Evolutionary aspects of elemental hyperaccumulation

Abstract

Hyperaccumulation is the uptake of one or more metal/metalloids to concentrations greater than 50-100× those of the surrounding vegetation or 100-10,000 mg/kg dry weight depending on the element. Hyperaccumulation has been documented in at least 515 taxa of angiosperms. By mapping the occurrence of hyperaccumulators onto the angiosperm phylogeny, we show hyperaccumulation has had multiple origins across the angiosperms. Even within a given order, family or genus, there are typically multiple origins of hyperaccumulation, either for the same or different elements. We address which selective pressures may have led to the evolution of hyperaccumulation and whether there is evidence for co-evolution with ecological partners. Considerable evidence supports the elemental-defense hypothesis, which states that hyperaccumulated elements protect the plants from herbivores and pathogens. There is also evidence that hyperaccumulation can result in drought stress protection, allelopathic effects or physiological benefits. In many instances, ecological partners of hyperaccumulators have evolved resistance to the hyperaccumulated element, indicating co-evolution. Studies on the molecular evolution of hyperaccumulation have pinpointed gene duplication as a common cause of increased metal transporter abundance. Hypertolerance to the hyperaccumulated element often relies upon chelating agents, such as organic acids (e.g., malate, citrate) or peptide/protein chelators that can facilitate transport and sequestration. We conclude the review with a summary and suggested future directions for hyperaccumulator research.