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X-ray fluorescence elemental mapping of roots, stems and leaves of the nickel hyperaccumulators Rinorea cf. bengalensis and Rinorea cf. javanica (Violaceae) from Sabah (Malaysia), Borneo

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Abstract

Aims

There are major knowledge gaps in understanding the translocation leading from nickel uptake in the root to accumulation in other tissues in tropical nickel hyperaccumulator plant species. This study focuses on two species, Rinorea cf. bengalensis and Rinorea cf. javanica and aims to elucidate the similarities and differences in the distribution of nickel and physiologically relevant elements (potassium, calcium, manganese and zinc) in various organs and tissues.

Methods

High-resolution X-ray fluorescence microscopy (XFM) of frozen-hydrated and fresh-hydrated tissue samples and nuclear microprobe (micro-PIXE) analysis of freeze-dried samples were used to provide insights into the in situ elemental distribution in these plant species.

Results

This study has shown that the distribution pattern of nickel hyperaccumulation is typified by very high levels of accumulation in the phloem bundles of roots and stems. In the leaves, nickel is preferentially located in epidermal cell region, whereas manganese is located mainly in the lower epidermis and zinc in the upper epidermis and palisade mesophyll. The abundant formation of calcium-oxalate crystals, lining the collenchyma, is a prominent feature of both Rinorea cf. bengalensis and Rinorea cf. javanica.

Conclusions

Future investigations on Rinorea cf. bengalensis and Rinorea cf. javanica should focus on unravelling the mechanisms of nickel uptake in the root, specifically targeting the identification of nickelspecific membrane transporters.

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Acknowledgements

We thank Rositti Karim, Sukaibin Sumail (Sabah Parks) and Postar Miun (Sabah Forestry Department) for their help during the fieldwork in Malaysia. We thank Sabah Parks for granting permission to conduct research in Kinabalu Park, and the Sabah Biodiversity Council for research permits. This research was undertaken on the X-Ray Fluorescence Microscopy beamline of the Australian Synchrotron (part of ANSTO), Victoria, Australia. This work was supported by the Multi-modal Australian ScienceS Imaging and Visualisation Environment (MASSIVE). This research was also undertaken at P06 at DESY, a member of the Helmholtz Association (HGF). We would like to thank Kathryn Spiers and Jan Garrevoet for assistance during the experiments. This research was undertaken at the nuclear microprobe facility of iThemba Laboratory for Accelerator Based Sciences in South Africa. We thank Eunice Grinan (UQ) for assistance with the SEM analysis. We acknowledge the Centre for Microscopy and Microanalysis of The University of Queensland. The French National Research Agency through the national “Investissements d’avenir” program (ANR-10-LABX-21, LABEX RESSOURCES21) and through the ANR-14-CE04-0005 Project “Agromine” is acknowledged for funding A. van der Ent's post-doctoral position in 2014–2015. A. van der Ent was the recipient of a Discovery Early Career Researcher Award (DE160100429) from the Australian Research Council. H. H. Harris acknowledges the Australian Research Council for financial support (DP140100176). W.J. Przybylowicz and J. Mesjasz-Przybylowicz are recipients of the South African National Foundation incentive grants No 114693 and 114694, respectively.

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Authors and Affiliations

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

    Antony van der Ent

  2. Laboratoire Sols et Environnement, Université de Lorraine, Nancy, France

    Antony van der Ent

  3. Australian Synchrotron, ANSTO, Melbourne, Australia

    Martin D. de Jonge

  4. School of Chemistry, University of Sydney, Sydney, Australia

    Rachel Mak

  5. Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

    Jolanta Mesjasz-Przybyłowicz & Wojciech J. Przybyłowicz

  6. Faculty of Physics & Applied Computer Science, AGH University of Science and Technology, al. Mickiewicza 30, 30-059, Kraków, Poland

    Wojciech J. Przybyłowicz

  7. Materials Research Department, iThemba LABS, National Research Foundation, P.O. Box 722, Somerset West 7129, South Africa

    Alban D. Barnabas

  8. Department of Chemistry, The University of Adelaide, Adelaide, Australia

    Hugh H. Harris

Authors
  1. Antony van der Ent
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  2. Martin D. de Jonge
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  3. Rachel Mak
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  4. Jolanta Mesjasz-Przybyłowicz
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  5. Wojciech J. Przybyłowicz
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  6. Alban D. Barnabas
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  7. Hugh H. Harris
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Contributions

A.vdE, H.H.H and J.M.P conducted the fieldwork and collected the samples in Malaysia. A.vdE, M.dJ and H.H.H conducted the synchrotron X-ray Fluorescence Microscopy (XFM) experiment. J.M.P and W.P conducted the nuclear microbe (PIXE) experiment. A.B conducted the anatomical investigations. R.M performed the XFM data processing and analysis. W.P performed the PIXE data processing and analysis. A.vdE conducted the SEM imaging and bulk elemental analysis. A.VDE, J.M.P, W.P., A.B, M.dJ, RM and H.H.H wrote the manuscript.

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Correspondence to Antony van der Ent.

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van der Ent, A., de Jonge, M.D., Mak, R. et al. X-ray fluorescence elemental mapping of roots, stems and leaves of the nickel hyperaccumulators Rinorea cf. bengalensis and Rinorea cf. javanica (Violaceae) from Sabah (Malaysia), Borneo. Plant Soil 448, 15–36 (2020). https://doi.org/10.1007/s11104-019-04386-2

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