Simulated herbivory enhances Cd phytoextraction efficiency of sunflowers

Background: Metal hyperaccumulators are plant species that can uptake and store high concentrations of heavy metals in their aboveground tissues, while maintaining high vigor. Hyperaccumulation of metals was suggested to provide defense against natural enemies such as herbivores. However, heavy-metal uptake can incur physiological and ecological costs, suggesting that, like other anti-herbivore defenses, it might be induced by herbivore attack. Nevertheless, this idea has been scarcely studied. Methods: We tested the hypothesis that herbivory could induce enhanced metal uptake in Helianthus annuus, which can accumulate high amounts of heavy metals in its aboveground tissues and is commonly used for phytoremediation of heavy-metal contaminated soils. In a greenhouse experiment, H. annuus plants were grown in low or high soil cadmium (Cd) concentration and subjected to control or herbivory treatments. Herbivory was simulated using both leaf damage and exogenous application of jasmonic acid, which activates anti-herbivore defenses in plants. Results: Simulated herbivory increased Cd concentration in the leaves of H. annuus by 24 and 39% under low and high soil Cd availability, respectively. Moreover, while simulated herbivory decreased shoot biomass of H. annuus it resulted in increased total Cd uptake. These results demonstrate that hyperaccumulation of heavy metals might be a facultative trait, whose extent can be enhanced in response to herbivore damage. Conclusions: This study provides first evidence that simulated herbivory can enhance total heavy metal uptake in plants that are used for remediation of contaminated soils, which can have important implications on the optimization of phytoremediation practices.