Ecological Engineering 18 (2002) 647–658 www.elsevier.com/locate/ecoleng

Phytoremediation: An ecological solution to organicchemical contamination

Sridhar Susarla a, Victor F. Medina b, Steven C. McCutcheon c,*a GeoSyntec Consultants, 1100 Lake Hearn Dr., N.E., Suite 200, Atlanta, GA 30342, USA

b Department of Ci�il and En�ironmental Engineering, Washington State Uni�ersity, 2710 Uni�ersity Dri�e, Richland,WA 99352, USA

c United States En�ironmental Protection Agency, National Exposure Research Laboratory, 960 College Station Road, Athens,GA 30605, USA

Received 30 October 1998; received in revised form 8 February 1999; accepted 23 June 1999

Abstract

Phytoremediation is a promising new technology that uses plants to degrade, assimilate, metabolize, or detoxifymetals, hydrocarbons, pesticides, and chlorinated solvents. In this review, in situ, in vivo and in vitro methods ofapplication are described for remediation of these compounds. Phytoaccumulation, phytoextraction, phytostabiliza-tion, phytotransformation, phytovolatilization and rhizodegradation are discussed and the role of enzymes intransforming organic chemicals in plants is presented. The advantages and constraints of phytoremediation areprovided. Our conclusions is that phytoremediation prescriptions must be site-specific; however, these applicationshave the potential for providing the most cost-effective and resource-conservative approach for remediating sitescontaminated with a variety of hazardous chemicals. © 2002 Elsevier Science B.V. All rights reserved.

Keywords: Chlorinated solvents; Pesticides; Plants; Phytodegradation; Phytoremediation; Rhizofiltration; TNT

1. Introduction

Advances in science and technology have en-abled humans to exploit natural resources to agreat extent, generating unprecedented distur-bances in global elemental cycles. The relativelyrecent introduction of anthropogenic toxic chemi-cals, and the massive relocation of natural materi-als to different environmental compartments

(soils, ground water, and atmosphere), has re-sulted in severe pressure on the self-cleansing ca-pacity of recipient ecosystems. Consequently,accumulated pollutants are of concern relative toboth human and ecosystem exposure and poten-tial impact. Currently, efforts are underway inmany countries to control the release of contami-nants (Schnoor et al., 1995) and to accelerate thebreakdown of existing contaminants by appropri-ate remediation techniques. For example, existingex-situ methods for remediation of contaminatedground waters include extraction and treatmentby activated carbon adsorption, microbes or air

* Corresponding author.E-mail address: Mccutcheon.Steven@epamail.epa.gov (S.C.

McCutcheon).

0925-8574/02/$ - see front matter © 2002 Elsevier Science B.V. All rights reserved.

PII: S0 925 -8574 (02 )00026 -5

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stripping. On the other hand, in situ methodsinvolve stimulation of anaerobic and aerobic mi-crobial activities in the aquifer. All of these tech-nologies involve relatively high capitalexpenditure and manpower as well as long termoperating costs. Hence, efforts are underway todevelop more cost-effective approaches to treatlarge volumes of contaminated natural resourcessuch as soil, ground water and wetlands.

Phytoremediation is an emerging technologythat utilizes plants and then the associated rhizo-sphere microorganisms to remove, transform, orcontain toxic chemicals located in soils, sediments,ground water, surface water, and even the atmo-sphere. Currently, phytoremediation is used fortreating many classes of contaminants includingpetroleum hydrocarbons, chlorinated solvents,pesticides, explosives, heavy metals and radionu-clides, and landfill leachates. According to a re-cent report (Best et al., 1997), approximately 80%of the polluted groundwaters are within 20 m ofthe surface. This suggests that a significant num-ber of sites are potentially suitable for low costphytoremediation applications.

In recent years, a number of articles have ad-dressed the role of plants in remediating contami-nated soils and ground waters (Paterson et al.,1990; Shimp et al., 1993; Schnoor et al., 1995;Simonich and Hites, 1995; Watanabe, 1997).Chang and Corapcioglu (1998) describe howplants promote by various processes the remedia-tion of a wide range of chemicals at toxic wastesites. These processes include: (1) modifying thephysical and chemical properties of contaminatedsoils; (2) releasing root exudates, thereby increas-ing organic carbon; (3) improving aeration byreleasing oxygen directly to the root zone, as wellas increasing the porosity of the upper soil zones;(4) intercepting and retarding the movement ofchemicals; (5) effecting co-metabolic microbialand plant enzymatic transformations of recalci-trant chemicals; and (6) decreasing vertical andlateral migration of pollutants to ground water byextracting available water and reversing the hy-draulic gradient.

