Skip to main content

Advertisement

Log in

The adsorbent capacity of growing media does not constrain myo-inositol hexakiphosphate hydrolysis but its use as a phosphorus source by plants

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

Abstract

Aims

The hydrolysis of organic P in soils is a relevant aspect contributing to the supply P to plants, which is affected by adsorbent capacity and biological properties of soils. This work aimed at studying the contribution of phytate to plant nutrition as affected by Fe oxides and phosphohydrolases releasing microorganisms in the growing medium.

Methods

An experiment with cucumber and myo-inositol hexakiphosphate (myo-Ins6P) as P source was performed involving two factors: Fe oxide –ferrihydrite– rates (0, 100, 300 mg kg−1 of citrate–ascorbate extractable Fe), and microbial inoculation (Trichoderma asperellum T34, Bacillus subtilis QST713, and non-inoculated).

Results

P uptake decreased with increased Fe oxides in the growing media. Phytase activity and organic anions concentration increased with increased Fe oxides in the media. Most of the P supplied was recovered as inorganic P at the highest Fe oxide concentration. Inoculants did not improve P uptake by plants, despite B. subtilis promoted an enhanced hydrolytic activity at the highest Fe oxide concentration.

Conclusions

An increased adsorption capacity of the growing media restricts the use of myo-Ins6P as P source by plants. This was not the result of its stabilization through adsorption or a decreased hydrolytic activity, but of the adsorption of inorganic P on Fe oxides after hydrolysis.

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

Access this article

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

Similar content being viewed by others

References

  • Adams MA, Pate JS (1992) Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.). Plant Soil 145:107–113

    Google Scholar 

  • Balwani I, Chakravarty K, Gaur S (2017) Role of phytase producing microorganisms towards agricultural sustainability. Biocatal Agric Biotechnol 12:23–29

    Google Scholar 

  • Baziramakenga R, Simard RR, Leroux GD (1995) Determination of organic acids in soil extracts by ion chromatography. Soil Biol Biochem 27:349–356

    CAS  Google Scholar 

  • Bol R, Julich D, Brödlin D, Siemens J, Kaiser K, Dippold MA, Spielvogel S, ZillaT MD, von Blanckenburg F, Puhlmann H, Holzmann S, Weiler M, Amelung W, Lang F, Kuzyakov Y, Feger KH, Gottselig N, Klumpp E, Missong A, Winkelmann C, Uhlig D, Sohrt J, von Wilpert K, Wu B, Hagedorn F (2016) Dissolved and colloidal phosphorus fluxes in forest ecosystems – an almost blind spotin ecosystem research. J Plant Nutr Soil Sci 179:425–438

    CAS  Google Scholar 

  • Borrero C, Trillas I, Delgado A, Avilés M (2012) Effect of ammonium/nitrate ratio in nutrient solution on control of Fusarium wilt of tomato by Trichoderma asperellum T34. Pathology 61:132–139

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Celi L, De Luca G, Barberis E (2003) Effects of interaction of organic and inorganic P with ferrihydrite and kaolinite-iron oxide systems on iron release. Soil Sci 168:479–488

    CAS  Google Scholar 

  • Celi L, Prati M, Magnacca G, Santoro V, Martin M (2020) Role of crystalline iron oxides on stabilization of inositol phosphates in soil. Geoderma 374:114442. https://doi.org/10.1016/j.geoderma.2020.114442

    Article  CAS  Google Scholar 

  • Chung YR, Hoitink HAJ (1990) Interactions between thermophilic fungi and Trichoderma hamatum in suppression of Rhizoctonia damping off in a bark compost-amended container medium. Phytopathology 80:73–77

    Google Scholar 

  • de Santiago A, Delgado A (2007) Effects of humic substances on iron nutrition of lupin. Biol Fertil Soils 43:829–836

    Google Scholar 

  • de Santiago A, Quintero JM, Avilés M, Delgado A (2009) Effect of Trichoderma asperellum strain T34 on iron nutrition in white lupin. Soil Biol Biochem 41:2453–2459

    Google Scholar 

  • de Santiago A, Quintero JM, Avilés M, Delgado A (2011) Effect of Trichoderma asperellum strain T34 on iron copper manganese and zinc uptake by wheat grown on a calcareous medium. Plant Soil 342:97–104

    CAS  Google Scholar 

  • de Santiago A, García-López AM, Quintero JM, Avilés M, Delgado A (2013) Effect of Trichoderma asperellum strain T34 and glucose addition on iron nutrition in cucumber grown on calcareous soils. Soil Biol Biochem 57:598–605

    Google Scholar 

  • Delgado A, Scalenghe R (2008) Aspects of phosphorus transfer from soils in Europe. J Plant Nutr Soil Sci 171:552–575

