2006) Improving phosphorus fertility in tropical soils through biological interventions. In: Uphoff N et al (eds) Biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 531–546

    Chapter  Google Scholar 

  • Ojo OD, Kintomo AA, Akinride EA, Akoroda MO (2007) Comparative effect of phosphorus sources for grain amaranth production. Commun Soil Sci Plant Anal 38:35–55. doi:10.1080/00103620601093611

    Article  CAS  Google Scholar 

  • Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP, Guimaraes CT, Schaffert RE, Sa NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787. doi:10.1016/j.soilbio.2008.01.012

    Article  CAS  Google Scholar 

  • Osorio NW (2008) Effectiveness of microbial solubilization of phosphate in enhancing plant phosphate uptake in tropical soils and assessment of the mechanisms of solubilization. Dissertation, University of Hawaii

  • Osorio NW, Habte M (2001) Synergistic influence of an arbuscular mycorrhizal fungus and P solubilizing fungus on growth and plant P uptake of Leucaena leucocephala in an Oxisol. Arid Land Res Manag 15:263–274. doi:10.1080/15324980152119810

    Article  CAS  Google Scholar 

  • Osorio NW, Habte M (2012) Phosphate desorption from the surface of soil mineral particles by a phosphate solubilizing fungus. Biol Fertil Soils 49:481–486. doi:10.1007/s00374-012-0763-5

    Article  Google Scholar 

  • Osorio NW, Habte M (2013) Synergistic effect of a phosphate solubilizing fungus and an arbuscular mycorrhizal fungus on leucaena seedlings in an oxisol fertilized with rock phosphate. Botany 91:274–281. doi:10.1139/cjb-2012-0226

    Article  CAS  Google Scholar 

  • Osorio NW, Habte M (2014) Soil phosphate desorption induced by a phosphate solubilizing fungus. Commun Soil Sci Plant Anal 45:451–460. doi:10.1080/00103624.2013.870190

    Article  CAS  Google Scholar 

  • Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martinez-Molina E, Velasquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorrhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33:103–110. doi:10.1016/S0038-0717(00)00120-6

    Article  CAS  Google Scholar 

  • Porter WM (1979) The most probable number method for enumerating propagules of vesicular arbuscular mycorrhizal fungi in soil. Austr J Soil Res 17:515–519

  • Pramanik P, Bhattacharyya S, Bhattacharyya P, Banik P (2009) Phosphorous solubilization from rock phosphate in presence of vermicompost in aqualfs. Geoderma 152:16–22. doi:10.1016/j.geoderma.2009.05.013

    Article  CAS  Google Scholar 

  • Randhawa P, Condron LM, Di HJ, Sinaj S, McLenaghen RD (2006) Phosphorus availability in soils amended with different phosphate fertilizers. Commun Soil Sci Plant Anal 37:25–39. doi:10.1080/00103620500403572

    Article  CAS  Google Scholar 

  • Razavi-darbar S, Lakzian A (2007) Evaluation of chemical and biological consequences of soil sterilization methods. Caspian J Environ Sci 5:87–91

    Google Scholar 

  • Schübler A, Walker C (2010) The Glomeromycota. A species list with new families and new genera. Edinburgh & Kew, UK: The Royal Botanic Garden; Munich, Germany: Botanische Staatssammlung Munich; Oregon, USA: Oregon State University. http://www.amf-phylogeny.com

  • Shrivastava M, Bhujbal BM, Souza SF (2007) Agronomic efficiency of Indian rock phosphate in acidic soils employing radiotracer A-value technique. Commun Soil Sci Plant Anal 38:461–471. doi:10.1080/00103620601174288

    Article  CAS  Google Scholar 

  • Sinegani AAS, Hosseinpur A (2010) Evaluation of effect of different sterilization methods on soil biomass phosphorus extracted with NaHCO3. Plant Soil Environ 56:156–162

    CAS  Google Scholar 

  • Smith FW (2002) The phosphate uptake mechanism. Plant Soil 245:105–114. doi:10.1023/A:1020660023284

    Article  CAS  Google Scholar 

  • Smith FW, Van Den Berg PJ, Gonzalez A, Andrew CS, Pieters WHJ (1992) Foliar symptoms of nutrient disorders in the tropical shrub legume Leucaena leucocephala. CSIRO, St. Lucia

