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

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.

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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.

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Correspondence to Alan E. Richardson.

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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.

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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 (2022). https://doi.org/10.1007/s11104-022-05405-5

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Keywords

  • NMR
  • Plant nutrition
  • Citrate
  • Malate
  • Oxalate
  • Phytate
  • Phytase