    CAS  Google Scholar 

  • Faucon M-P, Houben D, Reynoird J-P, Mercadal-Dulaurent A-M, Armand R, Lambers H (2015) Advances and perspectives to improve the phosphorus availability in cropping systems for agroecological phosphorus management. Adv Agron 134:1–29

    Google Scholar 

  • Fu S, Sun J, Qian L, Li Z (2008) Bacillus phytases: present scenario and future perspectives. Appl Biochem Biotechnol 151:1–8

    CAS  PubMed  Google Scholar 

  • García-López AM, Delgado A (2016) Effect of Bacillus subtilis on phosphorus uptake by cucumber as affected by iron oxides and the solubility of the phosphorus source. Agric Food Sci 25:216–224

    Google Scholar 

  • García-López AM, Avilés M, Delgado A (2015) Plant uptake of phosphorus from sparingly available P-sources as affected by Trichoderma asperellum T34. J Food Sci 24:249–260

    Google Scholar 

  • García-López AM, Avilés M, Delgado A (2016) Effect of various microorganisms on phosphorus uptake from insoluble Ca-phosphates by cucumber plants. J Plant Nutr Soil Sci 179:454–465

    Google Scholar 

  • George TS, Gregory PJ, Wood M, Reed D, Buresh RJ (2004) Phosphatase activity and organic acids in the rhizosphere of potential agroforestry species and maize. Soil Biol Biochem 34:1487–1494

    Google Scholar 

  • George TS, Richardson AE, Simpson J (2005) Behaviour of plant-derived extracellular phytase upon addition to soil. Soil Biol Biochem 37:977–988

    CAS  Google Scholar 

  • George TS, Quiquampoix H, Simpson RJ, Richardson AE (2007) Interactions between phytases and soil constituents: implications for the hydrolysis of inositol phosphates. In: Turner BL et al (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, pp 221–241

    Google Scholar 

  • Giaveno C, Celi L, Richardson AE, Simpson RJ, Barberis E (2010) Interaction of phytases with minerals and availability of substrate affect the hydrolysis of inositol phosphates. Soil Biol Biochem 42:491–498

    CAS  Google Scholar 

  • Gichangi EM, Mnkeni PNS, 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

    CAS  Google Scholar 

  • Giles CD, Richardson AE, Druschel GK, Hill JE (2012) Organic anion–driven solubilization of precipitated and sorbed phytate improves hydrolysis by phytases and bioavailability to Nicotiana tabacum. Soil Sci 177:591–598

    CAS  Google Scholar 

  • Gimsing AL, Borggaard OK (2007) Phosphate and glyphosate adsorption by hematite and ferrihydrite and comparison with other variable-charge minerals. Clay Clay Miner 55:108–114. https://doi.org/10.1346/CCMN.2007.0550109

    Article  CAS  Google Scholar 

  • Hayes JE, Richardson AE, Simpson RJ (1999) Phytase and acid phosphatase activities in roots of temperate pasture grasses and legumes. Aust J Plant Physiol 26:801–809

    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

    CAS  Google Scholar 

  • Hocking PJ (2001) Organic acids exuded from roots in phosphorus uptake and aluminium tolerance of plants in acid soils. Adv Agron 74:63–97

    CAS  Google Scholar 

  • Jatuwong K, Suwannarach N, Kumla J, Penkhrue W, Kakumyan P, Lumyong S (2020) Bioprocess for production, characteristics, and biotechnological applications of fungal Phytases. Front Microbiol 11:188. https://doi.org/10.3389/fmicb.2020.00188

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones DL, Darah PR, Kochian LV (1996) Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180:57–66

    CAS  Google Scholar 

  • Khan KS, Joergensen RG (2009) Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresour Technol 100:303–309

    CAS  PubMed  Google Scholar 

  • Kleinman PJA, Sharpley AN, Withers PJA, Bergström L, Johnson LT, Doody DG (2015) Implementing agricultural phosphorus science and management to combat eutrophication. Ambio 44:297–310

    CAS  PubMed Central  Google Scholar 

  • Liu J, Bo X, Zhao Z, Guo L (2015) Highly exposed Pt nanoparticles supported on porous graphene for electrochemical detection of hydrogen peroxide in living cells. Biosens Bioelectron 74:71–77

    CAS  PubMed  Google Scholar 

  • Lung SC, Lim BL (2006) Assimilation of phytate-phosphorus by the extracellular phytase activity of tobacco (Nicotiana tabacum) is affected by the availability of soluble phytate. Plant Soil 279:187–199

    CAS  Google Scholar 

  • Macklon AES, Grayston SJ, Shand CA, Sim A, Sellars S, Ord BG (1997) Uptake and transport of phosphorus by Agrostis capillaris seedlings from rapidly hydrolysed organic sources extracted from 32 P-labelled bacterial cultures. Plant Soil 190:163–167

