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Leaf mineral composition, the leaf ionome, reflects the complex interaction between a plant and its environment including local soil composition, an influential factor that can limit species distribution and plant productivity. Here we addressed within-species variation in plant–soil interactions and edaphic adaptation using Arabidopsis halleri, a well-suited model species as a facultative metallophyte and metal hyperaccumulator. We conducted multi-element analysis of 1972 paired leaf and soil samples from 165 European populations of A. halleri, at individual resolution to accommodate soil heterogeneity. Results were further confirmed under standardized conditions upon cultivation of 105 field-collected genotypes on an artificially metal-contaminated soil in growth chamber experiments. Soil-independent between- and within-population variation set apart leaf accumulation of zinc, cadmium and lead from all other nutrient and nonessential elements, concurring with differential hypothesized ecological roles in either biotic interaction or nutrition. For these metals, soil–leaf relationships were element-specific, differed between metalliferous and non-metalliferous soils and were geographically structured both in the field and under standardized growth conditions, implicating complex scenarios of recent ecological adaptation. Our study provides an example and a reference for future related work and will serve as a basis for the molecular–genetic dissection and ecological analysis of the observed phenotypic variation.

The cadmium (Cd) hyperaccumulator Sedum alfredii has been identified to have great ability to accumulate >100 ppm (dry weight) of Cd in its aboveground biomass. However, little attention has been paid to the possibility that S. alfredii may benefit from this trait. Here, we investigated the effect of Cd accumulation on the performance of the black bean aphid Aphis fabae in S. alfredii . The results showed that 6 weeks of Cd exposure prevented S. alfredii from being infested by aphids. In another experiment, S. alfredii was pretreated with 100 μmol⋅dm⁻³ CdCl 2 for 7 days. Prolonged Cd exposure significantly reduced the number of aphids in the Cd-pretreated S. alfredii after 7 days of aphid infestation. The Cd concentration in the phloem exudates of S. alfredii was also high. Micro X-ray fluorescence mapping of aphids collected from Cd-treated plants revealed high levels of Cd in the stylets. In summary, Cd protects S. alfredii from A. fabae through toxicity, but not deterrence, which may be related to the abundance of Cd in the phloem.

BACKGROUND AND AIMS: We characterized the relationship between soil and leaf concentrations of selenium in a hyperaccumulator and a non-accumulator to test the hypothesis that hyperaccumulators take up selenium while non-accumulators exclude it. We examined plant performance metrics and the ability of selenium to protect against herbivory by spider mites. METHODS: Known hyperaccumulator and non-accumulator species within the genus Astragalus were grown under a range of selenium concentrations and measured for tissue selenium, extent of herbivory, and vigor. RESULTS: Both hyperaccumulators and non-accumulators either failed to meet even the lenient threshold or exceeded even the strict threshold for hyperaccumulation depending on soil concentration. Both had decreased herbivory with increasing leaf selenium, and both grew larger at higher levels of selenium regardless of herbivory, despite a negative impact of higher relative uptake. CONCLUSIONS: The relationships between selenium dosage and tissue concentrations matched only some model predictions. Under these conditions, the bioconcentration factor was a better delimiter between species than the absolute tissue concentration. We provide evidence that despite the apparent cost of uptake, selenium can enhance the growth of hyperaccumulators even when herbivory is not a significant factor. We propose the term “elemental stimulation” for this phenomenon.

