The Evolution of Metal Hyperaccumulation

Metal hyperaccumulation evolved in different, taxonomically unrelated groups of plants (Brooks 1987) and may fulfil multiple functions, both within and between the evolutionary lines of metal-hyperaccumulating plants. Physiological mechanisms are preserved if they have a functional basis that provides direct or consequential positive-selective value to the plant (Ernst 2006). Because of the accumulation of enormous amounts of potentially toxic metal levels, hyperaccumulation is a contradictory phenomenon. Direct and indirect advantages have nevertheless been seen. Six different hypotheses for the ecological benefits of hyperaccumulation in plants have been postulated (Boyd and Martens 1998):

• Inadvertent uptake hypothesis: the uptake of essential elements in nutrient-poor habitats forces plants to inadvertently take up toxic metals.

• Tolerance hypothesis: metal hyperaccumulation is a mechanism that allows the sequestration of metals in tissues.

• Disposal hypothesis: the elimination of metals from the plant body by shedding tissues containing high metal levels.

• Elemental allelopathy hypothesis: perennials enrich the surface soil under their canopies by producing high-metal litter, to prevent the establishment of less metal-tolerant species.

• Drought resistance hypothesis: hyperaccumulated metal helps the plant to withstand drought.

• Defence hypothesis: elevated metal concentrations in plant tissues protect plants from certain herbivores and pathogens.

A possible evolutionary pathway by which elemental hyperaccumulation may have evolved from accumulation is known as the "defensive enhancement scenario", where stepwise increases in the element concentration may have led to further plant benefits (see Boyd 2007). Five different modes of action for metal defences have been proposed (Poschenrieder et al. 2006a):

• Phytosanitary effects: metal-containing compounds act to prevent herbivore and pathogen attack.

• Elemental defence hypothesis: the high metal concentrations that accumulate in leaf tissues either deter or intoxicate herbivores or pathogens.

• Trade-off hypothesis: increasing tissue concentrations of potentially toxic heavy metals in plants can replace organic defences.

• Metal therapy: the metal has a therapeutic effect, preventing the consequences of the metabolic disorder responsible for stress signalling failure.

• Metal-induced fortification: metal-stress-derived signals and metal-induced activation of pathogen-resistance-related defence genes are redundant.

The toxicity of high metal concentrations to phytopathogenic microorganisms is well established. A higher metal sensitivity of the pathogen than that of the host has been used practically in the formulation of different inorganic and organic metal compounds for phytosanitary treatments. The copper-containing Burgundy mixture is a widely used example. In these cases, the protection is achieved by the direct action of the metal ion or organometallic compound supplied, without the apparent participation of the host plant.

In the trade-off hypothesis, high metal accumulation by the plant is suggested to provide protection against herbivores, and thus energy for the synthesis of plant organic defences is saved (Boyd 1998). Nickel hyperaccumulation in the European Brassicaceae species can act in this way (Davis and Boyd 2000). However, to date, there is little evidence that confirms that the trade-off hypothesis is a general mechanism driving the evolution of metal-hyperaccumulating plants (Jhee et al. 2006; Tolra et al. 2001). In contrast to organic defences, the metals are not degrad-able (Boyd and Martens 1998). Therefore, metal defences may be effective against a broad range of herbivores and pathogens, except for those that are also tolerant to the metal. A further advantage is the effectiveness of metals against specialist herbivores that are adapted to and even attracted by the GS of their specific hosts, but can be sensitive to the metal concentrations reached in hyperaccumulator species (Jhee et al. 2006). Another role of metal hyperaccumulation in plant defence is based on the possibility that organic defences can increase the efficiency of protection by metals, by either additivity or synergy, and thus magnify the benefits of each defence in the so-called joint-effect hypothesis (Boyd 2007).

Thus, it appears likely that organic defences play a role in the evolution of metal hyperaccumulation and should therefore be considered further in studies of defence hypotheses. Interactions between metal accumulation and biotic stress can, however, be much more complex than envisaged by the hypotheses listed. They exceed the remit of this chapter, and the interested reader should consult recent reviews on this topic (Boyd 2007; Poschenrieder et al. 2006a) that explain these different possibilities in detail. In all cases, it should be noted that the particular characteristic of the hyperaccumulated element, its concentration, and the particular type of feeding employed by the herbivore (phloem sucking, chewing) or pathogen (necrotrophic, biotrophic) have significant effects on the results (Boyd 2007).

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