Metallophytes—a view from the rhizosphere

Some plants hyperaccumulate metals or metalloids to levels several orders of magnitude higher than other species. This intriguing phenomenon has received considerable attention in the past decade. While research has mostly focused on the above-ground organs, roots are the sole access point to below-ground trace elements and as such they play a vital role in hyperaccumulation. Here we highlight the role of the root as an effective trace element scavenger through interactions in the rhizosphere. We found that less than 10% of the known hyperaccumulator species have had their rhizospheres examined. When studied, researchers have focused on root physical characteristics, rhizosphere chemistry, and rhizosphere microbiology as central themes to understand plant hyperaccumulation. One physical characteristic often assumed about hyperaccumulators is that their roots are small, but this is not true for all species and many species remain unexamined. Transporters in root membranes provide avenues for root uptake, while root growth and morphology influence plant access to trace elements in the rhizosphere. Some hyperaccumulators exhibit unique root scavenging and direct their growth toward elements in soil. Studies on hyperaccumulator rhizosphere chemistry have examined the role of the root in altering elemental solubility through exudation and pH changes. Different interpretations have been reported for mobilization of non-labile trace element pools by hyperaccumulators. However, there is a lack of evidence for a novel role for rhizosphere acidification in hyperaccumulation. As for microbiological studies, researchers have shown that bacteria and fungi in the hyperaccumulator rhizosphere may exhibit increased metal tolerance, act as plant growth promoting microorganisms, alter elemental solubility, and have significant effects on plant trace element concentrations. New evidence suggests that symbiosis with arbuscular mycorrhizae may not be rare in hyperaccumulator taxa, even in some members of the Brassicaceae. Although there are several reports on the presence of mycorrhizae, a cohesive interpretation of their role in hyperaccumulation remains elusive. In summary, we present the current state of knowledge about how roots hyperaccumulate and we suggest ways in which this knowledge can be applied and improved.