In many remediation projects, phytoremedia-tion is seen as a final polishing step following theinitial treatment of the high-level contamination.

However, when contaminants are in low concen-tration, phytoremediation alone may be the mosteconomical and effective remediation strategy(Jones, 1991). Many sites with less toxic contami-nants are suitable for phytoremediation as a long-term solution to the problem. Some advantagesand constraints of phytoremediation are summa-rized in Table 1. This review article focuses onrecent advances made in applications of phytore-mediation to sites contaminated with chlorinatedsolvents, explosives, and pesticides. Additionally,the different processes involved in phytoremedia-tion and the role of certain enzymes is discussed.

2. Methods of application

2.1. In situ phytoremediation

In situ phytoremediation involves placement oflive plants in contaminated surface water, soil orsediment that is contaminated, or in soil or sedi-ment that is in contact with contaminated groundwater for the purpose of remediation. In thisapproach, the contaminated material is not re-

Table 1Advantages and constraints of phytoremediation

Advantages Constraints

Limited to shallow groundIn situwater, soils, and sediments

Passive High concentrations ofhazardous materials can betoxic to plants and animals thatconsume the plantsMass transfer limitationsSolar drivenassociated as with otherbiotreatments

Costs 10–20% of Slower than mechanicaltreatmentsmechanical treatmentsOnly effective for moderatelyFaster than natural

attenuation hydrophobic compoundsHigh public acceptance Toxicity and bioavailability of

biodegradation products is notknownContaminants may be mobilizedFewer air and water

emissions into the ground waterInfluenced by soil and climateConserves naturalconditions of the siteresources

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moved prior to phytoremediation. If the phytomechanism consists of only uptake and accumula-tion as opposed to transformation of a contami-nant, the plants may be harvested and removedfrom the site after remediation for disposal orrecovery of the contaminants. A requirement ofthe in-situ approach is that the contaminant mustbe physically accessible to the roots. This ap-proach generally is the least expensive phytoreme-diation strategy.

2.2. In-�i�o phytoremediation with relocatedcontaminants

For sites where the contaminant is not accessi-ble to the plants, such as contaminants in deepaquifers, an alternate method of applying phytore-mediation is possible. In this approach the con-taminant is extracted using mechanical means,then it is transferred to a temporary treatmentarea where it can be exposed to plants selected foroptimal phytoremediation. After treatment, thecleansed water or soil can be returned to itsoriginal location and the plants may be harvestedfor disposal if necessary. This approach generallywould be more expensive than the more passivemethod described above. Treatment could occureither at the site of contamination or at anotherlocation.

2.3. In �itro phytoremediation

In the first two approaches, live plants are usedfor phytoremediation. A third method of applyingphytoremediation is via components of live plants,such as extracted enzymes. In theory, this ap-proach could be applied in situ under some situa-tions, e.g. applying plant extracts to acontaminated pond or wetland, or through use ofon enzyme impregnated porous barrier in a con-taminated ground water plume. More likely, thisapproach could also be applied to contaminatedmaterial that has been relocated to a temporarytreatment area, as described in Section 2.2. Theo-retically, this approach would be the most expen-sive method of phytoremediation because of thecosts of preparing/extracting the plant enzymes;however, in some plants, such as tarragon,

(Artemisia dracunculas var satiya), exudates arereleased under stress that could result in reducedproduction costs. One important factor to con-sider for this approach is the length of time theenzymes remain active for breakdown ofcontaminants.

3. Mechanisms of phytoremediation

There are numerous mechanisms by whichplants may remediate contaminated sites. In somecases, the transformation takes place by live plantsas described in Section 2.1 and Section 2.2. Someof the chemicals that can be treated by thesemechanisms are listed in Table 2. Plant exudatesor enzymes that are responsible for the breakdownof compounds are summarized in Table 3 andTable 4.

