Stable Isotope Fractionation of Metals and Metalloids in Plants: A Review

Abstract

This work critically reviews stable isotope fractionation of essential (B, Mg, K, Ca, Fe, Ni, Cu, Zn, Mo), beneficial (Si), and non-essential (Cd, Tl) metals and metalloids in plants. The review (i) provides basic principles and methodologies for non-traditional isotope analyses, (ii) compiles isotope fractionation for uptake and translocation for each element and connects them to physiological processes, and (iii) interlinks knowledge from different elements to identify common and contrasting drivers of isotope fractionation. Different biological and physico-chemical processes drive isotope fractionation in plants. During uptake, Ca and Mg fractionate through root apoplast adsorption, Si through diffusion during membrane passage, Fe and Cu through reduction prior to membrane transport in strategy I plants, and Zn, Cu, and Cd through membrane transport. During translocation and utilization, isotopes fractionate through precipitation into insoluble forms, such as phytoliths (Si) or oxalate (Ca), structural binding to cell walls (Ca), and membrane transport and binding to soluble organic ligands (Zn, Cd). These processes can lead to similar (Cu, Fe) and opposing (Ca vs. Mg, Zn vs. Cd) isotope fractionation patterns of chemically similar elements in plants. Isotope fractionation in plants is influenced by biotic factors, such as phenological stages and plant genetics, as well as abiotic factors. Different nutrient supply induced shifts in isotope fractionation patterns for Mg, Cu, and Zn, suggesting that isotope process tracing can be used as a tool to detect and quantify different uptake pathways in response to abiotic stresses. However, the interpretation of isotope fractionation in plants is challenging because many isotope fractionation factors associated with specific processes are unknown and experiments are often exploratory. To overcome these limitations, fundamental geochemical research should expand the database of isotope fractionation factors and disentangle kinetic and equilibrium fractionation. In addition, plant growth studies should further shift toward hypothesis-driven experiments, for example, by integrating contrasting nutrient supplies, using established model plants, genetic approaches, and by combining isotope analyses with complementary speciation techniques. To fully exploit the potential of isotope process tracing in plants, the interdisciplinary expertise of plant and isotope geochemical scientists is required.

From soil to cacao bean: Unravelling the pathways of cadmium translocation in a high Cd accumulating cultivar of Theobroma cacao L

“…The Cd in the cacao plant was lighter than in the Ca(NO 3 ) 2extractable soil pool (Figure 1 and Table 3), indicating that preferentially light Cd isotopes were taken up from the soil. The isotope fractionation found in this study was similar to previous studies [D 114/110 Cd plant-source 0.00 to -0.45‰ (Wiggenhauser et al, 2022)], even though these values origin not only from cacao and were obtained in soils with distinct soil properties, including soil pH. The similar isotope fractionation for plant Cd uptake in previous studies and our acidic soil-cacao system suggests that Cd uptake mechanisms may be very similar in distinct soil-plant systems.…”

“…The transfer of Cd from root to aerial tissues was high (ITF leaf-root ≈1, Table 2), as observed in other studies on cacao plantations (Vanderschueren et al, 2021). The isotope fractionation revealed that the cacao surface roots in this study were enriched in light isotopes compared to above-ground parts (Figure 1), as observed in wheat, barley, rice, cacao, and a Cd accumulator plant (Solanum nigrum) (D 114/110 Cd shoot-root 0.00 to 0.50 ‰ (Wiggenhauser et al, 2022)). Other crops such as cereals translocate much less Cd from root to shoot (ITF root-shoot <0.05) (McLaughlin et al, 2011).…”

Translocation of elements and fractionation of Mg, Cu, Zn, and Cd stable isotopes in a penny bun mushroom (Boletus edulis) from western Czech Republic

“…As of now, we cannot say with certainty why these two isotope systems behaved the way observed. Although isotopically distinguishable Mg pools were reported to exist in vascular plants (Pokharel et al 2018;Wiggenhauser et al 2022), there are no obvious reasons for the presence of such pools in the studied mushroom sample. We can exclude influence of the selective contamination because all mushroom subsamples were prepared simultaneously by the same way, and were cleaned of all debris (mineral and organic) very carefully.…”

“…Analyses revealed preferential uptake of the lighter 63 Cu isotope by the mushroom. For redox sensitive transition metals such as Cu, reduction can be required prior to the uptake, and significant light Cu isotopic enrichment would be due to the reduction of free Cu 2+ to Cu + (see Criss 1999;Zhu et al 2002;Kavner et al 2008;Navarette et al 2011;Weinstein et al 2011;Jouvin et al 2012;Ryan et al 2013;Li et al 2016;Blotevogel et al 2022;Wiggenhauser et al 2022). Therefore, observed significant negative Cu isotope fractionation between the substrate and the B. edulis fruiting body (Δ 65 Cu stipe(0-3)-soil = −1.14‰; Δ 65 Cu fruiting body-soil = -0.96‰) (Fig.…”

“…Not only redox-induced, but also kinetic isotope fractionation could contribute to the enrichment of biological systems with the lighter 63 Cu isotope (Hindshaw et al 2013). Such fractionation may be due to the change of active Cu uptake to passive Cu uptake because of increased element availability (see Blotevogel et al 2022;Wiggenhauser et al 2022). This, however, unlikely occurs at low exposure to Cu, which was the case for the studied catchment (Table 2).…”