Bioresource Technology 77 (2001) 229±236

Review paper

Phytoextraction: a cost-e€ective plant-based technology for the
removal of metals from the environment
Carlos Garbisu a,*, Itziar Alkorta b
a

b

Departamento de Agrosistemas y Producci
on Animal, NEIKER, Instituto Vasco de Investigaci
on y Desarrollo Agrario, Berreaga 1,
E-48160 Derio, Spain
Departamento de Bioquõmica y Biologõa Molecular, Facultad de Ciencias, Universidad del Paõs Vasco, Apartado 644, E-48080 Bilbao, Spain
Accepted 31 July 2000

Abstract
Phytoremediation is an emerging technology that uses plants to clean up pollutants (metals and organics) from the environment.
Within this ®eld of phytoremediation, the utilization of plants to transport and concentrate metals from the soil into the harvestable
parts of roots and above-ground shoots is usually called phytoextraction. Most traditional remediation methods do not provide
acceptable solutions for the removal of metals from soils. By contrast, phytoextraction of metals is a cost-e€ective approach that
uses metal-accumulating plants to clean up these soils. Subsequently, the harvestable parts, rich in accumulated metals, can be easily
and safely processed by drying, ashing or composting. Some extracted metals can also be reclaimed from the ash, generating recycling revenues. Phytoextraction appears a very promising technology for the removal of metal pollutants from the environment
and may be, at present, approaching comercialization. Ó 2001 Elsevier Science Ltd. All rights reserved.
Keywords: Phytoextraction; Metal; Phytoremediation; Soil pollution

1. Introduction: soil pollution and heavy metals
Soil pollution, a very important environmental
problem, has been attracting considerable public attention over the last decades. As a matter of fact, increasingly widespread pollution has caused vast areas of land
to become non-arable and hazardous for both wildlife
and human populations. Nowadays, more and more
people consider that the magnitude of the pollution
problem in our soils calls for immediate action. Unfortunately, the enormous costs associated with the removal of pollutants from soils by means of traditional
physicochemical methods have been encouraging
companies to ignore the problem. In fact, the current
state-of-the-art technology for the remediation of metalpolluted soils is the excavation and burial of the soil at a
hazardous waste site at an average cost of $1 000 000 per
acre (Raskin et al., 1997). Other common approaches
used to treat metal-polluted soils are ®xation (chemical
processing of the soil to immobilize the metals) and
leaching (using acid solutions or proprietary leachants

*

Corresponding author. Fax: +349-4452-2335.
E-mail address: cgarbisu@neiker.net (C. Garbisu).

to desorb and leach metals from soil followed by the
return of clean soil residue to the site) (Salt et al., 1995).
Apart from minimizing the impact of future incidents by
means of controlling pollution input, it is imperative to
deploy innovative technologies which could economically remediate polluted soils (Garbisu and Alkorta,
1997).
In contrast to many organic pollutants, which are
anthropogenic and often degraded in the soil, metals
occur naturally and are conserved (Wade et al., 1993).
Due to their immutable nature, heavy metals are a
group of pollutants of much concern. The danger of
heavy metals is aggravated by their almost inde®nite
persistence in the environment. Although some metals
are essential for life (i.e., they provide essential cofactors
for metalloproteins and enzymes), at high concentrations they can act in a deleterious manner by blocking
essential functional groups, displacing other metal ions,
or modifying the active conformation of biological
molecules (Collins and Stotzky, 1989). In addition, they
are toxic for both higher organisms and microorganisms. In fact, many metals a€ect directly various physiological and biochemical processes causing reduction in
growth, inhibition of photosynthesis and respiration,
and degeneration of main cell organelles (Vangronsveld