Some of the factors affecting chemical uptakeand distribution within living plants include: (1)physical and chemical properties of the compound(e.g. water solubility, vapor pressure, molecularweight, and octanol-water partition coefficient,Kow); (2) environmental characteristics (e.g. tem-perature, pH, organic matter, and soil moisturecontent); (3) plant characteristics (e.g. type of rootsystem, and type of enzymes). Some of the mecha-nisms used by plants to facilitate remediationinclude: phytoextraction, phytopumping, phy-tostabilization, phytotransformation/degradation,phytovolatilization, and rhizodegradation, whichare described in the following sections.

3.1. Phytoextraction/phytoaccumulation

Phytoextraction is the removal of a contaminantfrom the soil, ground water or surface water bylive plants. Phytoaccumulation occurs when thecontaminant taken up by the plant is not degradedrapidly or completely, resulting in an accumula-tion in the plant. Certain plants hyperaccumulatemetals (e.g. nickel, zinc, copper, chromium), andradionuclides. Heavy metal hyperaccumulation isdefined as accumulation of more than 0.1% by dryweight in plant tissue (0.01% for cadmium. Hyper-accumulation of more common elements suchas iron and manganese is defined as more

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Table 2Phytoremediation mechanisms

Chemicals TreatedType

Cadmium, chromium, lead, nickel, zinc and other heavy metals, selenium, radionuclides; BTEXPhytoaccumulation/(benzene, ethyl benzene, toluene and xylenes), pentachlorophenol, short-chained aliphatic compounds,phytoextraction,and other organic compoundsMunitions (DNT, HMX, nitrobenzene, nitroethane, nitromethane, nitrotoluene, picric acid, RDX,Phytodegradation/

phytotrans- TNT), atrazine; chlorinated solvents (chloroform, carbon tetrachloride, hexachloroethane,tetrachloroethene, trichloroethene, dichloroethene, vinyl chloride, trichloroethanol, dichloroethanol,formationtrichloroacetic acid, dichloroacetic acid, monochloroacetic acid, tetrachloromethane, trichloromethane),DDT; dichloroethene; methyl bromide; tetrabromoethene; tetrachloroethane; other chlorine andphosphorus based pesticides; polychlorinated biphenols, other phenols, and nitrilesProven for heavy metals in mine tailings ponds and expected for phenols and chlorinated solventsPhytostabilization(tetrachloromethane and trichloromethane)Polycyclicaromatic hydrocarbons; BTEX (benzene, ethylbenzene, toluene, and xylenes); otherPhytostimulationpetroleum hydrocarbons; atrazine; alachlor; polychlorinated biphenyl (PCB); tetrachloroethane,trichloroethane and other organic compoundsChlorinated solvents (tetrachloroethane, trichloromethane and tetrachloromethane); mercury andPhytovolatilizationseleniumHeavy metals, organic chemicals; and radionuclidesRhizofiltration

than 1% of the element by dry weight in planttissue (0.01% for Cadmium). In the process ofhyperaccumulating contaminants (Dushenkov etal., 1995), some plants can remediate the contam-inated soils to acceptable levels.

Some plants can grow in contaminated areasand tolerate hyperaccumulation of metals andother contaminants such as perchlorate (Susarlaet al., 1999). Other plants may die or experiencesevere stress under conditions of hyperaccumula-tion. Less tolerant plants can still be used in areasof contamination then harvested and disposedafter these plants have hyperaccumulated the con-taminant to their maximum extent. Such cropscan be replanted, if necessary, to complete thisremediation. Another option is to recover thecontaminant after harvesting the plants(Dushenkov et al., 1995; Nanda Kumar et al.,1995; Moffat, 1995; Kelley and Guerin, 1995;Cornish et al., 1995; Wang et al., 1995; Banueloset al., 1998). If the remediation goal is to harvestafter these plants hyperaccumulate a contaminant,then it is desirable for the selected plants to beable to translocate the contaminant from the rootinto above ground tissue, such as shoots andleaves (Nellessen and Fletcher, 1993). If the con-taminant remains in the roots, harvesting for dis-posal or recovery may be more difficult.

