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A novel method for in situ imaging of root exudates and labile elements reveals phosphorus deficiency-induced mobilization of rare earth elements in the rhizosphere of Phytolacca americana

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Abstract

Aims

Phosphorus (P) deficiency-induced mobilization of rare earth elements (REEs) in the rhizosphere contributes to REE accumulation in the hyperaccumulator Phytolacca americana, but a lack of in situ methods for visualization of the root-soil interface limits our understanding of the underlying processes.

Methods

Diffusive gradients in thin-films (DGT) devices were used for probing root exudates, REEs and P in the P. americana rhizosphere. Desorption electrospray ionization mass spectrometry and laser-ablation inductively coupled mass spectrometry were used for in situ imaging of root exudates, REEs and P sorbed on the DGT.

Results

The novel approach demonstrated here is capable of synchronously and quantitatively characterizing the distribution of root exudates and labile elements in the rhizosphere. The secretion fluxes of citrate and oxalate in the rhizosphere under P deficiency were three times higher than under P sufficient condition; and the lanthanum (La) fluxes in the rhizosphere under P deficiency were ten times greater than at P sufficiency condition. The enrichment of P and La under P deficiency and depletion under P sufficient conditions in the rhizosphere suggests that P deficiency-induced organic acid secretion is crucial for the mobilization of soil REEs and subsequent REE accumulation in P. americana.

Conclusion

The combination of DGT devices with mass spectrometry imaging is technically feasible for in situ synchronous imaging of root exudates, REEs and labile elements at the root-soil interface. Our study shed light on processes of mobilization of mineral elements in the rhizosphere induced as a side-effect of the P acquisition mechanism.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgments

We thank Ms. Hai-Yun Zhou (Instrumental Analysis & Research Center, Sun Yat-Sen University) for her help in DESI-MS analysis.

Funding

This work was supported by the National Natural Science Foundation of China (41771343, 41920104003, 41877475, 42007110) and the 111 Project (B18060).

Author information

Authors and Affiliations

  1. School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou, 510006, China

    Chong Liu, Ting-Xuan Ding, Chang Liu, Wen-Shen Liu, Ye-Tao Tang & Rong-Liang Qiu

  2. Institute of Agricultural Resources and Environment, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China

    Chong Liu

  3. Laboratory of Genetics, Wageningen University and Research, Wageningen, 6708 PB, The Netherlands

    Antony van der Ent

  4. Laboratoire Sols et Environnement, INRAE, Université de Lorraine, Nancy, 54000, France

    Antony van der Ent, Jean Louis Morel  & Catherine Sirguey

  5. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, Brisbane, QLD, 4072, Australia

    Antony van der Ent

  6. Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Guangdong Provincial Engineering Research Center for Heavy Metal Contaminated Soil Remediation, Sun Yat-sen University, Guangzhou, 510006, China

    Wen-Shen Liu & Ye-Tao Tang

  7. Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Provincial Key Laboratory of Agricultural & Rural Pollution Abatement and Environmental Safety, College of Natural Resources and Environment, South China Agricultural University, Guangzhou, 510642, China

    Rong-Liang Qiu

Authors
  1. Chong Liu
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Contributions

Chong Liu: Conceptualization, Methodology, Investigation, Writing - Original Draft, Visualization. Ting-Xuan Ding: Methodology, Investigation, Visualization. Antony van der Ent, Chang Liu: Writing - Review & Editing. Wen-Shen Liu: Writing-Review & Editing, Funding acquisition. Jean Louis Morel, Catherine Sirguey: Review. Ye-Tao Tang, Rong-Liang Qiu: Supervision, Writing - Review & Editing, Funding acquisition.

Corresponding author

Correspondence to Wen-Shen Liu.

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Liu, C., Ding, TX., van der Ent, A. et al. A novel method for in situ imaging of root exudates and labile elements reveals phosphorus deficiency-induced mobilization of rare earth elements in the rhizosphere of Phytolacca americana. Plant Soil 495, 13–26 (2024). https://doi.org/10.1007/s11104-023-06146-9

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