Skip to main content

Advertisement

SpringerLink
Log in

Organic anions facilitate the mobilization of soil organic phosphorus and its subsequent lability to phosphatases

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

Abstract

Purpose

Organic anions commonly released from plant roots and microorganisms are widely reported to mobilize soil phosphorus (P). We characterized soil organic P that was mobilized by organic anions and assessed its amenability to hydrolysis by phosphatase enzymes.

Methods

Six soils differing in organic P concentration were extracted with citrate, malate or oxalate solutions and incubated with preparations of phosphomonoesterase, phosphodiesterase, or phytase. Organic P compounds present in these extracts were putatively identified and quantified with solution 31P-NMR spectroscopy and the enzyme-labile P fractions were assessed by changes in molybdate-reactive P (MRP) concentration.

Results

Organic P mobilization varied markedly among the organic anions. Extraction with 10 mM citrate was most effective and extracted 7.8-fold more total P than the water controls across all soils. Approximately 95% of the extracted P was non-MRP. The organic anions increased both the amount of P extracted and the proportion of the total extracted P that was phosphatase-labile. Phytase was generally the most effective enzyme with up to 60% of the total non-MRP being amenable to hydrolysis by phytase across all extracts. The presence of inositol hexakisphosphates in the extracts, as well as other forms of organic P including nucleic acids and phospholipids, was verified by 31P-NMR with concentrations dependent on both organic anions and soil type.

Conclusion

The combination of organic anions and phosphatases represents a key mechanism by which plants and microorganisms can enhance the bioavailability of soil P. This has important implications for understanding P dynamics in natural and managed ecosystems and for ongoing efforts to improve the P-acquisition efficiency of agricultural plants.

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

Similar content being viewed by others

References

  • Anderson G, Williams EG, Moir JO (1974) A comparison of the sorption of inorganic orthophosphate and inositol hexaphosphate by six acid soils. J Soil Sci 25:51–62

    Article  CAS  Google Scholar 

  • Barrow NJ (2017) The effects of pH on phosphate uptake from the soil. Plant Soil 410:401–410

    Article  CAS  Google Scholar 

  • Bowman RA, Moir JO (1993) Basic EDTA as an extractant for soil organic phosphorus. Soil Sci Soc Amer J 57:1516–1518

    Article  CAS  Google Scholar 

  • Bünemann EK (2008) Enzyme additions as a tool to assess the potential bioavailability of organically bound nutrients. Soil Biol Biochem 40:2116–2129

    Article  Google Scholar 

  • Burkitt LL, Moody PW, Gourley CJP, Hannah MC (2002) A simple phosphorus buffering index for Australian soils. Aust J Soil Res 40: 497–513

    Article  CAS  Google Scholar 

  • Celi L, Barberis E (2005) Abiotic stabilization of organic phosphorus in the environment. In: Turner BL, Frossard E, Baldwin D (eds) Organic phosphorus in the environment. CABI Publishing, Wallingford, pp 113–132

    Chapter  Google Scholar 

  • Darch T, Blackwell MSA, Chadwick D, Haygarth PM, Hawkins JMB, Turner BL (2016) Assessment of bioavailable organic phosphorus in tropical forest soils by organic acid extraction and phosphatase hydrolysis. Geoderma 284:93–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinkelaker B, Rӧmheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L). Plant Cell Environ 12:285–292

    Article  CAS  Google Scholar 

  • George TS, Richardson AE, Smith JB, Hadobas PA, Simpson RJ (2005) Limitations to the potential of transgenic Trifolium subterraneum L. plants that exude phytase, when grown in soils with a range of organic P content. Plant and Soil 258:263–274