3.2. Phytopumping and water balance control

Phytopumping is another mechanism that canbe used to remove or minimize migration of con-taminants. In this case, plants are used as organic‘pumps’ to pull-in large volumes of the contami-nated water as part of the transpiration process.The result is reduced migration of the contami-nant in ground water, in addition to potentialuptake. Plants that are capable of removing largeamounts of water from the soil are best for thispurpose. For example, the willow tree (Salix spp.)may use up to 200 liters of water per day (Gatliff,1994). Plants having these characteristics mayprovide an inexpensive alternative to mechanicalpump and treat systems for contaminated groundwater in shallow aquifers (Gatliff, 1994; Licht,1995).

3.3. Phytostabilization

Phytostabilization is another mechanism thatcan be used to minimize migration of contami-nants in soils. This process takes advantage ofplant roots ability to alter soil environment condi-tions, such as pH and soil moisture content.Many root exudates cause metals to precipitate,

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thus reducing bioavailability. One advantage ofthis strategy over phytoaccumulation is the dis-posal of the metal-laden plant material is notrequired. By choosing and maintaining an appro-priate cover of plant species, coupled with appro-priate soil amendments, it may be possible tostabilize certain contaminants (particularlymetals) in the soil (Cunningham et al., 1995), andreduce the interaction of these contaminants withassociated biota.

3.4. Phytotransformation/phytodegradation

A contaminant can be eliminated viaphytodegradation or phytotransformation byplant enzymes or enzyme co-factors (Dec andBollag, 1994; Strand et al., 1995). Dec and Bollag(1994) describe plants that can degrade aromaticrings in the absence of microorganisms. Polychlo-rinated biphenyls (PCBs) have been metabolizedby sterile plant tissues. Phenols have been de-graded by plants such as horseradish, potato(Solanum tuberosum), and white radish (Raphanussati�us) that contains peroxidase (Dec and Bollag,1994; Roper et al., 1996). Poplar trees (Populusspp.) are capable of transforming trichloro-ethylene in soil and ground water (Strand et al.,1995; Newman et al., 1997). Enzymes of particu-lar interest for phytoremediation include: (1) de-halogenase (transformation of chlorinatedcompounds); (2) peroxidase (transformation ofphenolic compounds); (3) nitroreductase (trans-

formation of explosives and other nitrated com-pounds); (4) nitrilase (transformation of cyanatedaromatic compounds); and (5) phosphatase(transformation of organophosphate pesticides).

3.5. Phyto�olatilization

Phytovolatilization is a mechanism by whichplants convert a contaminant into a volatile form,thereby removing the contaminant from the soilor water (Terry et al., 1995) at a contaminatedsite. For example, plants, possibly in associationwith microorganisms, can convert selenium todimethyl selenide. Dimethyl selenide is a lesstoxic, volatile form of selenium. Phytovolatiliza-tion may be a useful, inexpensive means of remov-ing selenium from sites contaminated with highconcentration selenium wastes. Similarly, sometransgenic plants (e.g. Arabidopsis thaliana) haveconverted organic and inorganic mercury salts tothe volatile, elemental form (Watanabe, 1997).

3.6. Rhizodegradation

Rhizodegradation is a biological treatment of acontaminant by enhanced bacterial and fungalactivity in the rhizosphere of certain vascularplants. The rhizosphere is a zone of increasedmicrobial density and acitivity at the root/surface,and was described originally for legumes byLorenz Hiltner in 1904 (Curl and Truelove, 1986).Plants and microorganisms often have symbiotic

Table 3Plant enzymes that have a role in transforming organic compounds

Plants known to produce enzymatic activityEnzyme Application

Dehalogenase Dehalogenates chlorinated solventsHybrid poplar (Populus spp.), algae (various spp.),parrot feather (Myriophyllum aquaticum)

Laccase Cleaves aromatic ring after TNT is reduced toStonewort (Nitella spp.), parrot-feathertriaminotoluene(Myriophyllum aquaticum)

Willow (Salix spp.)Nitrilase Cleaves cyanide groups from aromatic ringsHybrid poplar (Populus spp.), Stonewort (NitellaNitroreductase Reduces nitro groups on explosives and otherspp.), parrot feather (Myriophyllum aquaticum) nitroaromatic compounds, and removes nitrogen

from rings structuresDegradation of phenols (mainly used in wastewaterPeroxidase Horseradish (Armoracia rusticana P. Gaertner,treatment)Meyer & Scherb)

