Tolerance Mechanisms

The toxic effects of plant exposure to elevated metal concentrations, such as growth inhibition and chlorosis, are well documented. However, as for other organisms, the biochemical understanding of metal toxicity is limited. Class B metals such as Cu(I) and Hg and borderline metals such as Cu(II), Zn, Ni, and Cd (12) can form complexes with nitrogen and sulfur atoms in proteins, thereby potentially inactivating them. The nonessential metals Cd and Pb compete for binding with the essential metals Ca and Zn. Also implicated in symptoms of metal toxicity is the redox activity of some metals (e.g., Cu, Fe) that may result in the formation of reactive oxygen species.

A complex network enables plants to control tightly the intracellular concentrations and distribution of essential heavy metals such as copper and to minimize the cytosolic concentrations of nonessential heavy metals such as cadmium. The interplay of mainly transport and chelation processes that constitutes this network results in a "basic metal tolerance," the distribution, sequestration, and exclusion of potentially toxic heavy metal ions. In addition, a number of plant species show "metal hypertolerance." They can grow on soil that naturally or because of human activities contains heavy metal concentrations that are growth prohibiting to most plants. These species belong to a specialized flora that has colonized Ni-rich serpentine soils or Zn- and Cd-polluted areas (13). Two principal responses to otherwise toxic heavy metal concentrations can be found, metal exclusion and metal hyper-accumulation, with the latter mainly restricted to Ni, Zn, and Se. About 400 different species belonging to a wide range of taxa have been described as hyperaccumulators, about 75% of which are Ni hyperaccumulators (13).

It is a general characteristic of both basic metal tolerance of most organisms and hypertolerance of some specialized plants that most of the mechanisms involved appear to be specific for a certain metal or a small group of metals. For instance, fission yeast deficient in phytochelatin synthesis (see later) are Cd and Cu hypersensitive yet grow normally, when compared with wild-type cells, in the presence of elevated Zn concentrations (14). Some Ni-hyperaccumulating plants show the so-called histidine response, which mediates Ni tolerance (15). The sensitivity toward most other heavy metals, however, is not attenuated by the increases in histidine levels.

Five general metal tolerance mechanisms can be distinguished: chelation, sequestration, exclusion, biotransformation, and repair. The first three of these categories constitute the principal elements of the metal homeostasis network. Exclusion includes the regulation of metal uptake into cells. Biotransformation, i.e., reduction and possibly volatilization, appears to be restricted mainly to Hg and the metalloids Se and As.

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