Elsevier

Plant Science

Volumes 217–218, March 2014, Pages 8-17
Plant Science

Review
Facultative hyperaccumulation of heavy metals and metalloids

https://doi.org/10.1016/j.plantsci.2013.11.011Get rights and content

Highlights

  • We review research on plants that hyperaccumulate metals but also occur on low-metal soils.

  • Facultative hyperaccumulators are rare but include several well-known research models.

  • Research on facultative hyperaccumulators has focused disproportionately on a few species.

  • Future studies need to focus on plants from other phylogenetic and geographic groups.

  • We propose new hypotheses regarding the evolution of facultative hyperaccumulation.

Abstract

Approximately 500 species of plants are known to hyperaccumulate heavy metals and metalloids. The majority are obligate metallophytes, species that are restricted to metalliferous soils. However, a smaller but increasing list of plants are “facultative hyperaccumulators” that hyperaccumulate heavy metals when occurring on metalliferous soils, yet also occur commonly on normal, non-metalliferous soils. This paper reviews the biology of facultative hyperaccumulators and the opportunities they provide for ecological and evolutionary research. The existence of facultative hyperaccumulator populations across a wide edaphic range allows intraspecific comparisons of tolerance and uptake physiology. This approach has been used to study zinc and cadmium hyperaccumulation by Noccaea (Thlaspi) caerulescens and Arabidopsis halleri, and it will be instructive to make similar comparisons on species that are distributed even more abundantly on normal soil. Over 90% of known hyperaccumulators occur on serpentine (ultramafic) soil and accumulate nickel, yet there have paradoxically been few experimental studies of facultative nickel hyperaccumulation. Several hypotheses suggested to explain the evolution of hyperaccumulation seem unlikely when most populations of a species occur on normal soil, where plants cannot hyperaccumulate due to low metal availability. In such species, it may be that hyperaccumulation is an ancestral phylogenetic trait or an anomalous manifestation of physiological mechanisms evolved on normal soils, and may or may not have direct adaptive benefits.

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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