Skip to main content

Advertisement

SpringerLink
Log in

Effects of microbial bioeffectors and P amendements on P forms in a maize cropped soil as evaluated by 31P–NMR spectroscopy

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Identification of organic P species is important to understand their origin, turnover in soils and their effects on soil fertility. Attention has been recently devoted to microbial inocula, referred to as Bioeffectors, that are capable to increase P bioavailability and plant uptake. Nevertheless, little is known on the effect of Bioeffectors on soil P forms and their dynamics in agricultural soils upon different P fertilization.

Methods

We investigated the effects of the application of different commercial inocula strains (Trichoderma harzianum T 22, Pseudomonas sp., and Bacillus amyloliquefaciens) alone or in combination with different P fertilizers (triple superphosphate, rock phosphate, and both composted cow- and horse-manure) on soil organic P forms. P forms were characterized by liquid-state 31P–NMR spectroscopy, while plant P uptake from P-treated soil was followed in a greenhouse pot experiment under maize cultivation.

Results

NMR spectra showed that the type of P fertilizer and bioeffectors inoculation, affected the abundance and the composition of organic P forms. The specific capacity of all bioeffectors, and especially Pseudomonas, was related to an increased content of diesters P forms. Pseudomonas, and, to a lesser extent, B. amyloliquefaciens showed the largest increase in combination with organic P amendments, which also provided the largest plant P uptake. This suggests a key role of Diester-P forms in determining P availability in agroecosystems.

Conclusions

Microbial inoculation plays an important role in the dynamics of soil P, inducing a rapid P cycling that prevents P fixation and losses from soils, thus enhancing the P fertilizer use efficiency in agricultural soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240

    Article  CAS  Google Scholar 

  • Ahlgren L, Djodjic F, Börjesson G, Mattsson L (2013) Identification and quantification of organic phosphorus forms in soils from fertility experiments. Soil Use Manag 29:24–35

    Article  Google Scholar 

  • Antoun H (2012) Beneficial microorganisms for the sustainable use of phosphates in agriculture. Procedia Engineering 46:62–67

    Article  CAS  Google Scholar 

  • Ayaga G, Todd A, Brookes PC (2006) Enhanced biological cycling of phosphorus increases its availability to crops in low-input sub-Saharan farming systems. Soil Biol Biochem 38:81–90

    Article  CAS  Google Scholar 

  • Brady NC, Weil RR (2008) The nature and properties of soils (fourteenth ed.), Prentice Hall, Upper Saddle River, NJ, USA

    Google Scholar 

  • Bünemann EK, Marschner P, McNeill AM, McLaughlin MJ (2007) Measuring rates of gross and net mineralisation of organic phosphorus in soils. Soil Biol Biochem 39:900–913

    Article  CAS  Google Scholar 

  • Bünemann EK, Marschner P, Smernik RJ, Conyers M, McNeill AM (2008) Soil organic phosphorus and microbial community composition as affected by 26 years of different management strategies. Biol Fertil Soils 44:717–726

    Article  Google Scholar 

  • Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95

    Article  CAS  Google Scholar 

  • Cade-Menun BJ (2005) Characterizing phosphorus in environmental and agricultural samples by 31P nuclear magneatic resonance spectroscopy. Talanta 66:359–371

    Article  PubMed  CAS  Google Scholar 

  • Cade-Menun BJ, Lavkulich LM (1997) A comparison of methods to determine total, organic, and available phosphorus in forest soils. Commun Soil Sci Plant Anal 28:651–663

    Article  CAS  Google Scholar 

  • Cade-Menun BJ, Liu CW (2013) Solution phosphorus-31 nuclear magnetic resonance spectroscopy of soils from 2005 to 2013: a review of sample preparation and experimental parameters. Soil Sci Soc Am J 78:19–37

    Article  CAS  Google Scholar 

  • Celi L, Lamacchia S, Marsan FA, Barberis E (1999) Interaction of inositol hexaphosphate on clays: adsorption and charging phenomena. Soil Sci 164:574–585

