Phytometallomics

A range of metals and metalloids play key roles in the homeostasis of all plants as they are essential and broadly utilised in plants. Invariably these elements are toxic in large quantities yet cause functional deficiencies at low concentrations. In crops, deficiency and toxicity of particular metal(loid)s in agricultural soils are important factors reducing productivity. Plant metal(loid) deficiencies also have important implications for human health, as most mineral nutrients are (directly or indirectly) derived from plant-based foods.

Critical to research in many subfields across the plant sciences is to understand the distribution of both nutrients, and essential and potentially toxic elements within plant tissues.¹ There are numerous non-spatially resolved techniques appropriate for determining elemental concentrations in plant samples, such as inductively coupled plasma-atomic emission spectroscopy/mass spectrometry (ICP-AES/MS).¹ In contrast, in situ methods have the ability to directly probe elemental concentrations in plant organs and tissues. The most frequently used technique is X-ray fluorescence spectroscopy (μXRF) using both synchrotron and laboratory platforms.² This method is especially powerful because it provides a level of sensitivity for measurement of the full metallome and presents the only approach for determining the coordination environment of metal(loid) complexes in situ.³

Hyperaccumulators are rare plants that accumulate particular metals or metalloids in their living tissues to levels that may be orders of magnitude greater than is normal for most plants.⁴ Hyperaccumulator plants are known to accumulate a range of different elements, such as arsenic, nickel, cobalt, zinc, selenium, and thallium.⁵ Hyperaccumulator plants evolved highly efficient mechanisms for taking up metal(loid)s in roots followed by translocation and sequestration into the shoots, and this makes these plants particularly useful models for fundamental science.² They provide opportunities for better understanding of metal regulation, including the physiology of metal uptake, transport and sequestration, as well as evolution and adaptation in extreme environments.¹ Unravelling the mechanisms underlying hyperaccumulation is a key pre-requisite to engineering highly tolerant novel crop plants that are future-proofed for increasing global demand. Insights into the mechanisms of hyperaccumulation may also be applied to improve or limit the uptake and accumulation of deficient or toxic elements in food crops, such as soybean, wheat or potato.

Investigating metal(loid) homeostasis in plants is approached from molecular biology to physiology and spans several length-scales, from whole plants down to individual cells, and ultimately metalloproteins.² Often a combination of elemental distribution and chemical speciation, coupled to data on plant (stress) responses is powerful in deciphering key processes underlying metal(loid) homeostasis in plants.⁶

This themed collection in Metallomics contains studies focusing on wide-ranging aspects of metal(loid) homeostasis in plants, exemplified, but not limited to, the extreme instances provided by hyperaccumulators. A number of articles featured in the themed collection have utilised synchrotron-based μXRF approaches to determine in situ elemental distribution (and also chemical speciation) in the target species. Technological advances have made it possible to undertake fast scanning to investigate hydrated/live specimens, and also spurred the advent of handheld XRF devices and laboratory-based μXRF instruments. Although these instruments will not fully replace synchrotron-based μXRF, it will bridge the gap between what is currently possible in the laboratory environment and the capability of synchrotron facilities. The accessibility of such instrumentation at home institutions, as opposed to competitive access schemes at synchrotron facilities, offers exciting perspectives for studying the phytometallome into the future.

References

1. S. James, A. van der Ent and H. H. Harris, Tracking Metal Ions in Biology using X-ray Methods, Encycl. Inorg. Bioinorg. Chem., 2019 DOI:10.1002/9781119951438.eibc2692.
2. A. van der Ent, W. J. Przybyłowicz, M. D. de Jonge, H. H. Harris, C. G. Ryan, G. Tylko, D. J. Paterson, A. D. Barnabas, P. M. Kopittke and J. Mesjasz-Przybyłowicz, X-ray elemental mapping techniques for elucidating the ecophysiology of hyperaccumulator plants, New Phytol., 2018, 218, 432–452.
3. P. M. Kopittke, T. Punshon, D. J. Paterson, R. V. Tappero, P. Wang, F. P. C. Blamey, A. van der Ent and E. Lombi, Synchrotron-Based X-Ray Fluorescence Microscopy as a Technique for Imaging of Elements in Plants, Plant Physiol., 2018, 178(2), 507–523.
4. A. van der Ent, R. D. Reeves, A. J. M. Baker, J. Pollard and H. Schat, Hyperaccumulators of metal and metalloid trace elements: facts and fiction, Plant Soil, 2013, 362(1–2), 319–334.
5. R. D. Reeves, A. J. M. Baker, T. Jaffré, P. D. Erskine, G. Echevarria and A. van der Ent, A global database for hyperaccumulator plants of metal and metalloid trace elements, New Phytol., 2017, 218, 407–411.
6. P. M. Kopittke, E. Lombi, A. van der Ent, P. Wang, J. S. Laird, K. L. Moore, D. P. Persson and S. Husted, Methods to visualize elements in plants, Plant Physiol., 2020 DOI:10.1104/pp.19.01306.

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