E N V l R O N M E N T A L REV1EW
Phytoremediation, Part I:
Fundamental Basis for the Use of
Plants in Remediation of Organic
and Metal Contamination
E. Kudjo Dzantor, Robert G. Beauchamp
Phytoremediation, the use of plant systems for contaminant
cleanup, is among the fastest growing areas of environmental re-
mediation research, technology development, and implementa-
tion. The practice is facilitated by a number of plant adaptations.
First, selected plant species can take up and accumulate certain
metals in their shoots at levels that are toxic to ordinary plants
(hyperaccumulation).The phenomenon i s an evolutionary adap-
tation of specific plant species to natural metal enrichments; con-
sequently, its occurrence is geographically restricted, and the
plant species involved are highly specific with respect to types of
metals tolerated. Other plant species can take up, metabolize and
thereby detoxify certain organic contaminants in their shoots, or
cause their transformations through substances released into
their root zones (rhizospheres).The extent to which an organic
contaminant may be translocated in plants i s determined largely
by i t s partitioning into lipid phases (its lipophilicify), while rhizo-
sphere transformations are determined largely by types and
amounts of plant exudations, and microbial populations that are
stimulated by these exudates. interactions between plant systems
and contaminants that can facilitate phytoremediation are com-
plex, and complicated further by strong influences of climate,
particularly temperature, and matrix factors such as nature and
reactivity of surfaces, pH, and oxidation-reduction statuses. The
ways in which the various factors interact to render a contami-
nant more or less susceptible to phytoremediation are discussed,
with the objective of providing information needed for decision
making when considering phytoremediation for the cleanup of
particular contaminants.
EnvironmentalPractice4:77-87 (2002)
B iologically based technologies, collectively known as
bioremediation, have become either the preferred op-
tions, or approaches that can be integrated with other tech-
nologies for more effective remediation of environmental
contaminants. Biodegradation of organic materials occurs
naturally and is responsible for removing large amounts of
contaminants from the environment. Unfortunately, natu-
ral degradation rates of many man-made (xenobiotic) or-
ganic contaminants are extremely slow, which can lead to
contaminant accumulations and adverse impacts in ecosys-
tems. Practical bioremediation of organic contaminants in-
volves development of schemes that manipulate natural
processes to enhance contaminant removal from the envi-
ronment. Recent advances in bioremediation technology
development have led to strategies that can be used to clean
up contaminants in soil, water, sediments, and gas streams
under a broad range of environmental conditions. In spite
of their versatility, biologically based cleanup technologies
can be limited by extremes of environmental and matrix
conditions. The principal challenge for the bioremediation
practitioner is to determine appropriate technologies for
particular contaminants, and best implementation strate-
gies in the face of specific environmental and matrix condi-
tions, budget constraints, regulatory compliance, and pub-
lic acceptance.
Phytoremediation, the use of plant systems for contaminant
remediation, is a relatively new biologically based approach
that offers great promise for the cleanup of a broad range of
contaminants from organic as well as inorganic sources. In
the first of two articles aimed at the environmental man-
ager, we present current information about the technical
basis for the use of plant systems for remediating organic
and metal contaminants. In the second, we offer a guide for
integrating the technical information into management
Affiliation of authors: E. Kudjo Dzantor, Department of Natural Re-
source Sciences and Landscape Architecture, University of Maryland, Col-
lege Park, Maryland; Robert G. Beauchamp, Environmental Management
Program, Graduate School of Management and Technology, University of
Maryland University College, Adelphi, Maryland
Address correspondence to: E. Kudjo Dzantor, Assistant Professor, Soil
Biochemistry/Bioremediation, Department of Natural Resource Sciences
and Landscape Architecture, University of Maryland, College Park, MD
20742; (fax) 301-314-9041; (e-mail) kd78@umail.urnd.edu.
0 2002 National Association of Environmental Professionals
77
NEWS & INFORMATION
decision-making processes for selecting phytoremediation
as a contaminant cleanup strategy.
Phytoremediation of Organic Contaminants
The potential for using plant systems for the cleanup of or-
ganic contamination is facilitated by processes that are de-
scribed as direct and indirect effects of plants on a contami-
nant. Direct plant effects involve uptake, translocation, and
degradation of a contaminant (phytodegradation), or its
volatilization (phytovolatilization), as well as transforma-
tions caused by chemicals (e.g., enzymes) that plants exude
into the contaminated matrix. Indirect plant effects on a
contaminant involve interactions between plant roots and
microbes through which substrates and growth factors sup-
plied by the plant drive metabolic activities of microbes in
the vicinity of roots (also known as rhizospheres), which in
turn can cause enhanced biodegradation of specific con-
taminants (Cunningham et al., 1996). In nature, direct and
indirect processes usually impact contaminants concur-
rently or sequentially, and the separate effects are not obvi-
ous without scientific investigation. However, the distinc-
tions are not of academic interest only. It is important for
the bioremediation practitioner and manager to know
whether the processes of uptake and metabolism, or en-
hanced rhizosphere degradation result in complete removal
and detoxification of the contaminant, instead of accumu-
lation of equally or more hazardous intermediates within
the plant, or in the contaminated matrix.
