*3.4.1.2. Root exudates*

total level of heavy metal in the soil is greater than 1 (extraction coefficient > 1) (Rotkitti‐ khun *et al.,* 2006; Harrison and Chirgawi 1989); c) when the plant takes up between 10 – 500 times more heavy metals than normal plants (uncontaminated plants - control plants) (Fifield and Haines 2000; Allen,1989); and d) more than 100mg/kg of cadmium, 1000g/kg of copper, lead, nickel, chromium; or more than 10000mg/kg of zinc (Mganga *et al.,* 2011; Ernst, 2006; Brooks, 1998). An excluder is a plant that has high levels of heavy metals in the roots but with shoot/root quotients less than 1 (Boularbah *et al.,* 2006). Finally, Baker and Walker (1990) classified a plant as an indicator when the levels of heavy metals within

Resistant plants are able to grow on metal contaminated soil due to avoidance and/or tolerance strategies. Plant resistance to high levels of heavy metals in soils can result from either reduced uptake or once taken up, metals have to be transformed into a physiologically tolerable form.

The plasma membrane is the first structure of living cells exposed to heavy metals. The membrane functions as a barrier for the movement of heavy metals into cytoplasm. The restriction of metals at the plasma membrane limits the uptake and accumulation of metals by preventing their entry into the cytoplasm. This can be done by changing the ion binding capacity of the cell wall and/or decreasing the uptake of metal ions through modified ion channels, and/or by removing metals from cells with active efflux pumps and/or with root

The cell wall and membrane interface could be a site of metal tolerance since a signifi‐ cant amount of metals has been reported to be accumulated there. Divalent and trivalent metal cations can bind plant cell walls because of the presence of functional groups such as –COOH, -OH and –SH. Pectins are polymers that contain carboxyl groups which enable the binding of divalent and trivalent heavy metals ions. In enriched heavy metal environ‐ ments, some plants will increase the capacity of their cell wall to bind metals by increas‐ ing polysaccharides, such as pectins (Colzi *et al.,* 2011; Pelloux *et al.,* 2007). Konno *et al.* (2010; 2005) showed that the pectin in root cell walls was important in binding Cu in the fern, *Lygodium japonicum,* and in the moss, *Scopelophila cataractae*. The cell wall of *Minuar‐ tia verna sp. hercynica* growing on heavy metal contaminated medieval mine dumps has been found to have high concentrations of Fe, Cu, Zn and Pb (Solanki and Dhankhar 2011; Neumann *et al.,* 1997). On the other hand, Colzi *et al.* (2012) found that a copper tolerant *Silene paradoxa* population restricted the accumulation of Cu in roots, when exposed to high Cu, by decreasing their pectin concentration in the cell wall and increasing pectin methyl‐

their tissues reflect those in the surrounding soil.

**3.4. Physiological mechanisms of metal resistance**

*3.4.1. Restriction of metal uptake*

62 Environmental Change and Sustainability

with root exudates (Tong *et al.,* 2004).

ation thus preventing the binding of Cu.

*3.4.1.1. The cell wall*

Resistant plants can also restrict the entry of metals by immobilizing them in the rhizosphere with root exudates outside the plasma membrane (Colzi *et al.,* 2011). This has been reported in *T. aestivum* where the exudation of phytochelatins, citrate and malate may be responsible for Cu exclusion mechanisms in non accumulators (Yang *et al.,* 2005b; Bálint *et al.,* 2007). Hall (2002) also proposed a mechanism for Ni exclusion in plants involving Ni-chelating exudates which include histidine and citrate. In non hyperaccumulator plants, these Ni chelators accumulate in their root exudates which, in turn decreases Ni uptake. The copper exclusion could be due to its chelation with citrate and malate exudates in the rhizosphere of wheat roots. The restriction of Cu uptake in wheat by the efflux of these organic acids has been previously documented by Nian *et al.* (2002)*.*

#### *3.4.2. Chelation*

The phytotoxic effect of free metal ions can be eliminated by their chelation by specific highaffinity ligands (Yong and Ma 2002). The chelation of metals allows for the restriction of metal uptake, the uptake of metal ions, sequestration and compartmentation, as well as xylem loading and transport within the plant. Baker *et al.* (2000) categorized these ligands according to the characteristic electron donor centers, which include sulfur donor ligands, oxygen donor ligands and nitrogen donor ligands.