0960-8524/01/$ - see front matter Ó 2001 Elsevier Science Ltd. All rights reserved.
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. Raskin et al. municipal wastes.. 1997a. etc. pesticides and sewage. Microbial remediation of metal-polluted soils Microorganisms can detoxify metals by valence transformation. In fact. Garbisu..1. Hg(II). The primary sources of metal pollution are the burning of fossil fuels. the metal-loaded biomass can be either disposed of appropriately or. 1995b. 1994). enclosed in treatment tanks or other kinds of reactor vessels. some microorganisms can enzymatically reduce a variety of metals in metabolic processes that are not related to metal assimilation (Lovley.. 1997). Ishibashi et al. 1998. 1995). it is certainly not less true that when considering the remediation of a metal-polluted soil. or aromatic compounds. In the environment. Microorganisms can also enzymatically reduce other metals such as technetium. so far no cost-e€ective way exists to retrieve small organisms from the soil (Ow.. can also be detoxi®ed by bacterially mediated reduction and the enzymatic mechanism responsible for the reduction of Cr(VI) to Cr(III) is currently being studied and may ultimately lead to a commercial bioremediation process (Garbisu et al. large-scale solution to heavy metal-polluted areas. 1993): some bacteria obtain energy for growth by coupling the oxidation of simple organic acids and alcohols. 1993).. 1998). Alkorta / Bioresource Technology 77 (2001) 229±236 and Clijsters. I. 1996). gold. Subsequently. Heavy metals cannot be destroyed biologically (no ``degradation''. Phytoremediation is also preferable to currently used approaches for treating soils such as land®lling. 1997). to the reduction of Fe(III) or Mn(IV). water (liquid substrate) or the air (Salt et al. ®xation. plants can be compared to solar driven pumps which can extract and concentrate certain elements from their environment (Salt et al. microorganisms have been mostly used to treat industrial waste streams. as is the case for the in situ bioremediation systems. Garbisu and Alkorta. downwash from power lines. treated to recover the metals. 1995a. 1992). As a consequence. occurs) but are only transformed from one oxidation state or organic complex to another. fertilizers. In fact. although a wide variety of bacterial. probably due to some physiological barriers against metal transport to aerial parts.. for example. (ii) inherently less toxic. Hg(0). General aspects of phytoremediation Phytoremediation... Although it is true that microorganisms that use metals as terminal electron acceptors or reduce them as a detoxi®cation mechanism can be of use for the re- moval of these pollutants from the environment (Garbisu and Alkorta. The more toxic form of chromium. 1995). recycling it in a biologically safe state rather than permanently disposing of it by removal to a storage site (Salt et al. algal and plant systems are capable of concentrating toxic metals from their surroundings. 1990). As a consequence of the alteration of its oxidation state. extracellular chemical precipitation.230 C. In this respect. silver and copper. while others are easily transported in plants. Another natural reduction process now being developed for commercial applications is the transformation of mercuric ion. Phytoremediation is often also referred as botanicalbioremediation or green remediation (Chaney et al. depending on their concentrations. fungal. Cr(VI). theoretically rendering them clean (metal-free soils). mining and smelting of metalliferous ores. to volatile metallic mercury. However. or (iv) volatilized and removed from the polluted area (Garbisu and Alkorta. 1996. and in relation to the bioremediation of heavy metals. Some metals are accumulated in roots (especially Pb).. vanadium. 2. bacteria are not e€ective as a permanent. Cd. Therefore. Bacteria that use U(VI) as a terminal electron acceptor may be useful for removing uranium from contaminated sites. is being considered as a new highly promising technology for the remediation of polluted sites. metal-accumulating plants o€er numerous advantages over microbial processes since plants can actually extract metals from the polluted soils. 1997b. Phytoremediation 3. The reduction of the toxic selenate and selenite to the insoluble and much less toxic elemental selenium may be exploited to enhance removal of these anions from contaminated sites (Combs et al. de®ned as the use of green plants to remove pollutants from the environment or to render them harmless (Cunningham and Berti. This technology can be applied to both organic and inorganic pollutants present in soil (solid substrate). with the organisms either immobilized onto di€erent support matrixes or in a freeliving state. the metal may become either: (i) more water soluble and is removed by leaching. hydrogen. (iii) less water soluble so that it precipitates and then becomes less bioavailable or removed from the contaminated site. but reduction of these metals has not been studied extensively (Lovley. since this implies the ultimate removal of the contaminated biomass from the site. 3. 1994). change in the nuclear structure of the element. leaching. 1997). molybdenum. or volatilization. application of microbial bioremediation to the in situ removal of heavy metals from polluted soils is mainly limited to metal immobilization by precipitation or reduction (Summers. since it reclaims soil at the site. 1997). Heavy metals are present in soil as natural components or as a result of human activity. . Garbisu et al. the ability to accumulate heavy metals varies signi®cantly between species and between cultivars within a species. 1993.c.