Direct Effects of Plants on Organic Contaminants
Uptake and Translocation
The most important factor that controls uptake and subse-
quent translocation of an organic contaminant by plants is
the availability of the compound. This is governed by the
nature of the chemical and its interaction with the contami-
nated matrix. Specifically, the tendency of an organic chem-
ical to partition into lipid phases (i.e., its lipophilicity or fat-
solubility), versus its tendency to dissolve in aqueous phases
(water solubility), is considered to be the most important
characteristic that controls its availability and translocation
in a plant (Bromilow and Chamberlain, 1995). In the labo-
ratory, lipophilicity of a chemical is measured as the
octanol-water partition coefficient (KO,), which is defined
as the ratio of the concentration of a chemical in octanol
(CJ, to its concentration in water (C,), i.e., KO,,, = [C,,]/
[C,], when the contaminant is added to a solution con-
78 Environmental Practice 4 (2) J u n e 2002
taining both octanol and water. Accordingly, a compound
with a low KO, is readily soluble in water, while a compound
with a high KO, is lipophilic.
Research has shown that KO, of a chemical is directly pro-
portional to its uptake by plant roots (Briggs, Bromilow,
and Evans, 1982). This is consistent with partitioning of a
compound into lipid components of roots. In contrast, only
chemicals that fall within a narrow range of K,, can be
translocated within plants. The range of Kowof xenobiotic
contaminants lies between lo-' and iol0,but the optimum
range for uptake and translocation lies between 10' and 10'
(Bromilow and Chamberlain, 1995). KO, is usually repre-
sented in the logarithmic form, thus this optimum range is
between log KO, = 1-3. Below and above the optimum KO,
range, translocation of xenobiotic contaminants in plants
decreases as the result of complex interactions between
plant and chemical characteristics.
The exact mechanism for the occurrence of the seemingly
unusual translocation phenomenon is not completely clear.
Understandably, lipophilic membranes in plant cells could
limit ability of highly polar molecules (highly water-
soluble) to cross into plant vascular systems. Also, high wa-
ter solubility means that a compound does not have any
particular affinity for the root surface to begin with; it may
move toward the root just as well as it may move away from
it-and leach beyond the root zone. The behavior of non-
polar molecules with respect to translocation is not so
straightforward. For compounds with high KO, (KO, >3.5),
sorption onto organic matter in soil and strong affinity for
root surface ensures that availability for translocation is
quite limited to begin with. Then, for reasons that cannot be
explained by their partitioning into lipid membranes alone,
their delivery into plants' endodermis is further restricted
to a point where compounds with KO, > 4 are hardly taken
up into the shoots at all (Bromilow and Chamberlain, 1995).
Such compounds could easily accumulate on root surfaces
(high uptake) with little being translocated to the shoot.
Many common organic contaminants, including pesticides
and some industrial chemicals, have values of Kow that fall
within the optimum range for translocation. Thus, they can
be susceptible to phytodegradation or phytovolatilization
when other conditions are favorable. However, most poly-
chlorinated biphenyls (PCBs), polycyclic aromatic hydro-
carbons (PAHs), and dioxins fall in the log KO, range of 4
and 10. Accordingly, efforts at using phytoremediation for
their cleanup are most likely to be successful when they fo-
cus on enhanced rhizodegradation strategies.

Metabolisrnflra nsforrnation
Once they have entered into plants, xenobiotic compounds
may travel through the plant and be volatilized and/or they
may be metabolized through various mechanisms. The
types of enzymes and metabolic schemes that plants use to
metabolize xenobiotic compounds are so similar to animal
metabolism of foreign substances by the liver, as to earn
plants the description of green livers (Sandermann, 1992).
Indeed, plant metabolism and detoxification of xenobiotic
organic compounds is the basis of selective use of herbicides
to control weeds in crop production. For example, the ex-
tensive use of the herbicide atrazine in the production of
corn and sorghum is facilitated by the crops’ abilities to
transform the herbicide, mainly through enzymatic conver-
sions, into non-phytotoxic intermediates (Shimabukuro,
1968; Shimabukuro et al., i97i), while the weeds that the
herbicide controls cannot perform the same conversions.
In extensive studies of plant metabolism using tissue
cultures of soybean and wheat, Sandermann, Scheel,
and Trenck (1984) reported enzymatic transformations
of a broad range of environmental chemicals, including
2,4-dichloroacetic acid (2,4-D), 2,4,5-trichloroacetic acid
(2,4,5-T), hexachlorobenzene (HCB), pentachlorophenol
(PCP), DDT, and benzo[a]pyrene into conjugates, some of
which were further metabolized, incorporated into lignin,
or deposited in vacuoles. Based on those studies and nu-
merous others reported by researchers elsewhere, KomoBa,
Langebartels, and Sandermann (1995) suggested a concep-
tual division of plant metabolism of xenobiotic compounds
into initiation, conjugation, and compartmentalization
phases. Initiation of xenobiotic transformation is domi-
nated by oxidation reactions that can lead to direct struc-
tural modification and detoxification of some compounds,
or activation of others. The overall strategy behind oxida-
tion reactions is to render non-polar chemicals more polar
so they can be eliminated, or to make them more reactive
and therefore more prone to further reactions (i.e., conju-
gation reactions), which can lead to their ultimate deactiva-
tion. In addition to oxidations, the initiation phase for some
xenobiotic contaminants involves hydrolytic reactions, and
less commonly, reductive reactions.