Heavy metals are an important class of pollutants with both lethal and sublethal effects on organisms. The latter are receiving increased attention, as these may have harmful ecological outcomes. For example, recent explorations of heavy metals in freshwater habitats reveal that they can modify chemical communication between individuals, resulting in “info-disruption” that can impact ecological relationships within and between species. Info-disruption can affect animal behavior and social structure, which in turn can modify both intraspecies and interspecies interactions. In terrestrial habitats, info-disruption by metals is not well studied, but recent demonstrations of chemical signaling between plants via both roots and volatile organic molecules provide potential opportunities for info-disruption. Metals in terrestrial habitats also can form elemental plant defenses, in which they can defend a plant against natural enemies. For example, hyperaccumulation of metals by terrestrial plants has been shown to provide defensive benefits, although in almost all known cases the metals are not anthropogenic pollutants but are naturally present in soils inhabited by these plants. Info-disruption among microbes is another arena in which metal pollutants may have ecological effects, as recent discoveries regarding quorum sensing in bacteria provide an avenue for metals to affect interactions among bacteria or between bacteria and other organisms. Metal pollutants also may influence immune responses of organisms, and thus affect pathogen/host relationships. Immunomodulation (modification of immune system function) has been tied to some metal pollutants, although specific metals may boost or reduce immune system function depending on dose. Finally, the study of metal pollutants is complicated by their frequent occurrence as mixtures, either with other metals or with organic pollutants. Most studies of metal pollutants focus on single metals and therefore oversimplify complex field conditions. Study of pollutant impacts on chemical ecology also are difficult due to the necessity of studying effects at varying ecological scales: “dynamic scaling” of chemical ecology studies is rarely done completely. It is clear that much remains to be learned about how heavy metal pollution impacts organisms, and that exciting new research frontiers are available for experimental exploration.

The effects of metals on plants and herbivores, as well as the interaction among the latter, are well documented. However, the effects of simultaneous herbivory and metal accumulation remain poorly studied. Here, we shed light on this topic by infesting cadmium‐accumulating tomato plants (Solanum lycopersicum), either exposed to cadmium or not, with herbivorous spider mites, Tetranychus urticae or T. evansi during 14 days. Whereas on plants without cadmium T. evansi had higher growth rate than T. urticae, on plants with cadmium both mite species had similar growth rates, which were lower than on plants without metal. Plants were affected by both cadmium toxicity and by herbivory, as shown by leaf reflectance, but not on the same wavelengths. Moreover, changes in leaf reflectance on the wavelength affected by herbivores were similar on plants with and without cadmium, and vice versa. Long‐term effects of cadmium and herbivory did not affect H2O2 concentrations in the plant. Finally, plants infested with spider mites did not accumulate more cadmium, suggesting that metal accumulation is not induced by herbivory. We thus conclude that cadmium accumulation affects two congeneric herbivore species differently and that the effects of herbivory and cadmium toxicity on plants may be disentangled, via leaf reflectance, even during simultaneous exposure. Infestation with spider mites does not lead to higher cadmium accumulation in tomato plants, despite this metal negatively affecting the herbivores. Simultaneous exposure to metals and herbivores leads to distinct effects on plant physiology that can be detected through leaf spectral reflectance.

Extraordinarily high leaf metal concentrations in metal hyperaccumulator plants may serve as an elemental defence against herbivores. However, mixed results have been reported and studies using comparative approaches are missing. We investigated the deterrent and toxic potential of metals employing the hyperaccumulator Arabidopsis halleri. Effects of zinc (Zn) and cadmium (Cd) on the preferences of three Brassicaceae specialists were tested in paired-choice experiments using differently treated plant material, including transgenic plants. In performance tests, we determined the toxicity and joint effects of both metals incorporated in an artificial diet on the survival of a generalist. Feeding by all specialists was significantly reduced by metal concentrations from above 1000 μg Zn g−1 DW and 18 μg Cd g−1 DW. By contrast, metals did not affect oviposition. Generalist survival decreased with increasing concentrations of individual metals, whereby the combination of Zn and Cd had an additive toxic effect even at the lowest applied concentrations of 100 μg Zn g−1 and 2 μg Cd g−1. Metal hyperaccumulation protects plants from herbivory resulting from deterrence and toxicity against a wide range of herbivores. The combination of metals exacerbates toxicity through joint effects and enhances elemental defence. Thus, metal hyperaccumulation is ecologically beneficial for plants.

