Making a generalization about metal toxicity is difficult. This is due to the multidimensional varia-
tions of the parameters chosen for experiments, including concentrations, biospeciation, duration of in-
cubation, type of plant material (e.g., whole plant, algae, isolated organelles), and type of the affected tar-
get(s) (e.g., organ, cell, molecule).
A dysfunction due to an excess of metal(s) can be seen at the morphological level; e.g., roots or
leaves grow more slowly [5]. Plants growing in soil containing high concentrations of Al produce a shal-
low root system and are sensitive to drought. In addition, they can use other soil nutrients poorly [6–8].
Under metal excess, a general chlorosis of young leaves is observed [5,9,10], reflecting a weaker chloro-
phyll synthesis capacity [11]. Reduction of cell growth has been reported with green algae [12,13]. In mi-
croalgae, metals can also affect cell division and separation [12].
At the cellular level, the primary target of metals is the plasma membrane, leading to loss of K by
leakage into the extracellular spaces [14]. In lichens, Cu triggers larger K efflux than Pb and Zn [15].
Metal permeation in plant cells can be facilitated by chelating agents such as by some fungicides (dithio-
carbamate derivatives), which are pronounced lipophilic compounds. In contrast, hydrophilic metal
chelates are less available for plants and are toxic for microorganisms [16–18]. Once inside the cell, the
hydrophilic metal chelates can release the metal ions [19]. Cu was found to inhibit the enzyme responsi-
ble for the destruction of hydrogen peroxide in cells; this remaining toxic compound oxidizes lipids that
in turn damage membranes [20]. In addition, harmful activated oxygen species such as hydroxyl radicals
and hydrogen peroxide are triggered in the presence of excess Fe^2 , Cd^2 , or Cu^2 [21,22], finally dam-
aging DNA. Chloroplast ultrastructure is also damaged by an excess of metals [23].
At the biochemical level, heavy metals (HMs) have been found on pigments. Cd, Cu, Hg, Ni, Pb, and
Zn can substitute for the chlorophyll Mg [24,25] and lead to a breakdown of photosynthesis and even to
death of the cells. When dead, the plant remains green if Cu- or Zn-chlorophylls are present because of the
high stability of these substituted pigments. This was observed for plants stressed in shade [25]. Under
strong light, HM-treated plants bleach almost completely because of chlorophyll decay; a structural feature
was suggested by H. Küpper (personal communication) to explain that HMs cannot reach most of the
chlorophylls in high-light conditions. Generally speaking, photosynthesis is less efficient when HMs have
entered the chloroplasts; the pollutants interact at several steps [11], modifying, for instance, the structure
of pigment-protein complexes [26]. Interactions between toxic metals and proteins alone have also been
reported [21,26,27]. HMs may interact with thiol or histidyl groups of proteins, whose functions are then
inhibited. In this way, several steps of the chlorophyll biosynthetic pathway [reviewed in 28] are altered
[29]. In contrast, some toxic metal ions may increase enzyme activity or induce synthesis of specific pro-
teins. For instance, Cd increases the activity of arginine carboxylase (EC 4.1.1.19) [30], an enzyme in-
volved in the putrescine biosynthesis pathway, whereas Al increases the putrescine level in a different way.
III. MECHANISMS OF METAL ION UPTAKE BY CELLS
Free cations usually constitute the most available form of metals for living organisms [31]. The compo-
nents associated with metals in the plant environment also have to be considered; for instance, the metal
752 BERTRAND ET AL.
TABLE 1 Some Proteins That Require Metals for Either Structural or Activity Purposes
Proteins Type of metal(s) Role of metal(s)
Aldehyde oxidase Mo, Fe Catalysis
Carbonic anhydrase Zn Structure and catalysis
Cytochrome oxydase Cu Electron carrier
Formiate dehydrogenase Fe, Mo, Se, W Catalysis
Nitrogenase Fe, Mo Catalysis
Peroxidase Fe Catalysis
Plastocyanin Cu Electron carrier
Sulfite oxidase Fe, Mo Catalysis
Superoxide dismutases Cu/Zn; Fe; Mn Structure and catalysis
Water oxidase Mn Catalysis
Xanthine oxidase Fe, Mo Electron carrier