di€usely polluted areas where pollutants occur only at relatively low concentrations and super®cially (Rulkens et al. plants could participate directly through contaminant uptake and subsequent contaminant immobilization or degradation within the plant.. the fact that the remediation procedure may take rather long. 1994). root-associated microorganisms that actually accomplish contaminant detoxi®cation (this matches the previously named plant-assisted bioremediation). the weight and volume of contaminated material can be further reduced by ashing or composting. which penetrate the soil for several meters. As a result of their association with speci®c ore deposits. precipitate and concentrate toxic metals from polluted e‚uents.. 1998. Pollutant-accumulating plants are utilized to transport and concentrate contaminants (metals or organics) from the soil into the above-ground shoots. 1997)... trees have the most massive root systems of all plants. 1995).. from water and aqueous-waste streams. Raskin et al. 1997. 1983). On the other hand. Salt et al. 3. toluene.. and then harvesting and incinerating the biomass to produce a commercial ``bio-ore'' has been proposed (Brooks et al. Plants stabilize pollutants in soils. ethylbenzene. trichloroethylene. Phytovolatilization: the use of plants to volatilize pollutants. the air purifying uses of some plants. In this context. if economically feasible.. Phytoextraction: the use of plants to remove contaminants from soils. This ``phytomining'' o€ers the possibility of exploiting ore bodies that are otherwise uneconomic to mine and its e€ect on the environment is minimal when compared with the erosion caused by opencast mining (Brooks et al. roots can be harvested as well (Kumar et al. Phytodegradation: the use of plants and associated microorganisms (plant-assisted bioremediation) to degrade organic pollutants.. as is the case with phytoremediation methods. the possibility of planting metal hyperaccumulator crops over a low-grade ore body or mineralized soil. 1998).4. farther than most herbaceous plants (Stomp et al. In the case of indirect phytoremediation. Conclusions With a sound footing in basic research and a new regulatory environment supportive of innovative technologies. and trees will resprout without disturbance of the site. 3.2. In some tree species above-ground biomass can be harvested. Phytostabilization: the use of plants to reduce the bioavailability of pollutants in the environment. Alkorta / Bioresource Technology 77 (2001) 229±236 Following harvest of pollutant-enriched plants.3.. Interestingly enough. Plant roots or seedlings grown in aerated water absorb. Most existing remediation physicochemical technologies are meant primarily for intensive in situ or ex situ treatment of relatively highly polluted sites. I. Categories of phytoremediation These include (Chaney et al. used for metal recovery (Salt et al. many metallophyte plants are used in prospecting for mineral deposits (Brooks. Metal-enriched plants can be disposed of as hazardous material or..g. 1994). mainly metals. and thus are not very suitable for the remediation of vast.4. 1995. selenium. 1998). Garbisu. benzene.. This allows establishment of trees on sites with low fertility and poor soil structure.C. Plant roots in conjunction with their rhizospheric microorganisms are utilized to remediate soils contaminated with organics.. Phyto®ltration: the use of plant roots (rhizo®ltration) or seedlings (blasto®ltration) to absorb or adsorb pol- 231 lutants.. In some cases. Examples of pollutants that could possibly be removed by phytoremediation are heavy metals. Some authors (Stomp et al. is not considered a problem (Rulkens et al. 1998). 3. Plants extract volatile pollutants (e. Besides.6-trinitrotoluene. and provided that it will result in lower costs and that the risks posed to human populations and ecosystems are acceptable. 1994) also distinguish between indirect and direct phytoremediation.. trees potentially are the lowest-cost plant type to use for phytoremediation. Use of trees According to some authors (Stomp et al. 1998). 2. plants participate in the detoxi®cation of pollutants via their support of symbiotic. A number of tree species can grow on land of marginal quality. the term is mostly used to refer to metal removal from soils. 1994). in the last few years. phytoremediation appears as a very valid option since it is best suited for the remediation of these di€usely polluted areas and at much lower costs than other methods. sites with light to moderate toxic metal contamination can be remediated by growing metal-accumulating plants (Kumar et al. 1995). This attribute would be valuable if periodic removal of pollutants sequestered in plant tissue were desirable as in the case of heavy metals bound to wood (Stomp et al. mercury) from soil and volatilize them from the foliage. keeping costs low for plant establishment. 1998). thus rendering them harmless and reducing the risk of further environmental degradation by leaching of pollutants into the ground water or by airborne spread.. phytoremediation is increasingly being viewed as a cost-e€ective and user-friendly alternative to traditional methods of environmental cleanup (Boyajian and .. More and more often. While the most heavily contaminated soils do not support plant growth. 1998). and xylene (Rulkens et al.