Giant duckweed (Spirodela polyrhiza) Cleaves phosphate groups from largePhosphataseorganophosphate pesticides

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Table 4Plant species used in phytoremediation of organic compounds

ReferencePlant species Contaminant

Hexachlorobenzene, PCBs, pentachlorobenzene,Barley (Hordeum �ulgare L. cv. Klages) McFarlane et al.,1987trichlorobenzene

Forage grasses Chlorinated benzoic acids Siciliano andGermida, 1998Best et al., 1997Parrot feather Tetrachloroethane (PCE), Trichloroethane (TCE), TNTBurken and Schnoor,Atrazine, nitrobenzene, TCE, TNTHybrid poplar1997

Prairie grass Topp et al., 19892-chlorobenzoic acidBromacil, nitrobenzene, phenolSoyabean (Glycine max [L.] Merr. Cv. Fletcher et al., 1990

Fiskby v)TNTEurasian watermilfoil (Myriophyllum Hughes et al., 1997

spicatum)Roy and Hanninen,Pentachlorophenol, PCE, TCEWaterweed (Eichhornia crassipes)1994

relationships making the root zone or rhizospherean area of very active microbial activity (Ander-son et al., 1993, 1994; Schwab et al., 1995; Jordahlet al., 1997; Siciliano and Germida, 1998). Plantscan moderate the geochemical environment in therhizosphere, providing ideal conditions for bacte-ria and fungi to grow and degrade organic con-taminants. Plant litter and root exudates providenutrients such as nitrate and phosphate that re-duce or eliminate the need for costly fertilizeradditives. Plant roots penetrate the soil, providingzones of aeration and stimulate aerobicbiodegradation.

Many plant molecules released by root die backand exudatation resemble common contaminantschemically and can be used as co-substrates. Forexample, phenolic substances released by plantshave been found to stimulate the growth of PCB-degrading bacteria (Fletcher et al., 1993; Donnellyand Fletcher 1994a; Fletcher and Hegde, 1995;Fletcher et al., 1995). Recent studies have de-scribed enhanced degradation of pentachlorophe-nol in the rhizosphere of wheat grass (Agropyroncristatum) (Ferro et al., 1994), increased initialmineralization of surfactants in soil-plant cores(Knabel and Vestal, 1992), and enhanced degra-dation of TCE in soils collected from the rhizo-spheres. Anderson et al., (1993) provides a reviewof microbial degradation in the rhizosphere. Thus,current research suggests the interaction between

plants and soil microbes may be an importantfactor influencing biological remediation of con-taminated soils.

3.7. Combined mechanisms

In many cases, phytoremediation involves com-binations of the mechanisms described above. Forexample, phytoextraction and phytovolatilizationhave been credited with the removal of excessselenium in soil (Cornish et al., 1995). It is likelythat both processes occur simultaneously. Thetreatment of TCE in ground water using poplartrees requires extraction of the ground water bythe plant (phytoextraction) that will also degradeTCE (phytodegradation) within the plant. An-other example is degradation of PCB’s by plantcells (Fletcher et al., 1987), as well as by microor-ganisms stimulated by plants (Fletcher et al.,1993; Donnelly and Fletcher, 1994b; Fletcher andHegde, 1995; Fletcher et al., 1995), creating theopportunity to combine phytodegradation andrhizodegradation.

4. Applications of phytoremediation

Selected examples of the application of phytore-mediation for hazardous chemicals using thepreviously described mechanisms are listed inTable 5.

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4.1. Munitions

Numerous researchers have documented theability of plants to take-up and transform trini-trotoluene (TNT) from soil and water (Palazzoand Leggett, 1986; Folsom et al., 1998; Cataldoet al., 1989; Young, 1995; Mueller et al., 1995;Schnoor et al., 1995; Medina and McCutcheon,1996; Best et al., 1997; Medina et al., 1998).Axenic studies have shown that plants are capa-ble of transforming TNT without microbial con-tribution (Vanderford et al., 1997; Hughes et al.,1997). However, very little accumulation of TNThas been found in plant material (Hughes et al.,1997; Vanderford et al., 1997). The rates of phy-totransformation compare favorably to those ofpublished microbial studies, and there appears tobe no lag phases in plant based TNT remedia-tion (Medina and McCutcheon, 1996).

