Figure 1.

A more physiologically and evolutionarily relevant conceptual framework for the study of variation in the distinct physiological traits of metal accumulation and tolerance. Both traits are continuous, and plant phenotypes span a wide range of combinations of both traits. Traditional hyperaccumulators are those with both high accumulation and high tolerance (Quadrant I; e.g., Astragalus bisculcatus for selenium; (El Mehdawi et al., 2011)). Species with high accumulation of specific metals, but low tolerance to those metals, are also known to exist but are excluded from the naturalistic definition of hyperaccumulation (Quadrant II; e.g., Thlaspi goesingense for zinc; (Lombi et al., 2000)). Most plants are neither tolerant nor accumulate (Quadrant III; e.g., Arabidopsis thaliana for cadmium; (Hanikenne et al., 2008)), though many species are known to be tolerant of metal exposure while not accumulating (Quadrant IV; e.g., Silene vulgaris for copper; (van Hoof et al., 2001)). Both groups (III) and (IV) are typically collapsed together as non-hyperaccumulators, which is accurate, but fails to capture the important distinction and its relevance to the colonization of metal-rich soils and likely importance in hyperaccumulator evolution. Explicitly considering both tolerance and accumulation as separate traits is key to the study of hyperaccumulator physiology and evolution.