most hyperaccumulators are relatively small in size. soil science. Garbisu.. (1997). will increase the eciency of the phytoremediation processes (Ensley et al.. This is due to . 1994). Raskin et al. Plants can accumulate heavy metals essential for growth and development such as Fe. the capacity of plants to concentrate metals has usually been considered a detrimental trait since some plants are directly or indirectly responsible for a proportion of the dietary uptake of toxic heavy metals by humans (Brown et al. 1997).. Chelate-assisted or induced phytoextraction Chelating agents have been used as soil extractants... 1989. Cr. and possibly Ni. agricultural engineering. Mo. The ideal plant to be used in phytoextraction should have the following characteristics: · be tolerant to high levels of the metal. often endemic to naturally mineralized soils. 1989. 1997). Raskin et al. 1994). microbiology and genetic engineering. · have a profuse root system. Mn.1. Baker and Brooks. some of them have the capacity to accumulate heavy metals with no known biological functions. Ag. two strategies of phytoextraction: (1) chelate-assisted or induced phytoextraction and (2) continuous phytoextraction. Raskin et al. I. 1994. 1990. According to Raskin et al. 1997). Dietary intake of heavy metals through consumption of crop plants can have long-term e€ects on human health (Ow. Curiously enough. Phytoremediation is still a new ®eld which holds great potential and in order to develop this potential requires a multidisciplinary approach. Boyd et al. Phytoextraction of metals The term ``phytoextraction'' mainly concerns the removal of heavy metals or radionuclides from soil by means of the uptake capabilities of plants. high biomass plants (Ow. Co. Therefore. Ernst et al. and to maintain solubility of micronutrients in hydroponic solutions (Salt et al. often reaches 1±5% of their dry weight (an order of magnitude higher than those concentrations found in non-accumulating plants growing nearby). The idea of using plants to remove metals from soils came from the discovery of di€erent wild plants. planting and harvest time and the timing of amendment application.. 1997). such as irrigation. 4. the degree of accumulation of metals such as Ni. Pb.. 1989. observed in hyperaccumulators. 1997). 1997). agronomy. Unfortunately. As pointed out by its name. Zn.. Naturally occurring plants called ``metal hyperaccumulators'' can accumulate 10±500 times higher levels of elements than crops (Chaney et al. Robinson et al. 4.. 1996). · accumulate high levels of the metal in its harvestable parts. plants require a balance between the uptake of essential metal ions to maintain growth and development and the ability to protect sensitive cellular activity and structures from excessive levels of essential and non-essential metals.. Either the existing hyperaccumulator plants must be bred for increased growth and biomass. Boyd and Martens. Resistance of plants to heavy metal ions can be achieved by an avoidance mechanism. Mg.. (1998) there are. and possibly Cu.. In addition. The phytoextraction of heavy metals represents one of the largest economic opportunities for phytoremediation because of the size and scope of environmental problems associated with metal-contaminated soils and the competitive advantage o€ered by a plant-based remediation technology (Raskin et al. 1997). Tolerance to heavy metals is based on the sequestration of heavy metal ions in vacuoles. The prevention of herbivory and disease is thought to be the main function of this unique phenomenon of hyperaccumulation (Baker and Brooks. which includes mainly the immobilization of metal in root and in cell walls. Cunningham et al. In this respect. 1994. or hyperaccumulation traits must be engineered into fast growing. Zn. a source for micronutrient fertilizers. · have a rapid growth rate. 1979. 1995). this strategy of phytoextraction is based on the fact that the application of metal chelates to the soil signi®cantly enhances metal accumulation by plants. · have the potential to produce a high biomass in the ®eld. Alkorta / Bioresource Technology 77 (2001) 229±236 Carreira. Optimizing agronomic practices. spanning ®elds as diverse as plant biology. 1994). 1995). according to some authors (Chaney et al. Se and Hg (Baker and Brooks. proteins and peptides and on the presence of enzymes that can function at high levels of metallic ions (Harborne. have slow growth rates and we lack the technology for their largescale cultivation (Salt et al.. that accumulate high concentrations of metals in their foliage (Brooks et al. 1996). 1995.. natural metal hyperaccumulator phenotype appears to be much more important than high yield ability when using plants to remediate metal-contaminated soils. 1996).232 C. such as Cd. 1989. 1995). Cu.. The annual yields in biomass of hyperaccumulators are generally one to two orders of magnitude lower than those of robust crop plants (Ow. on binding them by appropriate ligands like organic acids.. For the metabolism of metals. at present. As pointed out in the excellent review by Salt et al. many authors have studied the metal-uptake capabilities of the cultivated Brassica (mustard) species because of their relation to wild metal-accumulating mustards (Kumar et al. fertilization. 1995. However. a lot of research emphasis has been placed on the evaluation of the metal-accumulating capacity of high biomass plants that can be easily cultivated using established agronomic practices.