    Article  Google Scholar 

  • George TS, Giles CD, Menezes-Blackburn D, Condron LM, Gama-Rodrigues AC, Jaisi D, Lang F, Neal AL, Stutter MI, Almeida DS, Bol R, Cabugao KG, Celi L, Cotner JB, Feng G, Goll DS, Hallama M, Krueger J, Plassard C, Rosling A, Darch T, Fraser T, Giesler R, Richardson AE, Tamburini F, Shand CA, Lumsdon DG, Zhang H, Blackwell MSA, Wearing C, Mezeli MM, Almas AR, Audette Y, Bertrand I, Beyhaut E, Boitt G, Bradshaw N, Brearley CA, Bruulsema TW, Ciais P, Cozzolino V, Duran PC, Mora ML, de Menezes AB, Dodd RJ, Dunfield K, Engl C, Frazao JJ, Garland G, Jimenez JLG, Graca J, Granger SJ, Harrison AF, Heuck C, Hou EQ, Johnes PJ, Kaiser K, Kjaer HA, Klumpp E, Lamb AL, Macintosh KA, Mackay EB, McGrath J, McIntyre C, McLaren T, Meszaros E, Missong A, Mooshammer M, Negron CP, Nelson LA, Pfahler V, Poblete-Grant P, Randall M, Seguel A, Seth K, Smith AC, Smits MM, Sobarzo JA, Spohn M, Tawaraya K, Tibbett M, Voroney P, Wallander H, Wang L, Wasaki J, Haygarth PM (2018) Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities. Plant Soil 427:191–208

    Article  CAS  Google Scholar 

  • Gerke J, Rӧmer W, Jungk A (1994) The excretion of citric and malic-acid by proteoid roots of Lupinus albus L. – effects on soil solution concentrations of phosphate, iron, and aluminum in the proteoid rhizosphere in samples of an oxisol and a luvisol. Z Pflanzenernaehr Bodenkd 157:289–294

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Giles CD, George TS, Brown LK, Mezeli MM, Richardson AE, Shand CA, Wendler R, Darch T, Menezes-Blackburn D, Cooper P, Stutter MI, Lumsdon DG, Blackwell NSA, Wearing C, Zhang H, Haygarth PM (2016) Does the combination of citrate and phytase exudation in Nicotiana tabacum promote the acquisition of endogenous soil organic phosphorus? Plant Soil 412:43–59

    Article  Google Scholar 

  • Giles CD, Richardson AE, Cade-Menun BJ, Mezeli MM, Brown LK, Menezes-Blackburn D, Darch T, Blackwell MSA, Shand CA, Stutter MI, Wendler R, Cooper P, Lumsdon DG, Wearing C, Zhang H, Haygarth PM, George TS (2018) Complementarity between citrate- and phytase-exuding Nicotiana tabacum plants depends on soil phosphorus availability and root intermingling. Physiol Plant 163:356–371

    Article  CAS  Google Scholar 

  • Hayes JE, Richardson AE, Simpson RJ (2000) Components of organic phosphorus in soil extracts that are hydrolysed by phytase and acid phosphatase. Biol Fert Soils 32:279–286

    Article  CAS  Google Scholar 

  • Hayes PE, Nge FJ, Cramer MD, Finnegan PM, Fu P, Hopper SD, Oliveira RO, Turner BL, Zemunik G, Zhong H, Lambers H (2021) Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in old phosphorus-impoverished landscapes. Plant Soil 462:67–88

    Article  CAS  Google Scholar 

  • He X, Augusto L, Goll DS, Ringeval B, Wang Y, Helfenstein J, Huang Y, Yu K, Wang Z, Yang Y, Hou E (2021) Global patterns and drivers of soil total phosphorus concentration. Earth Syst Sci Data 13:5831–5846

    Article  Google Scholar 

  • Hong JK, Yamane I (1981) Distribution of inositol phosphate in the molecular size fractions of humic and fulvic acid fractions. Soil Sci Plant Nutr 27:295–303

    Article  CAS  Google Scholar 

  • Irving GCJ, McLaughlin MJ (1990) A rapid and simple field test for phosphorus in Olsen and Bray No. 1 extracts of soil. Comm Soil Sci Plant Anal 21:2245–2255