    CAS  Google Scholar 

  • Madrid L, Diaz-Barrientos E, Contreras MC (1991) Relationships between zinc and phosphate adsorption on montmorillonite and an iron oxyhydroxide. Aust J Soil Res 29:239–247

    CAS  Google Scholar 

  • Martin JK (1973) The influence of rhizosphere microflora on the availability of 32P-myoinositol hexaphosphate phosphorus to wheat. Soil Biol Biochem 5:473–483

    CAS  Google Scholar 

  • Martin M, Celi L, Barberis E (2004) Desorption and plant availability of myo-inositol hexaphosphate adsorbed on goethite. Soil Sci 169:115–124

    CAS  Google Scholar 

  • Menezes-Blackburn D, Jorquera MA, Greiner R, Gianfreda L, de la Luz MM (2013) Phytases and phytase-labile organic phosphorus in manures and soils. Crit Rev Environ Sci Technol 43:916–954

    CAS  Google Scholar 

  • Metson GS, MacDonald GK, Haberman D, Nesme T, Bennett EM (2016) Feeding the corn belt: opportunities for phosphorus recycling in US agriculture. Sci Total Environ 542:1117–1126

    CAS  PubMed  Google Scholar 

  • Mezeli MM, Menezes-Blackburn D, George TS, Giles CD, Neilson R, Haygarth PM (2017) Effect of citrate on Aspergillus Niger phytase adsorption and catalytic activity in soil. Geoderma 305:346–353

    CAS  Google Scholar 

  • Missong A, Bol R, Willbold S, Siemens J, Klumpp E (2016) Phosphorus forms in forest soil colloids as revealed by liquid-state 31P-NMR. J Plant Nutr Soil Sci 179:159–167

    CAS  Google Scholar 

  • Montilla I, Parra MA, Torrent J (2003) Zinc phytotoxicity to oilseed rape grown on zinc-loaded substrates consiting of Fe oxide-coated and calcite sand. Plant Soil 257:227–236

    CAS  Google Scholar 

  • Mullaney EJ, Ullah AHJ (2003) The term phytase comprises several different classes of enzymes. Biochem Biophys Res Commun 312:179–184

    CAS  PubMed  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

    CAS  Google Scholar 

  • Ognalaga M, Frossard E, Thomas F (1994) Glucose-1-phosphate and myo-inositol hexaphosphate adsorption mechanisms on goethite. Soil Sci Soc Am J 58:332–337

    CAS  Google Scholar 

  • Oh B, Choi W, Park S, Kim Y, Oh TK (2004) Biochemical properties and substrate specificities of alkaline and histidine acid phytases. Appl Microbiol Biotechnol 63:362–372. https://doi.org/10.1007/s00253-003-1345-0

    Article  CAS  PubMed  Google Scholar 

  • Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl Soil Ecol 86:41–54

    Google Scholar 

  • Patel DK, Murawala P, Archana G, Kumar GN (2011) Repression of mineral phosphate solubilizing phenotype in the presence of weak organic acids in plant growth promoting fluorescent pseudomonads. Bioresour Technol 102:3055–3061

    CAS  PubMed  Google Scholar 

  • Quiquampoix H (1987) A stepwise approach to the understanding of extracellular enzyme activity in soil I. Effect of electrostatic interactions on the conformation of a β-D-glucosidase adsorbed on different mineral surfaces. Biochimie 69:753–763

    CAS  PubMed  Google Scholar 

  • Radersma S, Grierson PF (2004) Phosphorus mobilization in agroforestry: organic anions, phosphatase activity and phosphorus fractions in the rhizosphere. Plant Soil 259:209–219

    CAS  Google Scholar 

  • Rahmatullah MA, Torrent J (2000) Phosphorus dynamics and uptake by wheat in a model calcite-ferrihydrite system. Soil Sci 165:803–812

    CAS  Google Scholar 

  • Recena R, Cade-Menun BJ, Delgado A (2018) Organic phosphorus forms in agricultural soils under Mediterranean climate. Soil Sci Soc Am J 82:783–795

    CAS  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Richardson AE, George TS, Hens M, Simpson RJ (2005) Utilization of soil organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI, Wallingford, pp 165–184

    Google Scholar 

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

    CAS  Google Scholar 

  • Rowe H, Withers PJA, Baas P, Chan NI, Doody D, Holiman J, Jacobs B, Li HG (2016) Integrating legacy soil phosphorus into sustainable nutrient management strategies for future food, bioenergy and water security. Nutr Cycl Agroecosyst 104:393–412

    CAS  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev J Plant Physiol Pathol Plant J Mol Biol 52:527–560

    CAS  Google Scholar 

  • Sánchez-Rodríguez AR, del Campillo MC, Torrent J (2013) Phosphate aggravates iron chlorosis in sensitive plants grown on model calcium carbonate−iron oxide systems. Plant Soil 373:31–42

