The role of biotic interactions in determining metal hyperaccumulation in plants

Abstract

Heavy metal hyperaccumulation (MH) is a rare trait found in plant species that inhabit metal‐contaminated soils. Two main hypotheses proposed to explain the selective advantage of MH are the elemental defence hypothesis and elemental allelopathy hypothesis. The elemental defence hypothesis suggests that MH functions as defence against herbivores while the elemental allelopathy hypothesis suggests that MH acts to inhibit the growth of neighbours. Nevertheless, these hypotheses are not likely to be mutually exclusive. Here, we present the first study to test both hypotheses simultaneously. We examined these hypotheses with the Cd hyperaccumulator, Arabidopsis halleri, which inhabits both metalliferous and non‐metalliferous soils, thus providing an opportunity to test the hypotheses of both habitats. Arabidopsis halleri plants originating from several populations in both metalliferous and non‐metalliferous soils were grown in a greenhouse in soils with or without cadmium (Cd). Their leaves were used in a feeding experiment with a specialist herbivore and in a set of leaf‐leachate experiments that tested their effect on seed germination and seedling establishment of species co‐occurring with A. halleri. Finally, a field survey in several A. halleri populations was conducted to compare herbivore load between A. halleri and neighbours from metalliferous versus non‐metalliferous soils. Results of the feeding experiment and field survey suggest that Cd accumulation in A. halleri leaves could provide it with defence against herbivores. Results of the leaf‐leachate experiments reveal that Cd accumulation has no effect on seed germination of neighbouring species but inhibits seedling establishment, particularly of plant species originating from non‐metalliferous soils. Our results suggest that both herbivores and competing neighbours may jointly select for MH in plants. Moreover, MH could provide a selective advantage particularly in non‐metalliferous soils, where neighbouring plants lack metal tolerance. These results highlight the importance of including different origins and populations of both the target species and its neighbouring plant species when studying the ecological role of MH. A free Plain Language Summary can be found within the Supporting Information of this article.

Interspecific trait integration increases with environmental harshness: A case study along a metal toxicity gradient

“…This suggests a tradeoff between interspecific competitive ability and metal accumulation (Ernst et al, 1992); the sequestration of metal in the plant could incur a cost that would not allow larger species to reach reproductive maturity in a short growing season. However, this result could also support the idea that leaf metal accumulation is a mechanism of biotic interaction (allelopathy) that would benefit poorly competitive, small species (Mohiley, Tielbörger, Seifan, & Gruntman, 2020). There were only moderate interspecific correlations between leaf metal concentrations and LES traits, potentially indicating that the physiological mechanisms required for metal tolerance within the leaves do not interact with resources use.…”

Between the devil and the deep blue sea: herbivory induces foraging for and uptake of cadmium in a metal hyperaccumulating plant

“…Specifically, we asked if responses to herbivory differ between plants from metalliferous versus non-metalliferous origin. A. halleri from both these origins have been shown to hyperaccumulate Cd [ 19 , 22 , 23 ]. However, results from a previous study with the same genotypes used in this study showed that A. halleri from a non-metalliferous origin are less tolerant to high concentrations of Cd in their tissues and showed markedly reduced growth when grown in Cd-rich soils, while plants from metalliferous soil were not affected [ 22 ].…”

“…A number of such plant species can be found in the Brassicaceae family that hyperaccumulate heavy metals such as zinc (Zn), cadmium (Cd) or nickel (Ni) up to 100-1000-fold higher than those found in non-hyperaccumulating species [15]. Several hypotheses have been suggested to explain why such behaviour could be beneficial, and the most common is the elemental defence hypothesis, which suggests that heavy metals could serve as herbivore defence [16][17][18][19]. Interestingly, some metal-hyperaccumulating plants have been shown to forage for heavy metals [20,21].…”

“…Specifically, we studied these responses in the metal-hyperaccumulating clonal plant Arabidopsis halleri. This species can accumulate large concentrations of heavy metals (Zn and Cd) in its shoots and leaves [16][17][18], and these have been shown to deter herbivores [16,17,19]. In a first experiment, we asked whether simulated herbivore damage induces root foraging for Cd within ramets by studying root allocation in a 'split-root' design between Cd-rich and Cd-poor patches (figure 1).…”

Competition for light induces metal accumulation in a metal hyperaccumulating plant

“…An example for such plants are metal hyperaccumulating species, which actively uptake excessive concentrations of heavy metals into their aboveground tissues (Krämer 2010). Metal hyperaccumulation has been found to be important as herbivore defence (the elemental defence hypothesis: Kazemi-Dinan et al 2014;Plaza et al 2015) as well as provide plants with allelopathic abilities (the elemental allelopathy hypothesis: Morris et al 2009;Mohiley et al 2020). Allelopathic effects could be conveyed in these plants when their metal-enriched leaves are shed, and as a result increase the heavy metal concentration around them and inhibit the germination and growth of metal sensitive neighbouring species (Boyd and Jaffré 2001;El Mehdawi et al 2011Jaffe et al 2018).…”