Some of the more recent research and reviews on the en-
zymes and mechanisms involved in plant metabolism of or-
ganic compounds was lately published by the American
Chemical Society, based on a 1999 symposium on the sub-
ject (ACS Symposium Series 777,2001).A detailed examina-
tion of those proceedings is beyond the scope of these dis-
cussions. However, a brief mention of reduction reactions,
NEWS & INFORMATION
which are the least common of the initial phase reactions
in plant metabolism, is important in this context because
reduction reactions are directly relevant to the phyto-
remediation of nitroaromatic compounds such as 2,4,6-
trinitrotoluene (TNT). For example, Schnoor et al. (1995)
reported a study in which introduction of the Eurasian mil-
foil Myriuphyllum spicatum into a flooded mesocosm of
TNT-contaminated soil caused a decrease in dissolved TNT
concentration from a saturating and toxic level of 128 ppm
to 10 ppm within one week. This decrease was accompanied
by the ability of the aqueous phase of the mesocosm to sup-
port aquatic species. The disappearance of TNT was attrib-
uted to the enzyme nitroreductase detected in the milfoil;
however, the report did not mention reduced intermediates,
if any, found in the mesocosms. Evidence that TNT was ac-
tually taken up and transformed by Eurasian milfoil and the
related parrot feather (Myriuphyllum aquaticum) was re-
ported by Hughes et al. (1997).These authors reported small
amounts of reduced products (aminated nitrotoluenes) in
the extracellular medium and tissue extracts. In addition
to milfoil, Schnoor et al. (1995) listed stonewort (Nitella),
duckweed (Lemna minor), and hybrid poplars (Populus
spp.) among plants showing nitroreductase activity and
abilities to transform TNT. In laboratory experiments using
soil and hydroponic systems, up to 75% of TNT taken up by
hybrid poplars ended up in root tissue, where it was trans-
formed into reduced intermediates (aminotoluenes) and
unidentified products (Thompson, Ramer, and Schnoor,
1998). Up to 10% of the compound was translocated into
leaves. Still, the presence of metabolites in tissues caused the
investigators to issue the standard caution associated with
phytoremediation strategies based on phytodegradation:
the need to consider the fate and toxicities of metabolites.
In the final phase of plant metabolism of xenobiotic sub-
stances, products resulting from the initiation and conjuga-
tion phases (conjugates) are processed and incorporated
into polymers (biopolymers), which in turn are compart-
mentalized or deposited or stored within plant tissue. Solu-
ble conjugates are stored in vacuoles and insoluble conju-
gates are stored in cell walls (Sandermann, Scheel, and
Trenck, 1984). In animals, liver metabolism usually leads to
production of conjugates that are water-soluble and thus
excreted.
Transformations by Exuded Plant Enzymes
In addition to metabolism within the plant, contaminants
can also be transformed outside the plant by enzymes that
are exuded into a contaminated matrix, so-called ex pluntu
Phytoremediation, Part I 79
transformations (Cunningham et al., 1996). The most fre-
quently cited of these reactions involve peroxidase and lac-
case enzymes that catalyze polymerization reactions leading
to incorporation of xenobiotic contaminants into organic
matter with subsequent losses of toxicities, and to a les-
ser extent, dehalogenase enzymes that catalyze removal of
halogen groups from organic contaminants, resulting in
losses in toxicity. In their compilation of plant species and
contaminant transforming enzymes, Schnoor et al. (1995)
noted the alga, stofiewort, and Eurasian milfoil as species
that possess both laccase and dehalogenase activities.
Most reports on ex planta transformations appear to come
from studies in aquatic and sediment systems. It was sug-
gested that the enzymes performing such transformations
might be sorbed onto plant surfaces to protect them from
destruction or inactivation by toxicants in the environment
(Schnoor et al., 1995) or from degradation by microbial sys-
tems. The relative magnitude of the contribution of such
transformations to overall contaminant dissipation in soil
is not entirely certain.