Soil pollution by metals and metalloids as a consequence of anthropogenic industrialisation exerts a seriously damaging impact on ecosystems. However, certain plant species, termed hyperaccumulators, are able to accumulate extraordinarily high concentrations of these metal(loid)s in their aboveground tissues. Such hyperaccumulation of metal(loid)s is known to act as a defence against various antagonists, such as herbivores and pathogens. We investigated the influences of metal(loid)s on potential defence traits, such as foliar elemental, organic and mechanical defences, in the hyperaccumulator plant species Arabidopsis halleri (Brassicaceae) by artificially amending the soil with common metallic pollutants, namely cadmium (Cd) and zinc (Zn). Additionally, unamended and metal-amended soils were supplemented with the metalloid silicon (Si) to study whether Si could alleviate metal excess. Individuals originating from one non-/low- and two moderately to highly metal-contaminated sites with different metal concentrations (hereafter called accessions) were grown for eight weeks in a full-factorial design under standardised conditions. There were significant interactive effects of metal amendment and Si supplementation on foliar concentrations of certain elements (Zn, Si, aluminium (Al), iron (Fe), potassium (K) and sulfur (S), but these were accession-specific. Profiles of glucosinolates, characteristic organic defences of Brassicaceae, were distinct among accessions, and the composition was affected by soil metal amendment. Moreover, plants grown on metal-amended soil contained lower concentrations of total glucosinolates in one of the accessions, which suggests a potential trade-off between inorganic defence acquisition and biosynthesis of organic defence. The density of foliar trichomes, as a proxy for the first layer of mechanical defence, was also influenced by metal amendment and/or Si supplementation in an accession-dependent manner. Our study highlights the importance of examining the effects of co-occurring metal(loid)s in soil on various foliar defence traits in different accessions of a hyperaccumulating species.

Elemental defense is a relatively newly recognized phenomenon in which plants use elements present in their tissue to reduce damage by herbivores or pathogens. In the present study, neonates of the generalist herbivore, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) , were fed artificial diets amended with varying concentrations of Co, Cu, Ni, and Zn that are hyperaccumulated by plants to determine minimum lethal concentrations (MLC) and minimum sublethal concentrations (MSC) for each metal. MLC values (dry mass) for Co (45 μg/g), Ni (230 μg/g), and Zn (280 μg/g) were below published minimum hyperaccumulator levels. MSC levels (dry mass) for Co (15 μg/g), Ni (140 μg/g), and Zn (200 μg/g) were at concentrations lower than published minimum accumulator levels. Furthermore, both MLC and MSC values for Zn were within normal tissue concentrations. These results indicate that elemental defense for Co, Ni, and Zn may be effective at concentrations lower than hyperaccumulator levels and so may be more widespread than previously believed.

To investigate whether selenium (Se) accumulation in plants provides a chemical defense against generalist insect herbivores, the feeding preference and performance of a mix of orthopteran species were investigated. The selenium hyperaccumulator Stanleya pinnata and accumulator Brassica juncea were used in herbivory studies in the laboratory, and S. pinnata was also used in a manipulative field experiment. In laboratory studies, both crickets and grasshoppers avoided plants pretreated with selenate, while those given no choice died after eating leaves with elevated Se (447 ± 68 and 230 ± 68 μg Se g⁻¹ DW, respectively). B. juncea has previously been shown to accumulate selenate, while S. pinnata hyperaccumulates methyl-selenocysteine. Thus, these findings demonstrate that both inorganic and organic forms of selenium protect plants from herbivory. Grasshoppers fed S. pinnata contained methylselenocysteine in their midgut and absorbed this form into surrounding tissues. In a manipulative field experiment, methylselenocysteine protected S. pinnata from invertebrate herbivory and increased its long-term survival rate over an entire growth season. In native habitats of selenium hyperaccumulators, orthopterans represent a major group of insect herbivores. Protection offered by organic selenium accumulation against these herbivores may have promoted the evolution of selenium hyperaccumulation in plants.