uptake by Ulva lactucaincreases when salinity decreases [32]. The primary active transport system in al-
gae has been identified as an Mg^2 adenosinetriphosphatase (ATPase)–driven, V-sensitive electrogenic
Hefflux pump [33]. Metallic ion accumulation by cells, such as microalgae, consists of two phases: a
rapid phase of metal binding to the cell wall (i.e., biosorption) followed by a slower phase due to the si-
multaneous effects of growth and surface adsorption, active and passive transport [34,35]. Depending on
the metal ions and on the algal species, the proportion of metals during the first phase can account for up
to 50% [35]. The first phase can be described using the Freundlich adsorption isotherm [36], but a slight
deviation can be observed for high HM concentrations [35,37]. The deviation can be explained by a com-
petition between metal ions for available binding sites. A convenient way to characterize the adsorption
of metal ions on algae is to use the Scatchard plot [38], from which the maximal binding capacity and the
binding constant of metals can be estimated.
IV. METAL SUBCELLULAR LOCALIZATION
Metals are localized in different compartments of the cells; Table 2 shows the proportions measured in
various organisms. A study of the accumulation of Co, Zn, and Mn by Chlorellaindicated, for instance,
that the concentration of these elements is higher in vacuoles than in cytoplasm [35]. With excess of Ni,
Molas [39] observed vacuolization in leaf mesophyll cells of Brassica oleracea. In natural metal-rich
habitats, some hyperaccumulator plants can accumulate very high amounts of a metal (Ni, most often)
without showing any toxicity symptoms or reduction in growth [40,41]. Thlaspi caerulescenscan have
20,000g Zn g^1 dry weight of shoots [42]. Küpper et al. [42] estimated that more than 60% of the metal
accumulated by leaves was present in the epidermal vacuoles. The mechanism involved in this preferen-
tial accumulation is not known. The Zn was found in soluble form and not in deposits as globular crys-
tals as described by Vazquez et al. [43]. Anyway, a metal in excess changes the microelement balance and
photosynthesis of a plant [44].
V. DEFENSE MECHANISMS AGAINST METAL TOXICITY
To avoid undesirable metal penetration, plants are able to extrude material that can chelate free metallic
cations in the extracellular space. Toxic metals can also be trapped once they are inside the cells. Then
they are either rapidly excluded from the cells or stored in vacuoles. Metallic sequestration often involves
the formation of complexes between a metal cation and functional groups (e.g., carboxyl, carbonyl, sul-
fonate, phosphate) present on the surface or inside the porous structure of the biological material [45].
A. Extracellular Metal Sequestration
Differences in Al tolerance between several bean species have been attributed to the capacity of roots to
exude citric acid, a strong Al chelator [46]. A similar conclusion was drawn for monocotyledons (barley,
HOW PLANTS ADAPT TO EXCESS OF METALS 753
TABLE 2 Subcellular Localization of Some Metals in Different Plants
Metal Localization Organism Reference
Co Cell wall (38%) Chlorella 35
Cytosol (9%)
Vacuoles and organelles (10%)
Insoluble (43%)
Cu Vacuole, chloroplast, nuclei Armeria maritima 37
Mn Cell wall (43%) Chlorella 35
Cytosol (21%)
Vacuoles and organelles (15%)
Insoluble (21%)
Pb Dictyosome, cell wall Zea mays 39
Zn Cell wall (52%) Chlorella 35
Cytosol (16%)
Vacuoles and organelles (10%)
Insoluble (22%)