Skip to main content
Log in

Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil

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

Abstract

Exudation of organic acid anions by plants as well as root-induced changes in rhizosphere pH can potentially improve phosphate (Pi) availability in the rhizosphere and are frequently found to occur simultaneously. In non-calcareous soils, a major proportion of Pi is strongly sorbed to metal oxi(hydr)oxides of mainly iron (Fe) and aluminium (Al) and organic anions are known to compete with Pi for the same sorption sites (ligand exchange) or solubilize Pi via ligand-promoted mineral dissolution. Root-induced co-acidification may also further promote Pi release from soil. The relative efficiency of these different solubilization mechanisms, however, is poorly understood. The aims of this study were to gain a better mechanistic understanding of the solubilizing mechanisms of four carboxylates (citrate, malate, oxalate, malonate) in five soils with high and low P surface site saturation. Results indicate that at a lower P saturation of solid phase sorption sites, ligand-promoted mineral dissolution was the main Pi solubilization mechanism, while ligand exchange became more important at higher soil P concentrations. Co-acidification generally increased Pi solubility in the presence of carboxylates; however the relative solubilizing effect of carboxylates compared to the background electrolyte (KCl) control decreased by 20–50%. In soils with high amounts of exchangeable calcium (Ca), the proton-induced Ca solubilization reduced soluble Pi, presumably due to ionic-strength-driven changes in the electric surface potential favoring a higher Pi retention. Across a wider soil pH range (pH 3–8), Pi solubility increased with increasing alkalinity, as a result of both, more negatively charged sorption sites, as well as DOC-driven changes in Fe and Al solubility, which were further enhanced by the presence of citrate. Overall, the relative efficiency of carboxylates in solubilizing Pi was greatest in soils with medium to high amounts of anionic binding sites (mainly Fe- and Al-oxy(hydr)oxides) and a medium P sorption site coverage, with citrate being most effective in solubilizing Pi.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Akhtar MS, Oki Y, Adachi T (2009) Mobilization and acquisition of sparingly soluble P-sources by Brassica cultivars under P-starved environment II. rhizospheric pH changes, redesigned root architecture and Pi-uptake kinetics. J Integr Plant Biol 51:1024–1039

    Article  CAS  PubMed  Google Scholar 

  • Barrow NJ (1984) Modelling the effect of pH on phosphate sorption by soils. J Soil Sci 35:283–297

    Article  CAS  Google Scholar 

  • Barrow NJ (1999) The four laws of soil chemistry: the Leeper lecture. Aust J Soil Res 37:787–829

    Article  CAS  Google Scholar 

  • Barrow NJ, Cartes P, Mora LM (2005) Modifications to the Freundlich equation to describe anion sorption over a large range and to describe competition between pairs of ions. Eur J Soil Sci 56:601–606

    Article  CAS  Google Scholar 

  • Bhatti JS, Comerford NB, Johnston CT (1998) Influence of oxalate and soil organic matter on sorption and desorption of phosphate onto a spodic horizon. Soil Sci Soc Am J 62:1089–1095

    Article  CAS  Google Scholar 

  • Bowden JW, Nagarajah S, Barrow NJ, Posner AM, Quirk JP (1980) Describing the Adsorption of phosphate, citrate and selenite on a variable-charge mineral surface. Aust J Soil Res 18:49–60

    Article  CAS  Google Scholar 

  • Drever JI, Stillings LL (1997) The role of organic acids in mineral weathering. Colloids Surf, A Physicochem Eng Asp 120:167–181

    Article  CAS  Google Scholar 

  • Fox TR, Comerford NB, McFee WW (1990) Phosphorus and aluminium release from a spodic horizon mediated by organic acids. Soil Sci Soc Am J 54:1763–1767

    Article  CAS  Google Scholar 

  • Gerke J (1993) Phosphate adsorption by humic/Fe-oxide mixtures aged at pH 4 and 7 and by poorly ordered Fe-oxide. Geoderma 59:279–288

    Article  CAS  Google Scholar 

  • Gerke J, Hermann R (1992) Adsorption of orthophosphate to humic-Fe complexes and to amorphous Fe-oxide. Z Pflanzenernahr Bodenkd 155:233–236

    Article  CAS  Google Scholar 

  • Gerke J, Beißner L, Römer W (2000) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters. J Plant Nutr Soil Sci 163:207–212

    Article  CAS  Google Scholar 

  • Guerrero C, Mataix-Solera J, Arcenegui V, Mataix-Beneyto J, Gómez I (2007) Near-infrared spectroscopy to estimate the maximum temperatures reached on burned soils. Soil Sci Soc Am J 71:1029–1037