Indirect Effects of Plants on Organic
Contaminants: Enhanced Rhizosphere
Biodegradation or “Enhanced Rhizodegradation”
Indirect plant effects on xenobiotic compounds are those
brought about by enhanced microbial activities in plant rhi-
zospheres, spurred on by generous endowments of photo-
synthate from plants, and creation of suitable physicochem-
ical environments for transformations to occur. Plants may
exude 12% to 40 YOof their annual photosynthate produc-
tion into their rhizospheres (Whipps, 1990; Whipps and
Lynch, 1986). The amount and variety of these exudates
greatly influences the organisms associated with particular
plants and thus their potentials for use in phytoremediation
of specific contaminants. Some plant root exudates can en-
hance general microbial activity and accelerate biodegrada-
tion of certain contaminants in the process. Other sub-
strates in exudates can cause induction of specific enzymes
in specialized microbes for the enhanced degradation of
more recalcitrant compounds such as PCBs. For example, a
greenhouse study of 17 perennial plant species demon-
strated root exudation of polyphenolic compounds that
were shown in a separate laboratory investigation to sup-
port growth and PCB degradation by competent PCB-
degrading bacteria (Donnelly, Hegde, and Fletcher, 1994;
Fletcher and Hedge, 1995). Although production of the in-
ducing compounds in the greenhouse cultures was gener-
ally 100 to 200 times lower than the amounts that supported
growth of the bacteria in the laboratory, it was concluded
80 Environmental Practice 4 (2) J u n e 2002
that portions of the rhizosphere of one plant, the mul-
berry (Morus rubra) contained sufficiently high enough
phenols to support microbial growth (Fletcher and Hedge,
1995). However, whether the same types and amounts of
exudation and appropriate microbial associations would
combine to cause PCB degradation in the field was not
demonstrated.
In addition to providing substrates, physical and chemical
modifications produced by plant root-microbe interactions
(Tinker and Nye, 2000) can create conditions that favor
degradation of specific contaminants. For example, respira-
tory activities of the plant-microbe complex can lead to cre-
ation of reduced conditions, which promote transforma-
tions such as those involving highly chlorinated or nitroaro-
matic compounds.
Rhizosphere interactions have been investigated for as long
as the disciplines of plant and soil science have existed. Not
surprisingly, the investigations have focused on interactions
as they relate to plant nutrition (Lynch, 1987; Tinker and
Nye, 2000) and plant protection from soil-borne pathogens
(Agnihotri, 1964; Balasubramanian and Rangaswami, 1973;
Ramachandra-Reddy, 1959). Accelerated dissipation of xe-
nobiotic organic compounds under rhizosphere influences
had been known since the early applications of pesticides,
and rhizodegradation had been implicated as the major
mechanism for the dissipation (Hsu and Bartha, 1979).
However, exploitation of the phenomenon for remediating
organic contamination is a relatively recent development.
Logically, the initial surge of research activity to capitalize
on the process involved the search for plants with superior
abilities to enhance rhizodegradation. To date, the searches
have led to species from a broad range of plant families, act-
ing on an equally broad range of chemical families. For ex-
ample, Walton and Anderson (1990) reported accelerated
dissipation of trichloroethylene under mixed vegetation
dominated by a grass, Paspalurn notaturn, a legume, Lespe-
deza cuneata, an herbaceous plant, Solidago sp., and the
Loblolly pine, Pinus taeda. Qiu et al. (1997) reported accel-
erated dissipation of PAHs under rhizosphere influences of
prairie buffalograss (Buchloe dactyloides var. Prairie) and
Kliengrass (Panicurn coloraturn var. Verde), while Banks,
Lee, and Schwab (1999) demonstrated the accelerated disap-
pearance of benzo[a]pyrene in rhizospheres of tall fescue
(Festuca arundinacea Schreber). Recently, our own screen of
eight forage and conservation crops showed enhanced PCB
dissipation under rhizosphere influences of flat pea (Lath-
yrus sylvestris L.), reed canary grass (Phalaris arundinacea
L.), and switchgrass (Panicurn virgatum L.) (Dzantor,
Chekol, and Vough, 2000). We are investigating these plants
further to elucidate the mechanisms involved in their stim-
ulations of PCB dissipation, and exploring strategies for
further enhancement of their potentials.
Phytoremediation of Metal Contaminants
Unlike organic compounds, metals cannot be biodegraded.
Thus, remediation of metal contamination typically in-
volves physical removal processes such as excavation and
subsequent landfilling of contaminated soils, containment
and stabilization in situ, or physicochemical processes such
as leaching or electrochemical mobilization. Unfortunately,
most of these processes have serious limitations. Practices
such as landfilling offer only temporary remedies because
they simply represent contaminant relocation. Additionally,
these methods can be costly, involving risk during trans-
port, and they can be disruptive to a site. Microbial pro-
cesses have been explored for metals remediation (Fran-
kenberger and Losi, 1993); however, potential applications
are limited to a few elements under narrow ranges of condi-
tions. There appears to be increasing recognition that phy-
toremediation offers by far the greatest opportunity for us-
ing natural systems for remediating metals contamination
in an environmentally safe, undisruptive, and aesthetically
pleasing way. For metals with economic value, for example,
nickel and copper, this can be done for profit in a process
termed phytomining (Brooks and Robinson, 1998; Chaney
et al., 2000).
Metal phytoremediation is facilitated by the fact that certain
plants known as hyperaccumulators can take up specific
metals from their growth media and accumulate them in
their above ground parts at levels that are toxic to ordinary
plants. A hyperaccumulator has been defined as a plant with
the ability to yield greater than or equal to 0.1% chromium,
cobalt, or nickel, or greater than or equal to LO% zinc or
manganese in the above ground shoots on a dry weight ba-
sis. The USEPA utilizes specific metals such as nickel, cop-
per, and zinc as benchmarks because approximately 400
known plants favor their accumulation. According to Cha-
ney et al. (i995), some hyperaccumulating plants can accu-
mulate metal such as zinc, nickel, selenium, copper, cobalt,
manganese, and arsenic at levels as high as 1% of their
biomass.