    Article  CAS  Google Scholar 

  • Isbell RF (1996) The Australian soil classification. CSIRO Publishing, Melbourne

    Google Scholar 

  • Jackman RH, Black CA (1951) Solubility of iron, aluminum, calcium and magnesium inositol phosphates at different pH values. Soil Sci 72:179–186

    Article  CAS  Google Scholar 

  • Jarosch KA, Kandeler E, Frossard E, Bünemann EK (2019) Is the enzymatic hydrolysis of soil organic phosphorus compounds limited by enzyme or substrate availability? Soil Biol Biochem 139:107628

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Khademi Z, Jones DL, Malakouti MJ, Asadi F, Ardebili M (2009) Organic acid mediated nutrient extraction efficiency in three calcareous soils. Aust J Soil Res 47:213–220

    Article  CAS  Google Scholar 

  • Kidd DR, Ryan MH, Hahne D, Haling RE, Lambers H, Sandral GA, Simpson RJ, Cawthray GR (2018) The carboxylate composition of rhizosheath and root exudates from twelve species of grassland and crop legumes with special reference to the occurrence of citramalate. Plant Soil 424:389–403

    Article  CAS  Google Scholar 

  • Kooyman RM, Laffan SW, Westoby M (2017) The incidence of low phosphorus soils in Australia. Plant Soil 412:143–150

    Article  CAS  Google Scholar 

  • Lambers H, Clements JC, Nelson MN (2013) How a phosphorus acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Amer J Bot 100:263–288

    Article  CAS  Google Scholar 

  • Lambers H, Finnegan PM, Laliberté E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156:1058–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martinez-Ferri E (2002) The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant Soil 238:111–122

    Article  CAS  Google Scholar 

  • Lambers H, Martinoia E, Renton M (2015) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biology 25:23–31

    Article  CAS  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    Article  PubMed  Google Scholar 

  • Lynch JP, Brown KM (2001) Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237

    Article  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

    Article  CAS  Google Scholar 

  • Maruyama H, Yamamura T, Kaneko Y, Matsui H, Watanabe T, Shinano T, Osaki M, Wasaki J (2012) Effect of exogenous phosphatase and phytase activities on organic phosphate mobilization in soils with different phosphate adsorption capacities. Soil Sci Plant Nutri 58:41–51

    Article  CAS  Google Scholar 

  • McIvor JG, Guppy C, Probert ME (2011) Phosphorus requirements of tropical grazing systems: the northern Australian experience. Plant Soil 349:55–67

    Article  CAS  Google Scholar 

  • McLaren TI, Smernik RJ, McLaughlin MJ, Doolette AL, Richardson AE, Frossard E (2019a) The chemical nature of soil organic phosphorus – a critical review and global compilation of quantitative data. Advan Agron 160:51–124

    Article  Google Scholar 

  • McLaren TI, Verel R, Frossard E (2019b) The structural composition of soil phosphomonoesters as determined by solution 31P-NMR spectroscopy and transverse (T2) relaxation experiments. Geoderma 345:31–37

    Article  CAS  Google Scholar 

  • McLaughlin MJ, McBeath TM, Smernik R, Stacey SP, Ajiboye B, Guppy C (2011) The chemical nature of P accumulation in agricultural soils-implications for fertiliser management and design: an Australian perspective. Plant Soil 349:67–87

    Article  Google Scholar 

  • Neumann G, Massonneau A, Martinoia E, Rӧmheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382

    Article  CAS  Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120

    Article  CAS  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture Circular No. 939

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Chemical and microbiological properties, vol 2. ASA-SSSA, Madison, pp 403–430

    Google Scholar 

  • Otani T, Ae N (1999) Extraction of organic phosphorus in Andosols by various methods. Soil Sci Plant Nutr 45:151–161

    Article  CAS  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173:181–190

    Article  CAS  PubMed  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant Soil 288:127–139

    Article  CAS  Google Scholar 

  • Rayment G E, Lyons DJ (2011) Soil chemical methods: Australasia, 3. CSIRO publishing