    Google Scholar 

  • Sreenivasa M, Krishnaraj M (1992) Synergistic interaction between VA mycorrhizal fungi and a phosphate solubilizing bacterium in chili. Zentralbl Mikrobiol 147:126–130. doi:10.1016/S0232-4393(11)80373-2

    Article  Google Scholar 

  • Stamford NP, Santos PR, Santos CES, Freitas ADS, Dias SHL, Lira MA (2007) Agronomic effectiveness of biofertilizers with phosphate rock, sulphur and Acidithiobacillus for yam bean grown on a Brazilian tableland acidic soil. Bioresour Technol 98:1311–1318. doi:10.1016/j.biortech. 2006.04.037

    Article  CAS  PubMed  Google Scholar 

  • Toro M, Azcon R, Herrera R (1996) Effects on yield and nutrition of mycorrhizal and nodulated Pueraria phaseolides exerted by P-solubilizing rhizobacteria. Biol Fertil Soils 21:23–29. doi:10.1007/BF00335989

    Article  Google Scholar 

  • Toro M, Azcon R, Barea JM (1998) The use of isotopic dilution techniques to evaluate the interactive effects of rhizobium genotypes, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytol 138:265–273. doi:10.1046/j.1469-8137.1998.00108.x

    Article  CAS  Google Scholar 

  • Uchida R, Hue NV (2000) Soil acidity and liming. In Silva JA, Uchida R (eds) Plant nutrient management in Hawaiian soils, approaches for tropical and subtropical agriculture. University of Hawaii, Honolulu, pp 101–111

  • Vassileva M, Serrano M, Bravo V, Jurado E, Nikolaeva I, Martos V, Vassilev N (2010) Multifunctional properties of phosphate-solubilizing microorganisms grown on agroindustrial wastes in fermentation and soil conditions. Appl Microbiol Biotechnol 85:1287–1299. doi:10.1007/s00253-009-2366-0, PMID:19946684

    Article  CAS  PubMed  Google Scholar 

  • Vyas P, Rahi P, Chauhan A, Gulati A (2007) Phosphate solubilization potential and stress tolerance of Eupenicilium parvum from tea soil. Mycol Res 111:931–938. doi:10.1016/j.mycres.2007.06.003

    Article  CAS  PubMed  Google Scholar 

  • Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fertil Soils 40:36–43. doi:10.1007/s00374-004-0750-6

    Article  CAS  Google Scholar 

  • Whitelaw MA, Harden TJ, Bender GL (1997) Plant growth promotion of wheat inoculated with Penicillium radicum sp. nov. Aust J Soil Res 35:291–300. doi:10.1071/S96040

    Article  Google Scholar 

  • Young CC, Chen CL, Chao CC (1990) Effect of Rhizobium, vesicular arbuscular mycorrhiza, and phosphate solubilizing bacteria on yield and mineral phosphorus uptake of crops in subtropical-tropical. In: Proceedings of the 14th International Congress of Soil Science. Transactions, Vol. III. International Society of Soil Science, Kyoto, Japan, pp 55–60

  • Yusdar H, Anuar AR, Hanafi MM, Azifah H (2007) Analysis of phosphate rock dissolution determining factors using principal component analysis in some acid Indonesian soils. Commun Soil Sci Plant Anal 38:273–282. doi:10.1080/00103620601094239

    Article  CAS  Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M, Wani PA (2009) Recent advances in plant growth promotion by phosphate-solubilizing microbes. In: Khan MS (ed) Microbial strategies for crop improvement. Springer, Berlin, pp 23–50

    Chapter  Google Scholar 

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  1. Universidad Nacional de Colombia at Medellín, Calle 59A No. 63-20, 050034, Medellín, Colombia

    Nelson Walter Osorio

  2. University of Hawai’i, St. John 102, 3190 Maile Way, Honolulu, HI, 96822, USA

    Mitiku Habte

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  1. Nelson Walter Osorio
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Correspondence to Nelson Walter Osorio.

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Osorio, N.W., Habte, M. Effect of a phosphate-solubilizing fungus and an arbuscular mycorrhizal fungus on leucaena seedlings in tropical soils with contrasting phosphate sorption capacity. Plant Soil 389, 375–385 (2015). https://doi.org/10.1007/s11104-014-2357-5

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