Sr) (Salt et al. According to Blaylock et al. it is common to ®nd cases of low bioavailability.. Salt et al. radionuclides such as U. may act as phytosiderophores (Raskin et al. 1998). it is likely that Pb is transported within plants as a Pb± EDTA complex. Cs. 1995). 1998).e. Thus. Chaney et al. when applied to established plants several days before harvest. For instance. The existence of hyperaccumulators for metals other than Ni.. There is also the possibility that metal-chelating proteins. for ecient phytoextraction to occur. 1979. Cu. Therefore. cadmium... Due to this phenomenon of the low bioavailability of metals in soils. 1935. 4. Reeves and Brooks. translocate and resist high amounts of metals over the complete growth cycle. 1997).. I. 1998). Nonetheless. But even plants.. 233 synthetic chelates having a high anity for the metal of interest should be used: EDTA for lead. 1993). iron-chelating compounds have been studied in detail. that have a genetic capacity to accumulate Pb. Zn and Se is not . 1996). 1995). Apart from the addition of synthetic chelates.. In this context. the discovery that the application of certain chelates to the soil increases the translocation of heavy metals from soil into the shoots has opened a wide new range of possibilities for this ®eld of metal phytoextraction (Blaylock et al. 1984).C. In fact. perhaps related to metallothioneins or phytochelatins. 1997).. So far. 1997). will not contain much Pb in roots or shoots if cultivated in Pb-contaminated soil (Raskin et al. Ni. 1998). Bauman. However. hyperaccumulators are the most suitable plants for the phytoextraction of metal-polluted soils. For instance. ragweed (Ambrosia artemisii®lia) have been identi®ed as good accumulators of Pb (Huang and Cunningham. 1983. Metal accumulation eciency appears to be directly related to the anity of the applied chelate for the metal (Salt et al. Blaylock et al. plants roots increase metal bioavailability by extruding protons to acidify the soil and mobilize the metals. possibly citrate for uranium. Cd. only phytosiderophores. Cd. Continuous phytoextraction Continuous phytoextraction depends on the natural ability of some plants to accumulate. Roots can also reduce soil-bound metal ions by speci®c plasma-membrane bound metal reductases. A large proportion of many metals remains sorbed to solid soil constituents. Fe and Mg (Welch et al. (1997) demonstrated the simultaneous accumulation of several metals (Pb. Cu. Blaylock et al. Unfortunately.. hyperaccumulators can naturally accumulate more than 1% of shoot dry biomass as Zn. 1993). arsenic. 1885. as mentioned above. Alkorta / Bioresource Technology 77 (2001) 229±236 the fact that under many circumstances.. 1997). such as Brassica juncea. 1997). 