There has long been general agreement that metal hyperac-
cumulation is an evolutionary adaptation by specialized
plants to life in matrices that are naturally rich in specific
minerals. However, the mechanisms of metals uptake, toler-
ance to high metal concentrations, and the exact roles that
high levels of elements play in the survival of hyperaccumu-
lators have continued to be debated. It has been demon-
strated that tolerance to high levels of metals by hyperaccu-
mulators is under genetic control (Macnair, 1993), which
allows the plants to produce specific molecules that react
with metals to form complexes. These complexes can then
be stored away from sensitive tissues. The molecules that
have been implicated in the formations of complexes are
low molecular weight peptides called phytochelatins (Grill,
Winnacker, and Zenk, 1985; Scheller et al., 1987); however,
others have cited the involvement of organic acids, notably
citric, malic, and oxalic acids, in detoxification of metals in
plants (Kersten et al., 1980; Mathys, 1977).
Apart from the competitive advantage of being able to colo-
nize restricted and generally harsh matrix conditions, metal
hyperaccumulation has been credited with a number of
other functions. Baker and Walker (1990) discussed some of
these, in the face of observations that question their validity.
For example, deposition of metal in cell walls and presence
of metal in sap have been suggested as forms of moisture
management strategies under water stress conditions. How-
ever, hyperaccumulators have been found in geographic lo-
cations where water stress would not be of concern. It has
further been suggested that high levels of metals in plants’
foliage may protect plants from herbivores or insects by
making the foliage unpalatable or deadly to the feeding
party, but animals have been found to feed quite readily on
some hyperaccumulators without harmful effects (Baker
and Walker, 1990).
Regardless of questions about the mechanisms and eco-
physiological functions of hyperaccumulation, it is clear
that the phenomenon presents an excellent opportunity for
the cleanup of metals contamination. A 1988 document
cited by Frankenberger and Losi (1993) noted that about
50% of Superfund sites on the USEPA’s Record of Decisions
between 1982 and 1986 contained inorganic contaminants,
mainly heavy metals and metalloids. In order to fully exploit
this phenomenon of hyperaccumulation, it is essential to
distinguish true hyperaccumulators from plants that can
take up luxury amounts of certain elements, or use other
mechanisms that allow them to withstand high levels of po-
tentially toxic concentrations of elements in their growth
media.
Metal hyperaccumulators belong to a diverse range of plant
families that are distributed over areas equally diverse geo-
graphically, but possessing a common characteristic of nat-
ural enrichments for some specific element(s).A review by
Baker and Brooks (1989) listed 26 plant families that contain
Phytoremediation, Part I 81
hyperaccumulators of different metals. The most investi-
gated of these families, the Brassicaceae, includes the genera
Brassica and Thlusppi.One member of the Brassica genus has
been investigated for hyperaccumulation of lead, one of the
most common metal contaminants at Superfund sites, and
for cadmium, selenium, and zinc. For example, Kumar et
al. (1995) reported significant accumulation of lead in both
roots and shoots of B. juncea (108 and 34.5 mg Pblg dry
weight respectively) that was grown in a sand-perlite me-
dium that was enriched with lead. That study and another
study in hydroponic cultures demonstrated the ability of B.
juncea to also accumulate significant amounts of cadmium
in its tissues, with bioaccumulation coefficients (ratio of
metal concentration in plant to concentration of metal in
soil) of up to 175 in the shoots, and 20,574 in the roots when
grown at a non-phytotoxic cadmium concentration (Dus-
henkov et al., 1995; Salt et al., 1995). In other studies, Ba-
nuelos and Meek (i990) demonstrated up to 50% selenium
reductions in the top meter of a selenium-enriched soil that
was cultivated with B. juncea for several years under low ir-
rigation field conditions. Also, Ebbs and Kochian (1997)
showed dramatic increases in shoot accumulation of zinc by
B. juncea when EDTA, a chelating agent, was added to the
soil to increase zinc solubility.
Thlaspi caerulescens, or alpine pennycress, another member
of the Brassicaceae family, has been extensively studied for
its extraordinary ability to take up from soil and hyperaccu-
mulate zinc (up to 4Yo) and cadmium (up to 1%) in its
shoots and leaves. Brooks and Robinson (1998) noted that
zinc and cadmium tend to occur together at many contami-
nated sites. Laboratory studies by Brown et al. (1995) on
7: caerulescens demonstrated efficient translocation of zinc
and cadmium from solution to shoots, with zinc concentra-
tions in harvestable shoots high enough to be considered
low-grade ore. Field tests of 7: caerulescens by Li et al. (1997)
suggested that lowering soil pH favored zinc and cadmium
accumulation in the shoots, with the second harvest show-
ing double the zinc and cadmium accumulations of the
first harvest.
