Plants suitable for phytoremediation should possess a series of characteristics: (1) ability to accumulate metals preferably in the aboveground parts, (2) tolerance to metal concentration accumulated, (3) fast growth and high biomass, (4) widespread highly branched root system, (5) easy harvestability, and (6) non consumable by humans and animals (Arthur et al., 2005). However, plant species just can partially fulfill these conditions. For example, those few plants that can accumulate metals to exceptionally high concentrations in their shoots, with no adverse effects on their growth (hyperaccumulators), are both small and slow growing, and often they are rare species of limited population size and very restricted distributions (Pollard et al., 2002). On the other hand, high biomass producing species, such as trees and agricultural crops tend to take up relatively smaller amounts of heavy metals than hyperaccumulators. Comparing with agricultural species, trees have some advantages as for example their deep rooting favoring the metal extraction from deeper soil layers (Dos Santos and Wenzel, 2007). The phytoremediation of HM contaminated sites by trees has been reviewed in detail by Pulford and Watson (2003).
2.3.1. Heavy Metals in Plants. Functions and Negative Effects
Plants used for phytoremediation of HMs must be able to cope with negative effects of metal excess. Heavy metals occur naturally, but not all of them have a biological role (Schutzendubel and Polle, 2002). Among HMs, only 17 may be bioavailable for cells and being of importance for organisms and ecosystems. For example, metals such as Cu, Zn, Ni, or Cr are toxic with high or low importance as trace elements. Cadmium, Pb or Ag has no known function as nutrients and seem to be more or less toxic to plants and micro-organisms. High concentrations of HMs in soils could be toxic for plants resulting in varied effects on plant physiology affecting its growth and survival. According to Hermle et al. (2006), Cd, Cu and Zn become toxic for sensitive plants if they reach values in the concentration range of 5 -10 mg kg-1, 15 - 20 mg kg-1and 150 - 200 mg kg-1, respectively.
The effects of Cd on plant physiology are only partially understood (Vollenweider et al., 2006). Visible effects of exposure to high Cd concentrations are growth reduction and leaf chlorosis (Clemens, 2006). Cadmium interferes with the uptake, transport, and use of different elements (e.g. Fe, Zn and Mg) (Pietrini et al., 2010a). This metal can disturb the plant water balance, inhibiting the stomatal opening and affecting the photosynthetic apparatus (Vollenweider et al., 2006). At the cell level, Cd can damage different organelles including chloroplasts, nucleus, vacuole and mitochondria. It inhibits or activates many enzymes, particularly those rich in sulfhydryl groups. Oxidative stress has been discussed as a primary effect of Cd exposure even though Cd is not a redox-active metal and it does not take part in Fenton and Haber-Weiss reactions (Clemens, 2006). Rather, symptoms of oxidative stress, such as lipid peroxidation are consequence of the activation or the inactivation of antioxidative enzymes (Vollenweider et al., 2006) or the depletion of glutathione (Clemens, 2006).
Copper is an essential trace element for plants as cofactor of various proteins. It plays an important role in process such as photosynthesis and respiration, carbon and nitrogen metabolism, oxidative stress protection, perception of ethylene, and cell wall synthesis. Copper functions as a redox agent in biochemical reactions. However, this property makes it also potentially toxic when plants grow under high concentrations. Cu excess induces stress and causes injury to plants leading to growth retardation and leaf chlorosis (Yadav, 2009). At cell level, Cu ions can catalyze the production of highly toxic hydroxyl radicals, in particular through Fenton chemistry, thus leading to the damage to macromolecules and disturbance of metabolic pathways (Hansch and Mendel, 2009). In addition, Cu is highly reactive to thiols and can displace other essential metals in proteins (Burkhead et al., 2009). To balance needs and avoiding potential toxic excess, the cellular concentrations of Cu are tightly controlled (Pilon et al., 2009).
Zinc is an essential nutrient for plants. This element is a co-factor required for the structure and function of numerous proteins (Grotz and Guerinot, 2006), energy production and structural integrity of membranes (Hansch and Mendel, 2009). High levels of Zn inhibit many plant metabolic functions resulting in retarded growth and senescence. Zinc toxicity in plants limits the growth of both roots and shoots and produces leaf chlorosis. Even though Zn is not redox active, too high levels of this metal are toxic because it can displace other metals (e.g. Fe, Mn and Cu) in the cell (Pilon et al., 2009; Yadav, 2009). Because this, Zn homeostasis is also strongly regulated in plant cells.
2.3.2. Mechanisms of Heavy Metal Homeostasis and Tolerance
Despite the negative effects that excess of HMs can produce, some plant species have developed ecotypes able to survive and grow on highly contaminated soil (Salt et al., 1998). Plants living in a contaminated environment can be roughly classified into three types (Hassinen et al., 2009): (1) excluders that tolerate metals by restricting uptake, (2) accumulators that have increased cellular detoxification mechanisms especially in the above-ground parts, and (3) indicators in which the elemental concentrations reflect the soil concentrations due to the lack of protective mechanisms. Within the second group, hyperaccumulating plants are an important case. As it was showed, they can accumulate metals to exceptionally high concentrations in their shoots, and without negative effects on their growth. The accepted shoot concentrations defining hyperaccumulation are (on a w/w basis) 0.01 % for Cd, 0.1 % for Cu and 1.0 % for Zn (Pollard et al., 2002).
Plants respond to negative effects of exposition to toxic levels of HMs developing different homeostatic mechanisms to maintain essential metallic ions in suitable concentrations within different cell compartments and minimize the damage caused by non-essential metallic ions. In this way, a regulated network of transport, chelation, traffic and compartmentation control the absorption, distribution and detoxification of the metallic ions (Clemens et al., 2002). The way in which is regulated determinate the ability of plants for restricting uptake and/or root to shoot transport, and sequestrating and compartmenting metals in organs and/or organelles.
The operation of phytoremediation systems depends on both biological and environmental factors as well as on the interaction between them. The efficiency of phytoremediation can be improved through genetic selection (breeding of selected parental genotypes and progeny testing, hybridization between compatible species and direct clonal assessment of potentially useful pedigrees, etc.) of plants with the desired properties (tolerance level, metal accumulation patterns, biomass production, etc.) and by the application of the adequate agronomic practices (e.g. management of soil compaction, irrigation, fertilization, etc.). In terms of plant improvement, biotechnological approaches as such as the use of transgenic plants engineered for metal tolerance/accumulation or the marker assisted selection are key to complement traditional breeding techniques and developing plants with suitable phenotypes. In a similar way, plant growth, HM tolerance and accumulation can be also enhanced by the selection of the adequate plant interacting rhizospheric microorganisms.
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