Environ. Sci. Technol. 2008, 42, 289–293
Degradation of Low Molecular
Weight Volatile Organic Compounds
by Plants Genetically Modified with
Mammalian Cytochrome P450 2E1
C. ANDREW JAMES,† GANG XIN,†
SHARON L. DOTY,‡ AND
S T U A R T E . S T R A N D * ,†
Department of Civil and Environmental Engineering, and
College of Forest Resources, University of Washington, Seattle,
Washington
Received May 21, 2007. Revised manuscript received October
12, 2007. Accepted October 22, 2007.
Cytochrome P450 2E1 (CYP2E1) is a key enzyme in the
mammalian metabolism of several low molecular weight
volatile organic compounds (VOCs), such as trichloroethylene
(TCE), vinyl chloride (VC), carbon tetrachloride (CT), benzene,
chloroform, and bromodichloromethane (BDCM), which are all
common environmental pollutants that pose risks to human
health. We have developed a transgenic tobacco (Nicotiana
tabacum cv. Xanthii) that expresses CYP2E1 with increased
activity toward TCE and ethylene dibromide. In experiments
with tobacco plant cuttings exposed to VOCs in small hydroponic
vessels, the transgenic tobacco had greatly increased rates
of removal of TCE, VC, CT, benzene, toluene, chloroform, and
BDCM, compared to wild-type or vector control tobacco, but not
of perchloroethylene or 1,1,1-trichloroethane.
Introduction
Low molecular weight volatile organic compounds (VOCs)
such as trichloroethylene (TCE), carbon tetrachloride (CT),
benzene, and chloroform are common pollutants in the air,
soil, and groundwater. Exposure can lead to adverse health
effects; all are listed either as known or possible human
carcinogens. Trichloroethylene is a widespread organic
pollutant, having been used for years in industrial and
commercial settings as a cleaning solvent. It is commonly
found at United States Environmental Protection Agency
Superfund sites and is one of the pollutants most frequently
detected in groundwater (1, 2). Carbon tetrachloride was
widely used as a dry cleaning solvent and precursor for the
production of chlorofluorocarbons during the last century.
Although use and production have been phased out through
a series of regulations, CT is still a common groundwater
pollutant (3). Benzene is associated with petroleum contamination and is found in soil and groundwater at numerous
leaking underground storage tank sites. Benzene is a leading
gaseous pollutant of indoor air due to fuel storage in attached
garages and environmental tobacco smoke (4). In addition
to being a frequent contaminant of groundwater, chloroform
is a disinfection byproduct formed during the chlorine
* Corresponding author phone: 206-543-5350; e-mail: sstrand@
u.washington.edu; address: College of Forest Resources, P.O. Box
352100, University of Washington, Seattle, WA 98195.
†
Department of Civil and Environmental Engineering.
‡
College of Forest Resources.
10.1021/es071197z CCC: $40.75
Published on Web 12/04/2007
 2008 American Chemical Society
treatment of drinking water and wastewater. Chloroform can
be volatilized into indoor air during household water use,
especially in showers or other hot water applications. Fiss et
al. (5) found that use of household products containing
triclosan, a common antibacterial agent, could result in the
production of sufficient chloroform to present a significant
exposure risk through the air.
There are many traditional treatment technologies, such
as pump-and-treat and excavation, available to address sites
contaminated with VOCs, but they may be cumbersome,
expensive, and time-consuming to apply. Phytoremediation
is an innovative treatment that uses plants and plant-related
processes (e.g., rhizosphere activity, transpiration) to remediate contaminated sites; it is potentially less intrusive,
cheaper, and more widely accepted. However, there are
limiting factors such as extensive land requirements for
planting and a limited growing season, which may restrict
its employment. To help optimize phytoremediation applications, plants have been genetically modified to increase
metabolism of specific contaminants (6, 7). Transgenic
tobacco plants expressing the nitroreductase nsfI from
Enterobacter cloacae showed a marked improvement in the
ability to tolerate and transform TNT (8). An Arabidopsis
thaliana transformed to express the bacterial gene xplA,
which encodes for a cyclotrimethylenetrinitramine (RDX)degrading cytochrome P450, has been shown to degrade RDX
whereas vector control plants only sequester small amounts
of RDX (9). Transgenic rice plants expressing human cytochrome P450 isoforms 1A1, 2B6, and 2C19 were found to
improve the phytoremediation potential of the herbicides
atrazine and metolachlor in soils (10). Doty et al. (11) have
shown that tobacco transformed to express mammalian
cytochrome P450 2E1 (CYP2E1) rapidly metabolizes TCE and
ethylene dibromide. These plants are the subject of this study.