    Article  CAS  Google Scholar 

  • Cheesman AW, Turner BL, Inglett PW, Reddy KR (2010) Phosphorus transformations during decomposition of wetland Macrophytes. Environ Sci Technol 44:9265–9271

    Article  PubMed  CAS  Google Scholar 

  • Colvan S, Syers J, O'Donnell A (2001) Effect of long-term fertiliser use on acid and alkaline phosphomonoesterase and phosphodiesterase activities in managed grassland. Biol Fertil Soils 34:258–263

    CAS  Google Scholar 

  • Condron LM, Newman S (2011) Revisiting the fundamentals of phosphorus fractionation of sediments and soils. J Soils Sediments 11:830–840

    Article  CAS  Google Scholar 

  • Condron LM, Frossard E, Tiessen H, Newmans RH, Stewart JWB (1990) Chemical nature of organic phosphorus in cultivated and uncultivated soils under different environmental conditions. Eur J Soil Sci 41:41–50

    Article  CAS  Google Scholar 

  • Condron LM, Turner BL, Cade-Menun BJ (2005). Chemistry and dynamics of soil organic phosphorus. In: JT Sims and AN Sharpley (eds) Phosphorus: agriculture and the environment. Agron Monogr 46. ASA, CSSA, and SSSA, Madison, WI pp 87–121

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Cosgrove DJ (1967) Metabolism of organic phosphates in soil. In: McLaren AD, Peterson H (eds) Soil biochemistry. Marcel Dekker, New York, USA, pp 216–228

    Google Scholar 

  • Cozzolino V, Di Meo V, Piccolo A (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochem Explor 129:40–44

    Article  CAS  Google Scholar 

  • Cozzolino V, Di Meo V, Monda H, Spaccini R, Piccolo A (2016) The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biol Fertil Soils 52:15–29

    Article  CAS  Google Scholar 

  • Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214

    Article  CAS  Google Scholar 

  • Ding SM, Xu D, Li B, Fan CX, Zhang CS (2010) Improvement of 31P NMR spectral resolution by 8-Hydroxyquinoline precipitation of paramagnetic Fe and Mn in environmental samples. Environ Sci Technol 44:2555–2561

    Article  PubMed  CAS  Google Scholar 

  • Fröhlich A, Buddrus-Schiemann K, Durner J, Hartmann A, von Rad U (2012) Response of barley to root colonization by Pseudomonas sp. DSMZ 13134 under laboratory, greenhouse, and field conditions. J Plant Interact 7:1–9

    Article  Google Scholar 

  • Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23

    Article  CAS  Google Scholar 

  • Gichangi EM, Mnkeni PN, Brookes PC (2009) Effects of goat manure and inorganic phosphate addition on soil inorganic and microbial biomass phosphorus fractions under laboratory incubation conditions. Soil Sci Plant Nutr 55:764–771

    Article  CAS  Google Scholar 

  • Giles CD, Hsu PC, Richardson AE, Hurst MR, Hill JE (2014) Plant assimilation of phosphorus from an insoluble organic form is improved by addition of an organic anion producing Pseudomonas sp. Soil Biol Biochem 68:263–269

    Article  CAS  Google Scholar 

  • Greaves MP, Wilson MJ (1970) The degradation of nucleic acids and montmorillonite-nucleic acid complexes by soil microorganisms. Soil Biol Biochem 2:257–268

    Article  CAS  Google Scholar 

  • Guggenberger G, Christensen BT, Rubaek G, Zech W (1996) Land-use and fertilization effects on P forms in two European soils: resin extraction and 31P-NMR analysis. Eur J Soil Sci 47:605–614

    Article  CAS  Google Scholar 

  • Harman GE, Björkman 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. Taylor and Francis, London, pp 229–265

    Google Scholar 

  • Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976

    Article  CAS  Google Scholar 

  • Herrera-Estrella L, López-Arredondo D (2016) Phosphorus: the underrated element for feeding the world. Trends Plant Sci 21:461–463

    Article  PubMed  CAS  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Khan AA, Jilani G, Akhtar MS, Naqvi SSM, Rasheed M (2009) Phosphorus solubilizing bacteria: occurrence, mechanism and their role in crop production. J Agric Biol Sci 1:48–58

