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Keywords:

  • biofortification;
  • elemental contaminants;
  • ionome;
  • phylogenetic effects;
  • stoichiometry

Since early metallurgy the ores for smelting were probably located with the help of botanical prospecting – ‘leadworts’ and ‘zinc violets’ of Europe, for example, suggest long-known links between soil composition and plant distribution. It was recognized that plants did not just tolerate particular substances but accumulated high concentrations of them – ‘glassworts’ of saline soils, for example, provided high concentrations of soda ash used for glass making. Such dramatic links have perhaps helped to obscure the fact that the elemental composition of a plant species, ‘its ionome’, can be surprisingly constant despite it growing on different soils. Plant ionomes are determined by both the elemental composition of the environment and plant characteristics that affect the uptake of elements. In this issue of New Phytologist, White et al. (pp. 101–109) report the most experimentally rigorous comparison thus far of these influences on plant ionomes.

‘We are what we eat and White et al. 's analyses suggest that the plants we eat might have ionomes that at least in part resist fertilizer regimes.’

Taxonomically-informed analyses of plant ionomes have improved significantly with the availability of new molecular phylogenies of plants. Experimental designs have included growing taxonomically divergent species under one set of conditions (Broadley et al., 2004), sampling from botanic gardens (Watanabe et al., 2007) or using Residual Maximum Likelihood modelling in meta-analyses of data (Broadley et al., 2001; Willey & Wilkins, 2008). In each of these designs variation due to external environment is minimized and there has been no previous experiment specifically to test simultaneously the effect of environment and plant characteristics on plant ionomes. There is increasing evidence that plant characters affect the ionome but how this compares to environmental effects has not been clear. White et al., writing from the James Hutton Institute in Scotland, show that plant characters exert significant control over plant ionomes even when elemental differences in the environment are sustained over many years. In the early twentieth century the steel workers of Scotland were famously encouraged to drink a still very successful, non-alcoholic alternative to beer which became known as ‘Irn-Bru’. The work of White et al. is a significant step forward in understanding the ion-brew of plants.

Human mobilization of elements in the environment started early but accelerated in the twentieth century (Lee et al., 2008). The contamination of natural and agricultural environments with elemental toxins, in particular cadmium (Cd) and arsenic (As) but also many others, significantly affects biomass production and/or quality. Plant ionomics might improve significantly the understanding and management of elemental toxins in both natural and agricultural ecosystems. Cadmium, one the most problematic elemental contaminants for human health, has chemical similarities to zinc (Zn) which is included in White et al.'s analysis. Strontium-90 (90Sr) and caesium-137 (137Cs) blight the Chernobyl exclusion zone, and 137Cs the Fukushima exclusion zone, and crop plants inadvertently take up these radioisotopes from soil as if they were calcium (Ca) and potassium (K) – two other elements for which White et al. have quantified ionome effects.

Plant ionomics is even more important for managing flows of nutrient elements in crops. We are what we eat and White et al.'s analyses suggest that the plants we eat might have ionomes that at least in part resist fertilizer regimes. Understanding crop ionomes is particularly useful for micronutrient management because several hundred million people on Earth are deficient in iron (Fe), Zn or selenium (Se) in significant part because of low dietary intake. Efforts to enhance the micronutrient ionomes of crop plants, that is, to biofortify them, especially in Fe and Zn which are included in White et al.'s analysis, might benefit from understanding how variation in the ionome arises. In their data Zn concentrations in plants were surprisingly resistant to fertilizer regime.

Plant ionomics might also have implications for elemental enrichment of natural ecosystems. Biomass production in natural ecosystems is frequently limited by nutrient availability, perhaps most often by nitrogen (N) or phosphorus (P), but also in, for example, high Ca soils by lack of Fe. One of the main conclusions of experiments on the effects of increasing CO2 or temperature on plants is that the effects often depend on nutrient dynamics. Understanding variation in the ionomes of plants might help us to better understand the biogeochemical cycling of the elements in terrestrial ecosystems and thus what impacts our inputs to them might have. Interestingly, the element concentration least resistant to environmental perturbation in White et al.'s, and in data of others, is P – whose input into the environment causes more environmental impact than any of the other elements they analysed.