Cytochrome P450 2E1 is an enzyme that is significant in
the degradation of xenobiotics in mammalian systems,
including TCE, CT, 1,1,1-trichloroethane (TCA), chloroform,
and benzene (12). The goal of this work was to evaluate the
activity of transgenic tobacco against various organic pollutants. Sterile apical cuttings from either modified or
unmodified tobacco plants were placed in sealed vials with
liquid growth media and dosed with VOCs. The headspace
concentration was measured over time and the normalized
loss rates were calculated and compared.
Materials and Methods
Plant Material. Transgenic, vector control, and wild type
tobacco plants (Nicotiana tabacum cv. Xanthii) were used
in this experiment. Plant transformations were as described
in Doty (11). Briefly, plasmid pSLD3 containing cDNA for
human CYP2E1 under control of the Mac promoter was
introduced into tobacco leaf discs via Agrobacterium mediated transformations. Transformations were verified by
polymerase chain reaction and the plants regenerated. The
CYP2E1 expression and TCE transformation capability of
several lines were evaluated and the best-performing line
was self-crossed and progeny, designated 3–1–2, were used
for further study (11). Vector control plants were transformed
with plasmid pCGN1578, which did not contain cDNA for
CYP2E1. Wild type plants were not transformed.
Sterile plant material was obtained by propagating apical
cuttings from whole plants in sterile vessels with amended
growth media consisting of Murashige and Skoog (MS) +
vitamins (Caissons MSP002), 30 g L-1 sucrose, 1 g L-1 phytogot
gellan gum, 3.5 g L-1 phytagar, 1 mL L-1 Fungigone (Bioworld,
Dublin OH), and 1 mM indole-3-butyric acid. Apical cuttings
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TABLE 1. Initial Mass Dosing (µg) and Equilibrium Liquid
Concentration (µg/mL) of the Compounds Tested in This
Study
compound
perchloroethylene
trichloroethylene
vinyl chloride
chloroform
carbon tetrachloride
bromodichloromethane
1,1,1 - trichloroethane
toluene
benzene
initial mass
(µg)
equilibrium liquid
concentration
(µg/mL)
54
125
1000
0.25
10
0.6
16
15
85
1.64
5.6
22
0.0025
0.2
0.05
0.5
0.9
1
were placed in water in 50 mL plastic centrifuge tubes
(Sarstedt, Newton, NC) for 24 h prior to sterilization.
Sterilization was performed by submersing the cuttings for
10 min in 10% bleach solution (final concentration 0.35%
NaClO), rinsing with sterile, deionized water, 5 min in 1%
Iodophor solution, rinsing three times with sterile, deionized
water, and transferring into a sterile growth vessel. All work
was performed in a sterile, laminar-flow hood. Plants grew
in 6-8 weeks and served as sterile source material for the
vial experiments. Cuttings for the vial experiments were
obtained from the apical ends of the sterile plants. Each apical
cutting had 3-5 leaves and wet mass from 1.5 to 2 g.
Experimental Setup. Sterile plant cuttings were placed
in clear glass volatile organic analysis (VOA) vials, 40 mL
nominal volume, in 10 mL of half-strength MS basal salt
mixture with 30 g L-1 sucrose (pH 5.7). Vials were capped
with 24 mm Mininert valves with silicone septa (VICI Valco
Instruments, Houston, TX) and held for 24 h prior to chemical
exposure. Cuttings were incubated at approximately 23 °C
under fluorescent lights with a 16-h photoperiod.
Several chemicals were investigated in this study including
perchloroethylene (PCE), TCE, vinyl chloride (VC), CT, TCA,
chloroform, bromodichloromethane (BDCM), benzene, and
toluene. For each experiment, a set of at least three transgenic
and three vector control plant cuttings was set up, with one
cutting per vial, and injected with known amounts of chemical
using gastight glass syringes (Hamilton Co., Reno, NV) either
in the form of a stock solution in water, or as a gas (Table
1). Chemical mass from the stock solutions was calculated
based on volume, solubility in water, and temperature. Mass
from gas injections was calculated based on volume, temperature, and pressure.