Perhaps the biggest reason why full and large-scale deploy-
ment of metal phytoremediation has lagged behind the
length or intensity of research exploration is the specialized
nature of hyperaccumulators. Because of their unique ad-
aptation to particular environments, optimum conditions
for growth and effective metal uptake of hyperaccumulators
were generally poorly understood initially. Even when these
conditions were understood somewhat, they were not
readily reproducible in the laboratory or in field contami-
nated matrices. In addition to this, hyperaccumulators are
82 Environmental Practice 4 (2) June 2002
usually small plants that produce low biomass, a likely con-
sequence of their unusual adaptation to harsh ecological
niches. So, while the amounts of metal concentration per
unit of plant biomass can be high, the total amounts of
metal removed at a site during a given period can be quite
low. Low yields and slow growth rates have been cited as
limiting factors for the development of effective metal
phytoremediator plants (Brown et al., 1995).
Now, there is increasingly better understanding of the cul-
tural conditions of hyperaccumulators, and management
practices that enhance further their metal uptake capabili-
ties are now integral parts of phytoremediation applica-
tions. Perhaps more importantly, research is progressing in
efforts to address the issue of biomass production through
genetic engineering. Emphasizing the potential role of bio-
technology in the development of metal phytoremediator
plants, Chaney et al. (2000) noted that the ability to hyper-
accumulate and tolerate metals of interest is probably of
greater significance in the long run than high biomass pro-
duction per se. They point out that biotechnology and tra-
ditional breeding techniques may be used to obtain hyper-
accumulator phenotypes with high biomass characteristics
to address the problem of metal removal efficacy. The wide
variety of genotypes of species such as T caerulescens is an
asset, from a biotechnological point of view, since the pool
of genetic traits from which to draw desirable characteris-
tics is large.
The process through which metal hyperaccumulation oc-
curs in plants growing in contaminated matrices has been
termed phytoextraction. The accumulation of metals in
shoots is important for phytoremediation because the metal
must be transported to the harvestable parts of the plant for
removal. However, other phytoremediation schemes being
investigated rely on accumulations of metals in plant tissues
other than shoots. For example, rhizofiltration is a process
that removes metals from surface or groundwater by ab-
sorption, concentration, and precipitation by plant roots
(Dushenkov et al., 1995; Salt et al., 1995). In some applica-
tions, plants are grown in water in greenhouses to develop
adequate root systems. The plants can then be placed in
constructed wetlands or engineered shallow lagoons and
groundwater or wastewater can be pumped through the
system for the removal of metal contaminants. Another
process, phytostabilization, is a process that can limit the
mobility and bioavailability of metals in soil (see review by
Salt et al., 1995).Plants that have a high tolerance for metals
and can grow vigorously in surrounding soils but exhibit
low accumulation of metals may be used as phytostabilizers
by exerting significant hydraulic control over the transport
of the contaminant. This mechanism, while requiring more
research, may be suitable for use as an interim containment
strategy at sites with relatively low contamination levels or
where large-scale removal action is not feasible.
Environmental and Matrix Considerations
for Phytoremediation
Bioremediation methods involve living systems; ac-
cordingly, they are limited in application by climate and
other environmental factors that influence establishment,
growth, proliferation, and specific performance of the bior-
emediation agents (plants, in the case of phytoremedia-
tion). Also, matrix characteristics such as pH, oxidation-
reduction status (redox), composition and distribution of
reactive surfaces, and the presence of multiple and mixed
contamination and/or toxicants, as well as the spatial and
temporal distribution of specific contaminants, interact
with climatic factors to strongly influence a contaminant’s
susceptibilityto phytoremediation.
Climatic Influences on Phytoremediation
Regardless of whether a contaminated site contains organic
or metal contaminants, the climate at a site, in particular
temperature, poses the greatest and most obvious limita-
tion to the applicability of phytoremediation, and for that
matter other biologically based remediation schemes. Tem-
perature dependency of bioremediation has been one of the
major limitations of the technology, especially in temperate
regions where most field bioremediation is limited to the
warmer parts of the year between spring and summer-a
very short time for many biologically based remediation
technologies. Technologies currently exist for warming up
contaminated matrices to allow bioremediation implemen-
tation during cold periods, but it is questionable whether
adoption of such energy-demanding approaches can still
make bioremediation the favored, cost effective alternative
to other remediation schemes.
Matrix Effects on Contaminant Behavior and
Susceptibility to Phytoremediation
The direct effects of matrix characteristics such as adequate
supply of nutrients, optimum ranges of pH, moisture, and
redox on growth of potential phytoremediation plants are
obvious. However, matrix influences on contaminant be-
havior, and therefore susceptibility to phytoremediation,
are quite complex and can be exerted to different degrees
on organic versus inorganic contaminants. In soil, the most
important matrix characteristics that influence contami-
nant behavior are the constitution and organization of the
soil solid phases, pH, and redox. In general, these variables
impact form and availability of contaminants, and thereby
regulate their exposures and susceptibilities to biological
transformation and/or removal processes. In the following
discussion, the individual variables will be considered sepa-
rately and the appropriate emphasis will be placed on the
contaminant type (organic or metal) that is most impacted.
However, it must be emphasized that the behaviors of par-
ticular chemicals in the natural environment are the net re-
sult of complex interactions, rather than the impact of a
single variable.