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

    Chapter  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 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson AE, Simpson RJ, George TS, Hocking PJ (2009) Plant mechanisms to optimize access to soil phosphorus. Crop Pasture Sci 60:124–143

    Article  CAS  Google Scholar 

  • Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ 24:891–903

    Article  CAS  Google Scholar 

  • Ryan PR, James RA, Weligama K, Delhaize E, Rattey A, Lewis DC, Bovill WD, McDonald G, Rathjen TM, Wang E, Fettell NA, Richardson AE (2014) Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat. Physiol Plant 151:230–242

    Article  CAS  PubMed  Google Scholar 

  • Schoenau JJ, Huang WZ (1991) Anion-exchange membrane, water, and sodium bicarbonate extractions as soil tests for phosphorus. Com Soil Sci Plant Anal 22:465–492

    Article  CAS  Google Scholar 

  • Shane MW, Lambers H, Cawthray GR, Kuhn AJ, Schurr U (2008) Impact of phosphorus mineral source (Al-P or Fe-P) and pH on cluster-root formation and carboxylate exudation in Lupinus albus L. Plant Soil 304:169–178

    Article  CAS  Google Scholar 

  • Shi J, Strack D, Albornoz F, Han Z, Lambers H (2020) Differences in investment and functioning of cluster roots account for different distributions between Banksia attenuata and B. sessilis, with contrasting life history. Plant Soil 447:85–98

    Article  CAS  Google Scholar 

  • Shi S, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone M, Condron L (2011) Influence of selected root exudate components on soil microbial communities. FEMS Microb Ecol 77:600–610

    Article  CAS  Google Scholar 

  • Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of temperate farming systems. Plant Soil 349:89–120

    Article  CAS  Google Scholar 

  • Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme. Plant Soil 155:95–98

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Turner BL (2007) Inositol phosphates in soil: amounts, forms and significance of the phosphorylated inositol stereoisomers. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol Phosphates: Linking Agriculture and the Environment. CAB International, Wallingford, pp 186–206

    Chapter  Google Scholar 

  • Turner BL (2008) Resource partitioning for soil phosphorus: a hypothesis. J Ecol 96:698–702

    Article  CAS  Google Scholar 

  • Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forest. Nature 555:367–370

    Article  CAS  PubMed  Google Scholar 

  • Turner BL, Mahieu N, Condron LM (2003) Phosphorus-31 nuclear magnetic resonance spectral assignments of phosphorus compounds in soil NaOH-EDTA extracts. Soil Sci Soc Amer J 67:497–510

    Article  CAS  Google Scholar 

  • Turner BL, Papházy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philos Trans Roy Soc Series B 357:449–469

    Article  CAS  Google Scholar 

  • Turner BL, Richardson AE (2004) Identification of scyllo-inositol phosphates in soils by solution phosphorus-31 nuclear magnetic resonance spectroscopy. Soil Sci Soc Amer J 68:802–808

    Article  CAS  Google Scholar 

  • Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197

    Article  CAS  Google Scholar 

  • Wang X, Pearse SJ, Lambers H (2013) Cluster-root formation and carboxylate release in three Lupinus species as dependent on phosphorus supply, internal phosphorus concentration and relative growth rate. Ann Bot 112:1449–1459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Lambers H (2020) Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives. Plant Soil 447:135–156

    Article  CAS  Google Scholar 

  • Wassen MJ, Olde Venterink H, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437:547–550

    Article  CAS  PubMed  Google Scholar 

  • Weaver DM, Wong MTF (2011) Scope to improve phosphorus (P) management and balance efficiency of crop and pasture soils with contrasting P status and buffering indices. Plant Soil 349:37–54

    Article  CAS  Google Scholar 

  • Wei LL, Chen CR, Xu ZH (2010) Citric acid enhances the mobilization of organic phosphorus in subtropical and tropical forest soils. Biol Fert Soils 46:765–769