1936.. hyperaccumulators for the most environmentally important metallic pollutants (Pb. plants can remove between 180 and 530 kg/ha of Pb per year. As. The addition of chelates to the soil can also bring metals into solution through desorption of sorbed species.. pea plants de®cient in Fe or Cu have an increased ability to reduce Fe3‡ and Cu2‡ . 1995). The formation of metal±chelate complexes prevents precipitation and sorption of the metals thereby maintaining their availability for plant uptake (Salt et al.. Pb and Zn (Raskin et al. lead. 1998). dissolution of Fe and Mn oxides. it has been described that high biomass crop plants such as Indian mustard. 1997). making remediation of sites contaminated with up to 2500 mg/kg Pb possible in under 10 years (Salt et al. Fortunately. and avenic acid from oats (Welch et al. EGTA for cadmium (Blaylock et al. or Se (Ba~ nuelos and Meeks. 1991). Ni.. Zn) by Indian mustard plants after applying metal chelates. Mn. which is coupled with an increased uptake of Cu. Nonetheless. 1996. 1995).2. etc. Ethylenediaminetetraacetic acid (EDTA). 1998).e. not available for plant uptake) in the normal range of soil pH (Raskin et al... Garbisu.. corn and sun¯ower could accumulate signi®cant amounts of Pb when induced through the addition of metal chelates (Huang and Cunningham. U) have not been reliably described (Salt et al. 1983. Finally. 1995. lead (Pb) is usually extremely insoluble (i.. 1997). There are no reliable reports on the natural accumulation of the most environmentally important metallic pollutants (i. it can be concluded that. It may be possible to increase metal availability (and hence plant uptake) by means of maintaining a moderately acid pH in the soil through the use of ammonium containing fertilizers or soil acidi®ers (Salt et al. to a lesser extent. 1995. has proven to be very e€ective in facilitating the plant uptake of Cd. numerous studies have shown that lowering the pH of a soil decreases the adsorption of heavy metals and thus increases their concentration in the soil solution (Harter. Brooks et al. in the soil and depending on the metal itself. Corn (Zea mays) and. The mechanisms involved in metal-chelate induced plant uptake and translocation of metals are not well understood (Salt et al. Some of these phytosiderophores include mugeneic and deoxymugeneic acids from barley and corn. A similar mechanism has been observed for Fe mobilization in some Fe-de®cient dicotyledonous plants (Crowley et al. preventing the remediation process. plants secrete to the rhizosphere natural metal-chelating molecules to mobilize soil-bound metals.. Salt et al.. vegetation growing in heavily contaminated areas often has less than 50 mg/g Pb in shoots (Cunningham et al. Byers. it is common to observe that shoot metal accumulation in hydroponically cultivated plants greatly exceeds the metal accumulation measured in soilgrown plants.. and dissolution of precipitated compounds (Norwell. (1997) and Huang and Cunningham (1996). 1990. Ni..