Constitution and Reactivity of Soil Solids
Soil consists of solid, liquid, and vapor phases, which are all
important in determining contaminant behavior; however,
it is the solid phase that modulates this behavior. The solid
fraction of soils consists of inorganic and organic constit-
uents that control the amounts of contaminant in other soil
phases, and therefore susceptibility to phytoremediation.
The reactivity of the soil solids derives from colloidal frac-
tions ( p m size) that are characterized by immensely large
surface to mass ratios, surfaces that carry charges and func-
tional groups as a result of their formation processes. These
characteristics allow soil colloids to control attraction and
reaction with specific chemicals. In most soils, the inorganic
soil colloids exert the greatest influence on metal availabil-
ity. In temperate regions, this fraction is generally domi-
nated by layered crystal units that carry predominantly neg-
ative charges and hydroxyl (OH-) functional groups. These
characteristics govern not only retention and interactions
of metal contaminants, but also the behavior of the very cat-
ions that are essential for growth of any phytoremediator
plant.
The organic fraction can also influence the availability of
metal contaminants through bonding processes that range
in strength from weak physical bonding to strong chemical
ones. For the most part, organo-metal complexations tend
to reduce availability of metals in soil. This phenomenon
underlies the incorporation of biosolids in soil to stabilize
metal contaminants and prevent their further movement
offsite. Some complexations between organic molecules
and metals can increase mobility and availability of the
metal for uptake. Such complexations, known as chelation,
are the basis of the use of synthetic organic molecules, che-
lates, to increase plant uptake of certain metals (Blaylock et
al., 1997; Ebbs and Kochian, 1997). However, this practice
Phytoremediation, Part I 83
must be used with caution. It is important to couple release
of metal to uptake by plant in order to avoid metal migra-
tion offsite.
The influence of the organic fraction on contaminant be-
havior is exerted on organic contaminants in two different
ways. Many organic contaminants tend to partition into or-
ganic fractions in contaminated matrices. Thus, availability
of the contaminant for plant uptake and metabolism will
depend on the nature of the contaminant (e.g., lipophilicity,
as discussed earlier) and the matrix organic matter content.
On the other hand, soil organic fractions play dominant
roles in microbial growth and bioactivity, and therefore ex-
ert profound influences on contaminant biodegradation,
including enhanced rhizodegradation.
Matrix pH
With the exception of certain groups of pesticides (ionic or
ionizable organic compounds), most of the common or-
ganic contaminants are neutral molecules, and their avail-
ability and/or uptake are not impacted directly by matrix
pH. On the other hand, plants absorb mineral elements in
the ionic form in solution, and presence of these forms is
influenced strongly by matrix pH. In soil, the solution con-
centrations of metal contaminants tend to increase with de-
creasing pH because of their displacement from exchange-
able sites on solid surfaces by increasing activity of hydro-
gen ions ( H + )as acidity increases (i.e., pH decreases). From
a practical standpoint, this can increase the availability of
the contaminant for plant uptake. However, it can also re-
sult in concentrations of certain elements at levels that are
toxic to the bioremediation plant. In fact, in some soils, the
adverse effects of low pH on plants are due to aluminum
toxicity, and not to acidity per se.
The increased availability of metals at low pH has led phy-
toremediation researchers to study incorporation of acidi-
fiers into certain metal contaminated soils to improve the
success of phytoremediation (Li et al., 1997). Such practices
should take into consideration other impacts in the soil, in-
cluding aluminum toxicity and provision of other optimum
growth conditions for the phytoremediation plants. As soil
pH increases, most metal contaminants become increas-
ingly unavailable for plant uptake, largely because of their
precipitation as insoluble hydroxides.
Oxidation-Reduction Status
Most common metal contaminants exist in two or more ox-
idation states in natural matrices, with relative prevalence
84 Environmental Practice 4 (2) J u n e 2002
that is determined by the matrix redox status. The oxidation
state of a metal contaminant also determines its solubility
and relative availability for uptake by plant systems. In gen-
eral, the oxidized forms of most common metal contami-
nants are less soluble and consequengy less available for
plant uptake. The exception to this general observation is
chromium, which is arguably the most celebrated metal
contaminant in recent years, thanks to the movie Erin
Brockovich. In its higher oxidation state, Crh+(denoted as
Cr(V1)) chromium forms salts such as chromates and di-
chromates that are highly water-soluble and thus more
mobile in environmental matrices. In contrast, the lower
oxidation state Cr3+(denotedas Cr(II1)) readily forms in-
soluble and less mobile oxides and hydroxides. Coinciden-
tally, Cr6+is also more toxic than Cr3+.From a strictly phy-
toremediation standpoint, presence of Cr6+would be pre-
ferred for plant uptake. However, a complete environmental
remediation strategy would likely emphasize removal of the
contaminant from the environment by its reduction and
subsequent precipitation as the insoluble, immobile hy-
droxide, Cr(OH), The choice is the remediation practi-
tioner's decision to make-after other considerations.
The influence of redox status of soil on organic contami-
nants is exerted largely through selective enrichment for
aerobic versus anaerobic degradation processes that impact
the contaminant.