    Google Scholar 

  • Sattari SZ, Bouwman AF, Giller KE, van Ittersum MK (2012) Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc Natl Acad Sci U S A 109:6348–6353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I (2007) Proteome salicylic acid and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943–3952

    CAS  PubMed  Google Scholar 

  • Seltman HJ (2018) Experimental design and analysis. Available on line at http://www.stat.cmu.edu/~hseltman/309/Book/Book.pdf

  • Shang C, Huang PM, Stewart JWB (1990) Kinetics of adsorption of organic and inorganic phosphates by short-range ordered precipitate of aluminium. Can J Soil Sci 70:461–470

    CAS  Google Scholar 

  • Shao XH, Xing CH, Du ST, Yu CY, Lin XY, Zhang YS (2006) Phosphorus adsorption saturation of Ferrihydrate as an index of phosphorus availability to Paddy Rice. J Plant Nutr 29:1187–1197. https://doi.org/10.1080/01904160600767245

    Article  CAS  Google Scholar 

  • Singh B, Boukhris I, Pragya KV, Yadav AN, Farhat-Khemakhem A, Kumar A, Singh D, Blibech M, Chouayekh H, Alghamdi OA (2020) Contribution of microbial phytases to the improvement of plant growth and nutrition: a review. Pedosphere 30:295–313

    Google Scholar 

  • StatPoint Technologies (2013) Statgraphics centurion XVI. Warrenton

  • Stutter MI, Shand CA, George TS, Blackwell MSA, Bol R, MacKay RL, Richardson AE, Condron LM, Turner BL, Haygarth PM (2012) Recovering phosphorus from soil: a root solution? Environ Sci Technol 46:1977–1978

    CAS  PubMed  Google Scholar 

  • Stutter M, Stand C, George T, Blackwell M, Dixon L, Bol R, MacKay R, Richardson A, Condron L, Haygarth P (2015) Land use and soil factors affecting accumulation of phosphorus species in temperate soils. Geoderma 257–258:29–39

    Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    CAS  Google Scholar 

  • Tang J, Leung A, Leung C, Lim BL (2006) Hydrolysis of precipitated phytate by three distinct distinct families of phytases. Soil Biol Biochem 38:1316–1324

    CAS  Google Scholar 

  • Tran TT, Hashim SO, Gaber Y, Mamo G, Mattiasson B, Hatti-Kaul R (2011) Thermostability alkaline phytase from Bacillus sp. MD2: effect of divalent metals on activity and stability. J Inorg Biochem 105:1000–1007

    CAS  PubMed  Google Scholar 

  • Tuitert G, Szczech M, Bollen GJ (1998) Suppression of Rhizoctonia solani in potting mixtures amended with compost made from organic household waste. Phytopathology 88:764–773

    CAS  PubMed  Google Scholar 

  • Turner BL, Baxter R, Whitton BA (2002) Seasonal phosphatase activity in three characteristic soils of the English uplands polluted by long-term atmospheric nitrogen deposition. Environ Pollut 120:313–317

    CAS  PubMed  Google Scholar 

  • Vohra A, Satyanarayana T (2003) Phytases: microbial sources, production, purification, and potential biotechnological applications. Crit Rev Biotechnol 23:29–60

    CAS  PubMed  Google Scholar 

  • Wang X, Li W, Harrington R, Liu F, Parise JB, Feng X, Sparks DL (2013) Effect of ferrihydrite crystallite size on phosphate adsorption reactivity. Environ Sci Technol 47:10322–10331

    CAS  PubMed  Google Scholar 

  • Yang XZ, Chen LJ (2017) Distribution of exogenous phytase activity in soil solid–liquid phases and their effect on soil organic P hydrolysis. J Plant Nutr Soil Sci 180:39–48. https://doi.org/10.1002/jpln.201600421

    Article  CAS  Google Scholar 

  • Zhou X, Wu F (2012) Dynamics of the diversity of fungal and Fusarium communities during continuous cropping of cucumber in the greenhouse. FEMS Microbiol Ecol 80:469–478

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by the Spanish Ministry of Economy, Industry, and Competitiveness and the European Regional Development Fund of the European Union through the National Research, Development and Innovation Program (Plan Estatal I + D + i, Project AGL2017-87074-C2-1-R). The authors thank the Agricultural Research Service of the University of Seville (SIA) for technical assistance and access to experimental facilities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana María García-López.

Additional information

Responsible Editor: Tim S. George.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 29 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-López, A.M., Recena, R. & Delgado, A. The adsorbent capacity of growing media does not constrain myo-inositol hexakiphosphate hydrolysis but its use as a phosphorus source by plants. Plant Soil 459, 277–288 (2021). https://doi.org/10.1007/s11104-020-04764-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04764-1

Keywords

Navigation