Metal hyperaccumulation in Brassicaceae mediates defense against herbivores in the field and improves growth

Several Brassicaceae species are able to hyperaccumulate extraordinarily high levels of heavy metals in their aboveground tissues. This rare and complex trait named metal hyperaccumulation may offer effective protection against antagonists. Several laboratory studies provide evidence that metal hyperaccumulation acts as an elemental defense. Here, we investigated whether this elemental defense can be confirmed in the field and whether plant growth is affected when plants can hyperaccumulate metals from the soil. Plants of Arabidopsis halleri (L.) O'Kane & Al-Shehbaz, which can hyperaccumulate cadmium (Cd) and zinc (Zn), were cultivated in pots in unamended (control) ormetal-amended soil (test) for 2 months. The pots containing the plants were then transferred to a common garden. Leaf-damaging insect visitors were monitored over a period of 3 months. Plant size and shoot mass were measured directly before and at the end of the field exposure. Furthermore, before and at the end of the field exposure we determined leaf concentrations of Cd and Zn, as well as glucosinolates, which are characteristic secondary metabolites of the Brassicaceae that are known to act potentially as organic defense compounds. Growth of the test plants on metal-amended soil led to a significant increase in leaf Cd and Zn concentrations when compared to control plants on unamended soil. After two initial months of growth under standardized greenhouse conditions, plants grown on different soils did not differ in size or biomass. In contrast, by the end of the 3-month field exposure, test plants were larger than control plants. During field exposure, control plants were visited by more herbivores, suggesting that plants growing on metal-amended soil were well defended against herbivores. Total glucosinolate concentrations were significantly higher in test compared to control plants only after the initial growth period under standardized conditions, but not by the end of the field exposure, pointing to joint effects of defenses particularly in young plants. Our results demonstrate that metal hyperaccumulation affords an effective elemental defense and enables increased growth under field conditions.