and chemical extraction. 1992).. 4.. Alyssum murale and Arabidopsis thaliana for Zn.. 1989. Some laboratories are using traditional breeding techniques. some metals may be transported to the shoots complexed to organic acids. 1991). Therefore. 1997). I. 1997). apoplastic transport is further limited by the high cation-exchange capacity of cell walls (Raskin et al. 1993. in the tropics the Euphorbiaceae is the best represented group (Ensley et al. it should be possible to enhance uptake of heavy metals from soils.2. some studies (Salt et al..2.3... 1995). Particular emphasis has been placed on the evaluation of shoot metal-accumulation capacity of the cultivated Brassica (mustard) species because of their relation to wild metal-accumulating mustards (Kumar et al. 1997). In general.2. Thlaspi caerulescens. mainly citrate (Baker and Brooks. including land®lling. Pb and Cr. Several strains of Bacillus and Pseudomonas increased the total amount of Cd accumulated by Brassica juncea seedlings (Salt et al.1.234 C. Brassica oleracea. most metals are too insoluble to move freely in the vascular system so they usually form carbonate. Finally. From these studies. . Results to date suggest that the cost of phytoremediation of mercury-contaminated soils will be one-tenth to one-hundredth the cost of other traditional engineering methods. bacterial and animal sources that can enhance the metal-accumulating potential of the plants in which these genes are inserted. 1995). Alkorta / Bioresource Technology 77 (2001) 229±236 very clear and needs further substantiation (Salt et al. These plants are often endemic to these types of soils. to point out that although phytoextraction is still an active topic of research. and still others are looking at the direct insertion of novel genes to enhance the metabolic capabilities of a variety of plants (Newman et al. 1995). 1997). 1998). 1989).. Ni. The number of metal-accumulating taxa identi®ed to date has been reported to be 397 (Salt et al.. it is believed that plant uptake of certain mineral nutrients such as Fe and Mn may be facilitated by rhizospheric microorganisms (Barber and Lee. Similar results may be found for non-essential heavy metals.. take a relatively long time of continuous cultivation (13±14 years) to clean a site of Ni or Zn (Salt et al. Besides. there is increased support for the idea that genetically modi®ed plants can play an important role in extracting heavy metals from contaminated sources (Mo€at.. 1989). Rugh et al. sulfate or phosphate precipitates immobilizing them in apoplastic (extracellular) and symplastic (intracellular) compartments (Raskin et al. Senden et al. In addition. Cu. others are creating protoplastfusion hybrids. 1997). The ®rst hyperaccumulators characterized were members of the Brassicaceae and Fabaceae families. 1994).. 1991). 1974. 4. Microbes associated with phytoextraction Plant-assisted bioremediation has been mainly concerned with the degradation of organic pollutants and the use of microorganisms to improve the plant±metal uptake from soils has hardly been investigated. Although the largest numbers of temperate-climate hyperaccumulating species belong to the Brassicaceae (Baker and Brooks. one of the goals of plant genetic engineering is to enhance the ability of plants to metabolize many of the compounds that are of environmental concern. there is a continuous search for novel phytoextracting plants adapted to particular ecosystems and climates.. (1996) reported the production of a mercury-resistant transgenic plant that volatilized mercury into the atmosphere. 1995). 1989. such as Thlaspi caerulescens (Brassicaceae) (Baker et al. Several examples of ®eld trials for the continuous phytoextraction of metals have been reported: Thlaspi caerulescens and Silene vulgaris for Cd and Zn. 1993). it can be concluded that by populating the rhizosphere with selected microorganisms during the phytoextraction. However. 4... Brooks et al. Baker et al. However. Most metal-accumulating plant species known today were discovered growing on soils containing high levels of heavy metals. respectively (Baker et al. 1998). it is important to emphasize that even the best metal accumulators. The majority of hyperaccumulating species discovered so far are restricted to tropical areas (Baker and Brooks. 1995) have demonstrated that the ability to accumulate heavy metals varies greatly between species and between cultivars within a species.2. Crowley et al.. Cd. 1996). suggesting that metal accumulation is associated with heavy metal resistance (Baker and Brooks. Actually. 1997). By inserting an altered mercuric ion reductase gene (merA) into Arabidopsis thaliana. Garbisu. Genetics of phytoextraction One way to supplement the arsenal of plants available for remedial actions is to utilize genetic engineering tools to insert into plants those genes that will enable the plant to metabolize a particular pollutant (Newman et al. respectively (Brown et al. Alyssum lesbiacum. In fact. Roots can employ rhizospheric organisms (mycorrhizal fungi or root-colonizing bacteria) to increase the bioavailability of metals (Raskin et al. small-scale ®eld trials with wild metal accumulators collected from naturally contaminated soils have demonstrated the feasibility of the phytoextraction approach. Raphanus sativus. the e€ectiveness of metal extraction could increase by one or two orders of magnitude (Ow. Unless the metal ion is transported as a noncationic metal chelate... 1995).. if the high yield and hyperaccumulation traits could be bred into a single plant. Major long-term improvements in phytoextraction should come when scientists isolate genes from various plant. thermal treatments. Metal reactions in plants Once inside the plant. and as mentioned above..

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