Hughes et al., (1997) provided the first confir-mation that plants have the intrinsic capacity totransform TNT. In their experiments, axenic par-rot feather (Myriophyllum spicatum) was used todemonstrate transformation and to determinemass balances using radiolabeled TNT. The re-sults showed that complete mineralization of theTNT was not observed, but that no TNT or2-amino-4,6-dinitrotoluene or 4-amino-2,6-dini-trotoluene were indentified in extracellular mediaor tissue extracts. However, several unidentifiedmetabolites were observed in the plant. The un-known characteristics of these transformationproducts are of concern in the potential use ofphytoremediation for sites contaminated withTNT. Vanderford et al. (1997) reported thatTNT accumulated primarily in the roots of ax-

enic parrot feather (Myriophyllum aquaticum). Asincubation time increased, the plant-bound radi-olabelled fraction, consisting largely of uniden-tified transformation products, becameincreasingly more difficult to extract. Anotherconcern is that some species selected for labora-tory-scale testing that performed satisfactorily,such as Eurasian water-milfoil, are aggressivenon-native species (Godfrey and Wooten, 1981).Establishment and spread of many of these non-native plant species have resulted in considerableeconomic burden and environmental degradationby displacing valuable native plant and animalspecies.

Pilot studies have been conducted to determinethe treatment performance of TNT-contaminatedground water by constructed wetlands. In orderto model the disappearance of TNT and the as-sociated breakdown, a pseudo-first order, non-re-versible reaction, finite difference model was usedwith batch-scale experiments to determine disap-pearance kinetics for individual species (Medinaand McCutcheon, 1996). The results of themodel suggested that reasonably sized wetlandscould treat a waste stream with an influent TNTconcentration of 2.25 mg l−1 at flow rates rang-ing from 40 to 20 000 l min−1. Continuous, flow-through pilot systems treating 0.001 to 0.01 gl−1 solutions of TNT resulted in rapid removalof TNT at a retention time of 12 days (Medinaet al., 1998). However, aminodinitrotoluene(ADNT), a transformation product, was iden-tified in the effluent of the reactor. Increasing theresidence time to 76 days decreased but did noteliminate the effluent concentration of ADNT.No TNT was found in extractions from the plant

Table 5Examples of phytoremediation test sites (EPA, 1996)

Medium PlantApplicationLocation Contaminants

Phytoextraction PAHs Soil,Ogden, UT Alfalfa (Medicago sati�a), hybridgroundwater poplar trees

PAHs SoilPortsmouth, VA Rhizofiltration, phytodegradation Grasses, clover (Trifolium spp.)TNT Duckweed, parrot featherGroundwaterMilan, TN PhytodegradationTCE, PCE Hybrid poplar treesGroundwaterOrganic pumpingAberdeen, MD

phytovolatilization rhizofiltration

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tissue. However, small concentrations (up to0.74�0.133 mg/kg) of ADNT, as well as sometrinitrobenzene (up to 0.087�0.031 mg/kg), anda small concentration of 3,5-dinitroaniline (up to0.080�0.020 mg/kg) were found in plant tissues.

Thompson et al. (1998a) investigated the use ofhybrid poplar trees (Populus deltoides × nigraDN34) to treat soil contaminated with TNT. Insoil, TNT uptake was governed by its ability tobinding to soil particles (Thompson et al., 1998b).When the plant accumulated small amounts ofTNT, which remained primarily in the roots, thecontaminant was transformed during a 10-dayexperiment. A small amount of TNT was translo-cated to the leaves during the same period of time.However, in aqueous experiments more TNT wastaken-up by the same plant. The accumulatedTNT was transformed to 2-amino-4,6-dinitro-toluene, and 4-amino-2,6-dinitrotoluene, and intounidentifiable, insoluble, polar compounds thatwere bound in the plant tissue. The TNT also wasfound to have measurable toxic effects on hybridpoplar trees (Thompson et al., 1998b). However,removal and degradation rates were rapid enoughto justify using poplar trees as an experimentaltreatment technology for TNT based on biomassproduction.