Spatial Distribution of Contaminant vis-2-vis Plant
Root Systems
Because of their usually low solubility and their attraction
to soil surfaces, metal contaminants generally tend to re-
main within the conventional plant root zones, and are thus
amenable to uptake when appropriate plant species are em-
ployed. On the other hand, organic contaminants are usu-
ally distributed throughout a soil profile to as far down as
below water tables. When phytoremediation first began its
ascendancy to contaminant cleanup prominence, it was as-
sumed that its application would be limited to plant root
zones, usually considered to be the 15-30 cm depth for most
crop plants. Now, researchers have developed plant systems
that can be used for remediating contamination far beyond
crop root zones and down to water tables in some contami-
nated soils. The most widely demonstrated of these systems
is the use of fast growing, deep rooting hybrid poplar trees
for subsurface remediation of organic contaminants in-
cluding the ubiquitous groundwater-contaminating atra-
zine, and organic solvent contamination at defense industry
facilities (Schnoor, 1997; Thompson, Ramer, and Schnoor,
1998).
Presence of Other Toxicants
Perhaps the most frequently overlooked variable that in-
fluences the success of any biologically based remediation
implementation is the presence of other toxicants in the
contaminated matrix. Often, so much attention is focused
on the primary contaminant that it is easy to overlook other
factors that impede the remediation effort. With the excep-
tion of single event spills of individual types of chemicals,
most contaminated sites contain mixtures of compounds,
organic contaminants sometimes occurring together with
inorganic ones. This requires that an exhaustive site charac-
terization be performed at a site prior to decisions about
remedial strategy. This requirement cannot be overempha-
sized. Inadequate site characterization can lead to flawed
design parameters and consequent failures of remediation
schemes.
Summary
The appeal of phytoremediation as an environmental
cleanup alternative is obvious. The practices rely on poten-
tials of well-known, visible, natural systems that derive en-
ergy from the sun to mediate in cleanup processes in place
(in situ). As straightforward as it appears, phytoremedia-
tion did not begin to attract the level of attention it cur-
rently enjoys until recently. Even with the heightened level
of focus and investigation, additional information is needed
on key issues to allow full exploitation of phytoremediation.
Thus, after an initial focus on the search for plants with im-
,mediate promise for application, research has now appro-
priately begun to focus on understanding mechanisms in-
volved in the abilities of plant species that have thus far been
identified. This change was noted by Beath ( ~ o o o )who
, also
pointed out that regulatory agencies are more likely to ac-
cept a remediation plan if it is based on bench trials or
closely related field trials. We might add that a thorough un-
derstanding of the processes involved is needed, so they may
be enhanced further and/or modified as necessary to suit
specific circumstances.
For metal contaminants, the biggest issues relate to the for-
eignness of hyperaccumulators to contaminated matrices,
and low biomass production. Accordingly, research has fo-
cused primarily on: (1) identification and simulation of cul-
tural conditions in contaminated matrices that allow opti-
mum performance of hyperaccumulators and (2) potentials
for transferring high metal uptake and tolerance character-
istics into high biomass producing plant species. The possi-
bility that metal phytoremediation may be a lucrative un-
dertaking when high value metal contaminants are taken up
by plants, then recovered and recycled, should be a strong
driving force that hastens realization of the potentials of
this process.
Potentials for phytoremediation of organic contaminants
derive from uptake, translocation and metabolism of con-
taminants, andlor their transformations in plant rhizo-
spheres. Uptake and metabolism of xenobiotic compounds
is influenced strongly by the lipophilicity of the compound,
which regulates the extent to which it can move within a
plant. The lipophilicities of many common organic con-
taminants fall within the range that allows some uptake and
metabolism by particular plant species. Indeed, these pro-
cesses form the basis of the more visible organic phyto-
remediation implementations to date. For contaminants
that are highly lipophilic, and not readily translocated in
plants (e.g., PAHs, highly chlorinated PCBs, and dioxins),
prospects for successful implementation of phytoremedia-
tion depend on rhizosphere transformation phenomena,
which involve either direct reactions of contaminants with
plant exudates (e.g., enzymes), or indirect transformations
through enhanced rhizodegradation. Over the last five
years, research has intensified in understanding rhizosphere
processes, so they could be manipulated to enhance con-
taminant removal, destruction, and/or detoxification. Our
own experiences are pointing to potentials for substrate-
based rhizosphere manipulations to enhance PCB dissipa-
tion in soil (Dzantor and Woolston, 2001).
Added to the complexity of plant-contaminant interactions
are strong influences of the environment and specific con-
taminated matrix factors. Environmental factors such as
temperature, and matrix characteristics such as constitu-
tion and organization of reactive surfaces, pH, and redox
status determine to a large degree the susceptibility of a
contaminant to the impacts of plant systems at specific sites.
Understanding these interactions and factors is essential
for allowing decisions to be made about the applicability
of phytoremediation under specific circumstances. In the
second paper, an attempt is made to integrate the technical
information presented here with management consider-
ations of phytoremediation as a cleanup alternative for dif-
ferent contaminants under various site and environmental
conditions.
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Phytoremediation, Part I 87