ReviewFacultative hyperaccumulation of heavy metals and metalloids
Introduction
The interaction of plants with toxic metal and metalloid elements in soils has been used as a productive model for physiological, ecological, genetic and evolutionary research for over half a century. Although many such elements are essential micronutrients, most are toxic at high concentrations. The early studies in this field focused on tolerance mechanisms that allow some plants to grow in metal-contaminated soils where most species cannot survive [1]. More recent interest has centered on a small subset of these plants that not only tolerate metals, but also concentrate them to exceptional concentrations in their leaves, the phenomenon of hyperaccumulation [2], [3]. Both tolerance and hyperaccumulation may have commercial applications, whether for revegetation of contaminated soils (phytostabilization), for extraction of metals for their intrinsic value (phytomining), or for plant-based remediation of polluted soils (phytoextraction) [4], [5].
This review focuses on metal hyperaccumulator species that occur naturally on both metalliferous and non-metalliferous soils. Such species may broadly be described as facultative hyperaccumulators, a classification which will be explained more fully in Section 2.1. Facultative hyperaccumulators make up a minority of the known hyperaccumulator species and in general have been poorly studied, yet they also include a few of the most thoroughly investigated research models for metal tolerance and uptake. This paper does not attempt to comprehensively describe the biology of hyperaccumulation or its underlying genetics and physiology, which have been surveyed in other recent reviews [2], [3], [6], [7]. Instead, we will concentrate on the unique features of facultative hyperaccumulators. We will argue that ecological and evolutionary hypotheses regarding hyperaccumulating plants are expected to depend strongly on the biogeographic patterns of hyperaccumulator distribution, whether obligately restricted to metalliferous soils, primarily on metalliferous soils and occasionally on other substrates, or primarily on non-metalliferous soils but occasionally on metalliferous ones where they hyperaccumulate.
Section snippets
Defining and describing hyperaccumulators
A recent critique [7] has attempted to clarify, refine and update the definition of metal hyperaccumulation. To paraphrase its conclusions, a hyperaccumulator can be defined as a plant whose leaves contain a metallic element at a concentration exceeding a specified threshold, when growing in nature (not in experimental cultivation). The threshold concentration should be 2–3 orders of magnitude higher than in leaves of most species on normal soils, and at least one order of magnitude greater
Analysis of research on facultative hyperaccumulation
A summary of published research on facultative hyperaccumulators is presented in Table 1. We have attempted to be as comprehensive and accurate as possible, given the uncertainties in distinguishing between facultative and obligate hyperaccumulators discussed in the previous section. The table is not simply a catalog of publications, but is intended to permit analysis of how research has been distributed across taxonomic groups, geographic areas, and metals. In order to evaluate the amount of
Ecophysiology of facultative hyperaccumulation
Facultative hyperaccumulators afford opportunities for research on questions that cannot be addressed in the majority of hyperaccumulators, which are obligate metallophytes. Perhaps the most fundamental question is whether the physiological ability to tolerate and accumulate metals occurs only in plants growing on metalliferous soils, or whether it is a universal property of the species. The latter has often been described as constitutive hyperaccumulation; however, this phrase may potentially
Evolution of facultative hyperaccumulators
It has widely been assumed that hyperaccumulation of heavy metals must incur some cost to the plant, related to transport, concentration, storage and detoxification of potentially toxic elements [6], [71], [72], although quantification of these costs has been problematic. In the face of such costs, many researchers have hypothesized that there must also be some compensatory benefit selecting for the evolution of hyperaccumulation. An influential paper on this topic [73] divided these hypotheses
Conclusions
The majority of plants that hyperaccumulate heavy metals are obligately endemic to metalliferous soils, but a significant minority are facultative metallophytes, including many of the best-known research models. Facultative hyperaccumulators can be used as promising model systems for physiological and genetic research. However, previously-published evolutionary models attempting to explain the adaptive significance and selective advantage of hyperaccumulation do not apply well to facultative
Acknowledgements
We thank Jonathan Gressel and eight anonymous reviewers of an earlier version of this paper for their helpful comments.
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