Much less work has been done on the treatmentof other munitions, such as hexahydro-1,3,5-trini-tro-1,3,5-triazine (RDX) and octahydro-1,3,5,7-te-tranitro-1,3,5,7-tetraocine (HMX). However,preliminary results suggest that treatment of thesecompounds via plants is not as successful as phy-toremediation of TNT (Best et al., 1997; Medinaet al., 1998; Sikora et al., 1998). Results of at leastone study suggest phytodegradation of nitroglyc-erin can be accomplished (Goel et al., 1997). Inconclusion, phytoremediation of TNT is promis-ing due to rapid removal coupled with extensivetransformation rather than phytoaccumulation.Unfortunately, the exact toxicity of the transfor-mation byproducts is not understood. Further-more, the formation and temporary accumulationof amino dinitrotoluenes needs investigation. Fi-nally, more work is needed to investigate thetreatment of other munitions, particularly RDXand HMX.

4.2. Chlorinated sol�ents

Chlorinated solvents, such as TCE and PCE,are major contaminants of the soil and groundwater in the US. They are used in many forms,including as anesthetics by the medical commu-nity, degreasers by industry and the military, sol-vents by the dry cleaning industry and otherforms by the general public. Past widespread useand indiscriminate disposal make chlorinated sol-vents the most common pollutants in the country.Phytoremediation has been applied successfully totreat sites contaminated with chlorinated solvents.The initial data on TCE degradation in plant–rhi-zosphere–soil systems provided a strong incentiveto explore the general interactions between thesoil, plant, root and associated microbes, in addi-tion to the variables that may influence biodegra-dation of waste chemicals in surface andnear-surface soils. Later work by Anderson andWalton (1995) indicated that TCE is oxidizedmore readily in the rhizosphere of certain types ofplants, such as pine (Pinus spp.) or legumes, ascompared with unvegetated soil. However, themineralization of TCE was limited. Uptake ofTCE by plant roots was correlated with wateruptake, but total uptake was small and transloca-tion insignificant. Others have reported thatplants also take up TCE vapor volatilized fromthe soil (Newman et al., 1997).

Strand et al. (1995) demonstrated that hybridpoplar trees have the capability to assimilate anddegrade the chlorinated solvent TCE to the aero-bic degradation products 2,2,2-trichloroethanol,trichloroacetic acid, and dichloroacetic acid. Inthat study, dichloroacetic acid detected in leaftissues was the most prominent metabolite. Insimilar studies, Schnabel et al. (1997) investigatedthe uptake and transformation of TCE by ediblegarden plants. Carrots (Daucus carota �ar. sati�a),spinach (Spinacia oleracea), and tomatoes (Ly-copersicon esculentum) were exposed to [14C] radi-olabeled and unlabeled TCE. Most of the TCE(74 to 95%) was volatilized through the plants.The remaining TCE was adsorbed to soil parti-cles. Very small, non-extractable amounts (1 to2%) of the [14C]-label were found in the planttissue. This suggested that the TCE was taken-up,transformed, and bound to the plant material.

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Newman et al. (1997) were first to report degra-dation of TCE into several known oxidizedmetabolites in hybrid poplar plant tissues, anddemonstrated the potential for the use of poplarsfor in situ remediation of TCE. In their study,axenic poplar cell cultures were used to eliminateany aspects of microbial degradation. Recently,the uptake and transformation of TCE, PCE, andother chlorinated solvents were examined in anumber of aquatic plants including waterweed(Elodea canadensis), parrot feather (M.aquaticum) and giant duckweed (Spirodelapolyrhiza). Rennels (1995) also reported that theseaquatic plants take-up TCE and PCE, then breakthe chemicals down to a number of compounds.These results support the potential usefulness ofaquatic plants in the removal of chlorinated con-taminants from contaminated ground and surfacewaters. Although the studies referenced abovemade significant contributions to the understand-ing of phytotransformation of chlorinated sol-vents, additional research is necessary to evaluatethe long-term field performance of these plants, aswell as the effects on animals that may use theseplants.