    Google Scholar 

  • Kpomblekou-a K, Tabatabai MA (1994) Effect of organic acids on release of phosphorus from phosphate rocks1. Soil Sci 158:442–453

    Article  CAS  Google Scholar 

  • Li M, Mazzei P, Cozzolino V, Monda H, Hu Z, Piccolo A (2015a) Optimized procedure for the determination of P species in soil by liquid-state 31P-NMR spectroscopy. Chem Biol Technol Agric 2:7

    Article  CAS  Google Scholar 

  • Li RX, Cai F, Pang G, Shen QR, Li R, Chen W (2015b) Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One 10:e0130081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lidbury ID, Murphy AR, Fraser TD, Bending GD, Jones AM, Moore JD, Goodall A, Tibbett M, Hammond JP, Scanlan DJ, Wellington EM (2017) Identification of extracellular glycerophosphodiesterases in Pseudomonas and their role in soil organic phosphorus remineralisation. Sci Rep 7:2179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Magid J, Tiessen H, Condron LM (1996) Dynamics of organic phosphorus in soils under natural and agricultural ecosystems. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, pp 429–466

    Chapter  Google Scholar 

  • Makarov MI, Haumaier L, Zech W (2002) Nature of soil organic phosphorus: an assessment of peak assignments in the diester region of 31P NMR spectra. Soil Biol Biochem 34(10):1467–1477

  • Makarov MI, Haumaier L, Zech W, Marfenina OE, Lysak LV (2005) Can 31P NMR spectroscopy be used to indicate the origins of soil organic phosphates? Soil Biol Biochem 37:15–25

    Article  CAS  Google Scholar 

  • Malik MA, Marschner P, Khan KS (2012) Addition of organic and inorganic P sources to soil–effects on P pools and microorganisms. Soil Biol Biochem 49:106–113

    Article  CAS  Google Scholar 

  • Mazzei P, Piccolo A (2012) Quantitative evaluation of non-covalent interactions between glyphosate and dissolved humic substances by NMR spectroscopy. Environ Sci Technol 46:5939–5946

    Article  PubMed  CAS  Google Scholar 

  • McDowell RW, Cade-Menun BJ, Stewart I (2007) Organic phosphorus speciation and pedogenesis: analysis by solution 31P nuclear magnetic resonance spectroscopy. Eur J Soil Sci 58:1348–1357

    Article  CAS  Google Scholar 

  • McLaren TI, Smernik RJ, Guppy CN, Bell MJ, Tighe MK (2014) The organic P composition of Vertisols as determined by P NMR spectroscopy. Soil Sci Soc Am J 78:1893–1902

    Article  CAS  Google Scholar 

  • McLaren TI, Smernik RJ, McLaughlin MJ, McBeath TM|, Kirby JK, Simpson RJ, Guppy CN, Doolette AL, Richardson AE (2015) Complex forms of soil organic phosphorus–a major component of soil phosphorus. Environ Sci Technol 49:13238–13245

    Article  PubMed  CAS  Google Scholar 

  • Menezes-Blackburn D, Inostroza NG, Gianfreda L, Greiner R, Mora ML, Jorquera MA (2016) Phytase-producing bacillus sp. inoculation increases phosphorus availability in cattle manure. J Soil Sci Plant Nutr 16:200–210

    CAS  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Murphy PNC, Bell A, Turner BL (2009) Phosphorus speciation in temperate basaltic grassland soils by solution 31P NMR spectroscopy. Eur J Soil Sci 60:638–651

    Article  CAS  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann EK et al (eds) Phosphorus in action. Springer-Verlag, Berlin Heidelberg, pp 215–243

    Chapter  Google Scholar 

  • Oberson A, Friesen DK, Tiessen H, Morel C, Stahel W (1999) Phosphorus status and cycling in native savanna and improved pastures on an acid low-P Colombian Oxisol. Nutr Cycl Agroecosyst 55:77–88

    Article  Google Scholar 

  • Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210

    Article  CAS  Google Scholar 

  • Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675

    Article  CAS  Google Scholar 

  • Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745

    Article  PubMed  PubMed Central  Google Scholar 

  • Paraskova JV, Sjoverg PJR, Rydin E (2014) Turnover of DNA-P and phospholipid-P in lake sediments. Biogeochemistry 119:361–370