The work of White et al. increases significantly the evidence that there is genuine biodiversity in the ionome, that is, variation that arises because of plant characters despite sustained differences in environmental factors. The Park Grass Continuous Hay experiment at Rothamsted (UK) was initiated in 1865 with plots of different fertilizer regime. Liming of some plots started in 1903, with liming to particular pHs introduced in 1965. White et al.'s analyses of the ionomes of 21 meadow species from plots limed to pH 7 for about four decades but contrasting fertilizer regimes for well over a century reveal significant plant effects on some elemental concentrations, plant × treatment effects for others and for some elements the dominant effects of treatments. White et al. not only provide significant support for the existence of ionomic biodiversity but also provide a taste of how we might use it. Ionomic biodiversity is potentially a mixed blessing – it provides raw material for manipulating crop ionomes and it is important to know for modelling of diverse ecosystems that plants do not all behave as the same black box, but unless we can quantify the biodiversity it might be easier if it did not exist. It is the taxonomic effects, and perhaps ultimately the phylogenetic effects, in ionomic data that might make it useful.

White et al.'s data suggest that taxonomic patterns of Ca and magnesium (Mg) concentrations are particularly clear, as they are in other datasets, and remain so despite decades of differential fertilizer and lime application (Fig. 1). In many parts of the world digitized high-resolution maps of geological and pedological variables enable much better descriptions of the environmental factors that contribute to plant ionome variability than we can make of the plant variables that contribute. Now we know there are taxonomic effects, on Ca, Mg and other elements, it might be possible to use them to predict the plant contribution to ionomes. It seems clear now that variation in Ca and Mg concentrations are constrained above the species level. White et al. used families to explain some of the effect on Ca and Mg but we are only just beginning to understand whereabouts in the taxonomic hierarchy the variation occurs because the data sets available include at most a few hundred species. The existence of increasingly detailed molecular phylogenies raises the hope that if large datasets of elemental concentrations are generated then a phylogenetic understanding of constraints on the ionome may be possible. Such effects might guide us as we try to mine the ionome for useful biodiversity in crop improvement. It might also enable us to refine predictions of elemental flows in natural ecosystems – White et al.'s conclusions reinforce previous suggestions that such predictions might be based on plant phylogeny (Willey, 2010). These constraints are likely to guide the identification of the mechanisms controlling plant effects on the ionome.

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Figure 1. White et al.'s analyses (this issue of New Phytologist, pp. 101–109) suggest that especially for calcium (Ca) and magnesium (Mg), but also several other elements, the contrasting ionomes reported in, for example, members of the Poaceae (Miscanthus spp.; a) and the Caryophyllales (Beta vulgaris subsp. cicla; b) are robust to environmental effects and arise from characters found at the family level and above.

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Understanding plant ionomes is also likely to be more widely useful to understanding Earth's terrestrial ecosystems. Wallace (1858), in some of the first writing to articulate the process of natural selection, noted that for plants adapting to their environments ‘nothing can be more abrupt than the change often due to diversity of soil, a sharp line dividing a pine- or heather-clad moor from calcareous hills.’. It has been suggested that for plants the exemplar of speciation by adaptation to local environment is adaption to particular soils. Metalliferous soils exemplify this – the serpentine soils of New Caledonia are thought to have a high number of plant endemics not just because of the island's long isolation but also because of the particular challenges its soils present. Its flora is, however, disharmonic, that is, particular taxonomic groups are overrepresented, which is thought to be because some plants dispersed to the island had exaptations that predisposed them to its soils (Pillon et al., 2010). The main challenge to plant life on ultramafic serpentine soils is their very high Mg concentration which produces a Ca:Mg ratio inimical to most plants. In fact the mafic rocks that are produced by emergent magma, for example basalts and gabbros, are distinguished from intrusive felsic rocks, such as granite, in part by their Mg and Ca concentrations and ratios. Perhaps plant ionomics and elemental ratios of rocks and soils might provide new insights into ecological filtering and the development of terrestrial ecosystems. It would also be interesting to explore the ionomic links to ecological stoichiometry (Jeyasingh & Weider, 2007) and to cellular distributions of elements (Conn & Gilliham, 2010). Humans are still, perhaps more than they remember, beholden to the elements of Earth. In the plant species investigated so far it now really seems that a combination of plant and environmental factors control ionomes. If this applies across the plant kingdom it has agricultural and ecological implications.

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