4.3. Other aromatic compounds

Chlorinated aromatics, including pesticides,such as atrazine and 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane (DDT), are common con-taminants in soils, surface and ground waters.Phytoremediation has been effective in treatingthese types of contaminants. For example, theuptake and translocation of phenol, nitrobenzeneand bromocil were related directly to transpira-tion rate in mature soybean plants (McFarlane etal., 1987). Recently, the use of minced horseradishroots has been proposed for the decontaminationof surface waters polluted with chlorinated phe-nols (Roper et al., 1996). In sealed-batch experi-ments using waterweed, p,p�-DDT and o,p�-DDTwere degraded (Garrison et al., 1996) with 1,1-dichloro-2-(o -chlorophenyl) -2-(p-chlorophenyl)-ethane (o,p= -DDD) and 1,1-dichloro-2-(p-chlorophenyl)-2-(p-chlorophenyl)ethane (p,p= -DDD) appearing as metabolite products. No

accumulation of DDD was observed during thecourse of the experiments. Burken and Schnoor(1997) used poplar trees for uptake andmetabolism of the pesticide atrazine. Results in-dicted that poplar trees can take-up, hydrolyze,and dealkylate atrazine to less toxic metabolites.In this study, the parent compound atrazine, and[14C]-radiolabeled metabolites were separated andidentified for the first time. Transformation oc-curred in roots, stems, and leaves. These findingssuggest that hybrid poplar trees have potential forphytoremediation of sites contaminated withatrazine.

5. Conclusions

5.1. Constraints of using plants for remediation ofhazardous wastes

Despite the diversity of potential options, phy-toremediation is in its infancy. The majority ofthe research has been conducted in laboratoriesunder relatively controlled conditions for shortperiods of time. More extensive research underfield conditions for longer durations is requiredfor a better understanding of the potential role ofphytoremediation. A limiting factor of phytore-mediation treatment includes the fact that a spe-cific phytoremediation ‘prescription’ cannot beapplied to every site with a certain chemical con-taminant because different site-specific conditions(e.g. soil and climate) may not be suitable for thetarget plant. Plants also interact with and areaffected by other living organisms such as insects,pests and pathogens, and exposure of plants tocontaminants and related stresses can make thephyto treatment more susceptible to these otheragents, ultimately influencing the outcome of phy-toremediation attempts. Additionally, phytoreme-diation generally is restricted to sites where theconcentration levels of contaminants are not toxicto the plants proposed for remediation. Finally,the contaminants must be accessible to the tissueresponsible for uptake (e.g. root system) in plants.As a result, in situ phytoremediation using liveplants is restricted to sites conducive to growth ofthe selected plant with the contaminant located

S. Susarla et al. / Ecological Engineering 18 (2002) 647–658656

within the potential root zone of the selectedplant.

5.2. Ad�antages of using plants forphytoremediation of organic chemicalcontaminated sites

Despite constraints referenced above, plantshave many features that result in a high potentialfor environmental cleanup. Energy costs and ex-penses are reduced and natural resources are con-served because plants use solar energy. Plants areadapted to a wide range of environmental condi-tions and are capable of modifying conditions ofthe environment to some extent. The unique en-zyme and protein systems of some plant speciesappear to be beneficial for phytoremediation. Ad-ditionally, since plants lack the ability to move,many plants have developed unique biochemicalsystems for nutrient acquisition, detoxification,and controlling local geochemical conditions.Some plants that grow well in nutrient poor soilsmay have useful mechanisms for removing andtransforming contaminants that resemble certainnutrients. Infiltration is a primary pathway incontaminant migration to ground water, andplants play an important role in regulating watercontent in soil. Plant roots aerate the soil, whichmay stimulate microbial activity in the soil. Rootexudates may be a nutrient source for microor-ganisms, since the rhizosphere generally containssignificantly higher numbers and more active mi-croorganisms than similar soils without plants.Thus, plants can contribute in many ways toenhance biodegradation in the soil. Phytoremedia-tion provides an aesthetically pleasing alternativeto structural remediation and decontaminationtechnologies. As a result of these advantages,phytoremediation has considerable potential forenvironmental restoration of contaminated sites.

Acknowledgements

Sydney Bacchus provided information onaquatic plants. The strategic Environmental Re-search and Development Program (Project c720managed by the U.S. Army Waterways Experi-

ment Station), U.S. Air Force Human SystemsCentre, U.S. Air Force Restoration Division, andU.S. Navy Southern Command provided supportduring the writing of this review.

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