    Article  CAS  Google Scholar 

  • Piccolo A, Huluka G (1985) Phosphorus status of some Ethiopian soils. Trop Agric 63:137–142

    Google Scholar 

  • Pierzynski GM, McDowell RW, Sims JT (2005) Chemistry, cycling and potential movement of inorganic phosphorus in soils. In: Sims JT, Sharpley AN (eds) Phosphorus: Agriculture and the environment. Agron. Monogr. 46. ASA, CSSA, and SSSA, Madison, WI, pp 53–86

    Google Scholar 

  • Qiao JQ, Wu HJ, Huo R, Gao XW, Borriss R (2014) Stimulation of plant growth and biocontrol by Bacillus amyloliquefaciens subsp. plantarum FZB42 engineered for improved action. Chem Biol Technol Agric 1:12

  • Ragot SA, Huguenin-Elie O, Kertesz MA, Frossard E, Bünemann EK (2016) Total and active microbial communities and phoD as affected by phosphate depletion and pH in soil. Plant Soil 408:1–16

    Article  CAS  Google Scholar 

  • Richardon H (2010) Transformation of phosphorus in soil. In: Hassan GD soil microbiology and biochemistry. New India Publishing, UK, pp 243–253

  • Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant Cell Environ 23:397–405

  • Richardson AE, Hadobas PA, Hayes JE, O'Hara CP, Simpson RJ (2001) Utilization of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil microorganisms. Plant Soil 229:47–56

    Article  CAS  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    Article  CAS  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 

  • Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:1521

    Article  CAS  Google Scholar 

  • Saunders WMH, Williams EG (1955) Observations on the determination of total organic phosphorus in soils. J Soil Sci 6:254–267

    Article  CAS  Google Scholar 

  • Schneider KD, Voroney RP, Lynch DH, Oberson A, Frossard E, Bünemann EK (2017) Microbially-mediated P fluxes in calcareous soils as a function of water-extractable phosphate. Soil Biol Biochem 106:51–60

    Article  CAS  Google Scholar 

  • Shafqat MN, Pierzynski GM, Xia K (2009) Phosphorus source effects on soil organic phosphorus: a 31P NMR. Commun Soil Sci Plan 40:1722–1746

    Article  CAS  Google Scholar 

  • Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem 61:69–75

    Article  CAS  Google Scholar 

  • Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochemistry 4:41–60

    Article  CAS  Google Scholar 

  • Sumann M, Amelung W, Haumaier L, Zech W (1998) Climatic effects on soil organic phosphorus in the north American Great Plains identified by phosphorus-31 nuclear magnetic resonance. Soil Sci Soc Am J 62:1580–1586

    Article  CAS  Google Scholar 

  • Tarafdar JC, Jungk 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 

  • Tate KR (1984) The biological transformation of P in soil. In: Tinsley J and Darbyshire JF (eds) Biological processes and soil fertility. Springer, Netherlands, pp 245–256

  • Thonar C, Lekfeldt JDS, Cozzolino V, Kundel D, Kulhánek M, Mosimann C et al (2017) Potential of three microbial bio-effectors to promote maize growth and nutrient acquisition from alternative phosphorous fertilizers in contrasting soils. Chem Biol Technol Agr 4:7

    Article  CAS  Google Scholar 

  • Torres-Dorante LO, Claassen N, Steingrobe B, Olfs H-W (2005) Hydrolysis rates of inorganic polyphosphates in aqueous solution as well as in soils and effects on P availability. J Plant Nutr Sci 168:352–358

    Article  CAS  Google Scholar 

  • Turner BL (2008) Soil organic phosphorus in tropical forest: an assessment of the NaOH-EDTA extraction procedure for quantitative analysis by solution 31P NMR spectroscopy. Eur J Soil Sci 59:453–466

    Article  CAS  Google Scholar 

  • Turner BL, Engelbrecht BMJ (2011) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103:297–315