    Article  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 

  • Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113:161–165

    Article  CAS  Google Scholar 

  • Johnson SE, Loeppert RH (2006) Role of organic acids in phosphate mobilization from goethite. Soil Sci Soc Am J 70:222–234

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Jones DL, Brassington DS (1998) Sorption of organic acids in acid soils and its implication in the rhizosphere. Eur J Soil Sci 49:447–455

    Article  CAS  Google Scholar 

  • Jones DL, Edwards AC (1998) Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol Biochem 30:1895–1902

    Article  CAS  Google Scholar 

  • Jones DL, Darrah 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

    Article  CAS  Google Scholar 

  • Kirk GJD, Santos EE, Santos MB (1999) Phosphate solubilization by organic anion excretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate solubility and uptake. New Phytol 142:185–200

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Jones DL (2006) Glucose uptake by maize roots and its transformation in the rhizosphere. Soil Biol Biochem 38:851–860

    Article  CAS  Google Scholar 

  • Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  PubMed  Google Scholar 

  • Lan Mu, Comerford NB, Fox TR (1995) Organic anions’ effect on phosphorus release from spodic horizons. Soil Sci Soc Am J 59:1745–1749

    Article  CAS  Google Scholar 

  • Lindsay WL (1979) Chemical equilibria in soils. Wiley, USA

    Google Scholar 

  • Loeppert RH, Inskeep WP (1996) Iron. In: Methods of soil analysis part 3: chemical methods, SSSA Book Series No 5, Madison, USA, 693–644

  • Martell AE, Smith RM (1976–1989) Critical Stability Constants, 6 vol. Plenum Press, New York

  • Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere—biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC Press Taylor & Francis Group, Boca Raton, p 23

    Chapter  Google Scholar 

  • Oburger E, Kirk GJD, Wenzel WW, Puschenreiter M, Jones DL (2009) Interactive effects of organic acids in the rhizosphere. Soil Biol Biochem 41:449–457

    Article  CAS  Google Scholar 

  • Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895

    Article  CAS  Google Scholar 

  • Oste LA, Temminghoff EJM, Van Riemsdijk WH (2002) Solid-solution partitioning of organic matter in soils as influenced by an increase in pH or Ca concentration. Environ Sci Technol 36:208–214

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sims JT, Pierzynski GM (2005) Chapter 2: chemistry of phosphorus in soil. In: chemical processes in soil, SSSA book series, no 8, Madison Wisconsin, USA, 151–192

  • Strobel BW (2001) Influence of vegetation on low-molecular-weight carboxylic acids in soil solution—a review. Geoderma 99:169–198

    Article  CAS  Google Scholar 

  • Ström L, Owen AG, Godbold DL, Jones DL (2002) Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Biol Biochem 34:703–710

    Article  Google Scholar 

  • Tipping E, Woof C (1990) Humic substances in acid organic soils: modeling their release to the soil solution in terms of humic charge. J Soil Sci 41:573–586

    Article  CAS  Google Scholar 

  • van Hees PAW, Vinogradoff SI, Edwards AC, Godbold DL, Jones DL (2003) Low molecular weight organic acid adsorption in forest soils: effects on soil solution concentrations and biodegradation rates. Soil Biol Biochem 35:1015–1026

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Wang Y-J, Chen J-H, Cui Y-X, Wang S-Q, Zhou D-M (2009) Effects of low-molecular-weight organic acids on Cu(II) adsorption onto hydroxyapatite nanoparticles. J Hazard Mater 162:1135–1140

    Article  CAS  PubMed  Google Scholar 

  • Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Martinoia E (2006) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927

    Article  CAS  PubMed  Google Scholar 

  • Wouterlood M, Cawthray GR, Scanlon TT, Lambers H, Veneklaas EJ (2004) Carboxylate concentrations in the rhizosphere of lateral roots of chickpea (Cicer arietinum) increase during plant development, but are not correlated with phosphorous status of soil or plants. New Phytol 162:745–753

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Austrian Science Fund (FWF, Grant No.: P20069) and the UK Biotechnology and Biological Sciences Research Council. We thank Dr Jim Barrow for a highly instructive e-mail conversation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eva Oburger.

Additional information

Responsible Editor: N. Jim Barrow.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplement Table 1

Statistical results corresponding to Figure 2 (DOC 40 kb)

Supplement Table 2

Statistical results corresponding to Figure 3 (DOC 81 kb)

Supplement Table 3

Statistical results corresponding to Figure 4 (DOC 37 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oburger, E., Jones, D.L. & Wenzel, W.W. Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil. Plant Soil 341, 363–382 (2011). https://doi.org/10.1007/s11104-010-0650-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0650-5

Keywords

Navigation