    Article  CAS  Google Scholar 

  • Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, 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, Turner S, Lambers H, Veneklaas EJ (2004) Rhizosphere carboxylate concentrations of chickpea are affected by genotype and soil type. Plant Soil 261:1–10

    Article  CAS  Google Scholar 

  • Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:1–4

    Article  Google Scholar 

Download references

Acknowledgements

This paper was prepared in specific tribute to Professor Hans Lambers as Editor in Chief for Plant and Soil. The data were compiled from historic data sets that were generated through a Grains Research and Development (GRDC) supported industry-based project awarded to CSIRO (CSP318) that was conducted 2001 to 2003. The experimental work was undertaken by Dr M. Hens as a post-doctoral scientist under the supervision and in the laboratory of the late Dr P. Hocking. We thank Dr Ben Turner for coordinating the NMR analyses and providing interpretation of the spectral data. The experimental work was conducted as part of the core effort of the CSIRO Plant Nutrition Group, who are represented as authors of the paper. The long-standing interaction of the Plant Nutrition Group with Professor Lambers and his laboratory at University of WA is greatly appreciated. In particular, the shared interests in the role of organic anions in mobilization of soil P, especially through the uniqueness of Australian native plants and in response to P deficiency that is very common across most Australian soils is acknowledged. In support of Prof Lambers, R. Simpson, P. Ryan, T. George and E. Delhaize have contributed to Plant and Soil as Section or Consulting Editors. In collaborative work with the Lambers Group, A. Richardson and R. Simpson have been adjunct Professors at UWA. Contribution of T George to this work was also supported by the Scottish Government. We thank Alex Blumenfeld (University of Idaho) for NMR technical support and also the many technicians at CSIRO that have supported the plant nutrition work conducted by the Group over many years.

Author information

Author notes

  1. Maarten Hens

    Present address: Flemish Government, Department of Environmental and Spatial Planning, Koning Albert II-laan 20, 1000, Brussels, Belgium

  2. Emmanuel Delhaize

    Present address: Research School of Biology, Australian National University, Canberra, ACT, 2601, Australia

Authors and Affiliations

  1. CSIRO Agriculture & Food, PO Box 1700, Canberra, ACT, 2601, Australia

    Alan E. Richardson, Emmanuel Delhaize, Peter R. Ryan, Richard J. Simpson & Peter J. Hocking

  2. Ecological Sciences, James Hutton Institute, Dundee, DD2 5DA, Scotland

    Timothy S. George

  3. Research Institute for Nature and Forest, Kliniekstraat 25, 1070, Brussels, Belgium

    Maarten Hens

Authors
  1. Alan E. Richardson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy S. George
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maarten Hens
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emmanuel Delhaize
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter R. Ryan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard J. Simpson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Peter J. Hocking
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alan E. Richardson.

Ethics declarations

This work was initiated through a Grains Research and Development (GRDC) supported research project awarded to PJH (CSP318). The authors declare that no other direct funds or grants were received during the preparation of this manuscript and that the authors were otherwise supported by their indicated host institutions. The authors have no relevant financial or non-financial interests to disclose. All authors contributed to the study conception and design. Data collection and analysis was initially conducted by M. Hens and completed by A. Richardson The first draft of the manuscript was written by A. Richardson and all authors (with exception of PJH) have provided comment to the paper and approved the final manuscript. The datasets generated and analyzed in the study are available from the corresponding author on reasonable request.

Additional information

Publisher's note

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

Responsible Editor: N. Jim Barrow.

In memoriam of Peter J. Hocking

Manuscript for submission to Plant and Soil—Special Edition—Hans Lambers 30 years

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Richardson, A.E., George, T.S., Hens, M. et al. Organic anions facilitate the mobilization of soil organic phosphorus and its subsequent lability to phosphatases. Plant Soil 476, 161–180 (2022). https://doi.org/10.1007/s11104-022-05405-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-022-05405-5

Keywords

Search

Navigation