    Article  CAS  Google Scholar 

  • Turner BL, Haygarth PM (2005) Phosphatase activity in temperate pasture soils: potential regulation of labile organic phosphorus turnover by phosphodiesterase activity. Sci Total Environ 344:27–36

    Article  PubMed  CAS  Google Scholar 

  • Turner BL, Newman S (2005) Phosphorus cycling in wetland soils: the importance of phosphate diesters. J Environ Qual 34:1921–1929

    Article  PubMed  CAS  Google Scholar 

  • Turner BL, Papházy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philos trans R Soc London Biol 357:449–469

    Article  CAS  Google Scholar 

  • Turner BL, Cade-Menun BJ, Westermann DT (2003a) Organic phosphorus composition and potential bioavailability in semi-arid arable soils of the western United States. Soil Sci Soc Am J 67:1168–1179

    Article  CAS  Google Scholar 

  • Turner BL, Mahieu N, Condron LM (2003b) The phosphorus composition of temperate pasture soils determined by NaOH–EDTA extraction and solution 31 P NMR spectroscopy. Org Geochem 34:1199–1210

    Article  CAS  Google Scholar 

  • Turrión MB, Gallardo JF, Haumaier L, González MI, Zech W (2001) 31P-NMR characterization of phosphorus fractions in natural and fertilized forest soils. Ann For Sci 58:89–98

    Article  Google Scholar 

  • Vazquez P, Holguin G, Puente ME, Lopez-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    Article  CAS  Google Scholar 

  • Vincent AG, Turner BL, Tanner EVJ (2010) Soil organic phosphorus dynamics following perturbation of soil cycling in a tropical moist forest. Eur J Soil Sci 61:48–57

    Article  CAS  Google Scholar 

  • Vincent AG, Vestergren J, Gröbner G, Persson P, Schleucher J, Giesler R (2013) Soil organic phosphates transformations in a boreal forest chronosequence. Plant Soil 367:149–162

    Article  CAS  Google Scholar 

  • Walker TW, Adams AFR (1958) Studies on soil organic matter: I. Influence of phosphorus content of parent materials on accumulations of carbon, nitrogen, sulfur, and organic phosphorus in grassland soils. Soil Sci 85:307–318

    Article  CAS  Google Scholar 

  • White AK, Metcalf WW (2004) The htx and ptx operons of pseudomonas stutzeri WM88 are new members of the pho regulon. J Bacteriol 186:5876–5882

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Withers PJA, Haygarth PM (2007) Agriculture, phosphorus and eutrophication: a European perspective. Soil Use Manag 23:1–4

    Article  Google Scholar 

  • Xu D, Ding SM, Li B, Jia F, He X, Zhang CS (2012) Characterization and optimization of the preparation procedure for solution P-31 NMR analysis of organic phosphorus in sediments. J Soils Sediments 12:909–920

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the European’s Seventh Framework Programme (FP/2007-2013) under Grant Agreement no. 312117. The first author was sponsored by the National Natural Science Fund Projects of China (No. U1133604) and China Scholarship Council (CSC). We thank three anonymous reviewers for their constructive suggestions in helping to improve the manuscript.

Author information

Authors and Affiliations

  1. College of Resources and Environment, Sino-Danish College, University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Meng Li & Zhengyi Hu

  2. Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy

    Vincenza Cozzolino

  3. Interdepartmental Research Centre CERMANU, University of Naples Federico II, Portici, Italy

    Pierluigi Mazzei, Marios Drosos, Hiarhi Monda & Alessandro Piccolo

Authors
  1. Meng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vincenza Cozzolino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierluigi Mazzei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marios Drosos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiarhi Monda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhengyi Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alessandro Piccolo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Vincenza Cozzolino or Alessandro Piccolo.

Additional information

Responsible Editor: Daniel Menezes-Blackburn.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, M., Cozzolino, V., Mazzei, P. et al. Effects of microbial bioeffectors and P amendements on P forms in a maize cropped soil as evaluated by 31P–NMR spectroscopy. Plant Soil 427, 87–104 (2018). https://doi.org/10.1007/s11104-017-3405-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3405-8

Keywords

Search

Navigation