Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting?

Abstract

The term “hyperaccumulator” describes a number of plants that belong to distantly related families, but share the ability to grow on metalliferous soils and to accumulate extraordinarily high amounts of heavy metals in the aerial organs, far in excess of the levels found in the majority of species, without suffering phytotoxic effects. Three basic hallmarks distinguish hyperaccumulators from related non-hyperaccumulating taxa: a strongly enhanced rate of heavy metal uptake, a faster root-to-shoot translocation and a greater ability to detoxify and sequester heavy metals in leaves. An interesting breakthrough that has emerged from comparative physiological and molecular analyses of hyperaccumulators and related non-hyperaccumulators is that most key steps of hyperaccumulation rely on different regulation and expression of genes found in both kinds of plants. In particular, a determinant role in driving the uptake, translocation to leaves and, finally, sequestration in vacuoles or cell walls of great amounts of heavy metals, is played in hyperaccumulators by constitutive overexpression of genes encoding transmembrane transporters, such as members of ZIP, HMA, MATE, YSL and MTP families. Among the hypotheses proposed to explain the function of hyperaccumulation, most evidence has supported the “elemental defence” hypothesis, which states that plants hyperaccumulate heavy metals as a defence mechanism against natural enemies, such as herbivores. According to the more recent hypothesis of “joint effects”, heavy metals can operate in concert with organic defensive compounds leading to enhanced plant defence overall.

Heavy metal contaminated soils pose an increasing problem to human and animal health. Using plants that hyperaccumulate specific metals in cleanup efforts appeared over the last 20 years. Metal accumulating species can be used for phytoremediation (removal of contaminant from soils) or phytomining (growing plants to harvest the metals). In addition, as many of the metals that can be hyperaccumulated are also essential nutrients, food fortification and phytoremediation might be considered two sides of the same coin. An overview of literature discussing the phytoremediation capacity of hyperaccumulators to clean up soils contaminated with heavy metals and the possibility of using these plants in phytomining is presented.

Introduction

From a chemical point of view, the term heavy metal is strictly ascribed to transition metals with atomic mass over 20 and specific gravity above 5. In biology, “heavy” refers to a series of metals and also metalloids that can be toxic to both plants and animals even at very low concentrations. Here the term “heavy metals” will be for these potentially phytotoxic elements.

Some of these heavy metals, such as As, Cd, Hg, Pb or Se, are not essential, since they do not perform any known physiological function in plants. Others, such as Co, Cu, Fe, Mn, Mo, Ni and Zn, are essential elements required for normal growth and metabolism of plants. These latter elements can easily lead to poisoning when their concentration rises to supra-optimal values. Heavy metal phytotoxicity may result from alterations of numerous physiological processes caused at cellular/molecular level by inactivating enzymes, blocking functional groups of metabolically important molecules, displacing or substituting for essential elements and disrupting membrane integrity. A rather common consequence of heavy metal poisoning is the enhanced production of reactive oxygen species (ROS) due to interference with electron transport activities, especially that of chloroplast membranes [1], [2]. This increase in ROS exposes cells to oxidative stress leading to lipid peroxidation, biological macromolecule deterioration, membrane dismantling, ion leakage, and DNA-strand cleavage [3], [4], [5]. Plants resort to a series of defence mechanisms that control uptake, accumulation and translocation of these dangerous elements and detoxify them by excluding the free ionic forms from the cytoplasm (Fig. 1). One commonly employed strategy lies in hindering the entrance of heavy metals into root cells through entrapment in the apoplastic environment by binding them to exuded organic acids [6] or to anionic groups of cell walls [7], [8]. Most of the heavy metals that do enter the plant are then kept in root cells, where they are detoxified by complexation with amino acids, organic acids or metal-binding peptides and/or sequestered into vacuoles [9]. This greatly restricts translocation to the above-ground organs thus protecting the leaf tissues, and particularly the metabolically active photosynthetic cells from heavy metal damage. A further defence mechanism generally adopted by heavy metal-exposed plants is enhancement of cell antioxidant systems which counteracts oxidative stress [4], [10].

It is interesting to notice that there are plants that survive, grow and reproduce on natural metalliferous soils as well as on sites polluted with heavy metals as a result of anthropogenic activities. The majority of species that tolerate heavy metal concentrations that are highly toxic to the other plants behave as “excluders” (Fig. 1), relying on tolerance and even hypertolerance strategies helpful for restricting metal entrance. They retain and detoxify most of the heavy metals in the root tissues, with a minimized translocation to the leaves whose cells remain sensitive to the phytotoxic effects [9]. Nevertheless, a number of hypertolerant species, defined as “hyperaccumulators”, exhibit an opposite behaviour as far as heavy metal uptake and distribution in the plant is concerned (Fig. 1).