Sampling and Analysis. Initial sampling occurred at least
two hours following the introduction of chemicals into the
VOA vials to allow air–liquid equilibrium. Subsequent
sampling frequency was either 24 or 48 h, according to the
uptake rate of the chemical of interest. Samples were obtained
by withdrawing a known volume of vial headspace with a
gastight glass syringe and injecting manually into a gas
chromatograph (GC) for analysis. Headspace samples from
vials containing PCE, TCE, CT, TCA, and chloroform were
analyzed with a GC-electron capture detector (ECD). Two
GC-ECDs were used during the course of the experiments:
Perkin-Elmer AutoSystem XL GC-ECD with a Supelco PTE-5
column (30 m, 0.32 mm i.d., 0.32 µm film thickness); and,
SRI 8610C with a Supelco SPB-624 column (60 m, 0.53 mm
i.d., 3.0 µm film thickness). Headspace of vials containing
VC, benzene, and toluene was analyzed with a SRI 8610C
GC-flame ionization detector (FID) with a Supelco Alumina
Sulfate Plot column (50 m, 0.53 mm i.d.). The GC oven
temperatures were isothermal for all experiments. Sample
injections were performed in triplicate.
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FIGURE 1. Degradation of chloroethenes TCE (A) and VC (B) by
CYP2E1-expressing and vector control or wild type tobacco
plant cuttings over time. Chemical dosing occurred at time
zero. Sample collection began 2–12 h after initial dosing to
allow air–liquid equilibrium. Points are the average mass of
individual vial tests (n ) 4 TCE; n ) 3 VC); error bars indicate
( 1 standard deviation.
Analysis for trichloroethanol (TCOH) was performed in
the TCA degradation experiments. Plants were removed from
vials, flash frozen in liquid nitrogen, and ground in a mortar
and pestle. Approximately 1.5 g of frozen tissue was placed
in a chilled centrifuge tube with 2 mL of 1 N H2SO4/10% NaCl
and shaken vigorously for 1 min. Methyl tert-butyl ether
(MTBE; 10 mL) was added and the mixture was shaken for
1 min, followed by centrifugation at 8000 rpm for 10 min.
The supernatant (7 mL) was transferred to a septa-capped,
amber glass vial containing 2 g of Na2SO4 and stored for 1 h.
An aliquot was transferred to an autosampler vial for analysis
on a GC-ECD. The GC oven temperature program was 40
°C for 1 min, ramped at 10 °C minute-1 for 19 min, and held
at 230 °C for 4 min.
Analysis for BDCM was performed by solvent extraction
due to difficulties in optimizing the peak response with
manual injection in the SRI GC-ECD. Initially, cuttings were
placed in 15 mL of liquid media. Following chemical dosing
and equilibration, 5 mL of media was extracted through the
septa with a gastight syringe and mixed with 5 mL of 1 N
H2SO4/10% NaCl in a 40 mL amber glass vial and shaken
vigorously for 1 min. Ten mL of MTBE was added, the mixture
was shaken for 1 min, and allowed to stand for 10 min. Seven
mL of MTBE was transferred, held with Na2SO4, and analyzed
by GC-ECD as described above for TCOH.
Analysis of the uptake kinetics was performed by a
regression analysis of the natural-log transformed concentration data over time. The significance of the regression was
verified through analysis of variance testing for each regression at a significance level of 0.05. First-order chemical loss
FIGURE 2. Degradation of haloalkanes by CYP2E1-expressing and vector control or wild type tobacco plant cuttings over time. Data
for chloroform (A), BDCM (B), CT (C), and TCA (D) are shown. Chemical dosing occurred at time zero. Sample collection began 2-12
h after initial dosing to allow air–liquid equilibrium. Points are the average mass of individual vial tests (n ) 3 BDCM; n ) 4
chloroform, CT, and TCA); error bars indicate ( 1 standard deviation.
rates were normalized for plant mass and compared using
Student’s t statistic at a significance level of 0.05.
Results
Chloroethenes. Tobacco plant cuttings genetically modified
with CYP2E1 displayed significant degradation of TCE, while
the vector control plant cuttings did not display activity
significantly different from that of the no-plant controls
(Figure 1A). Similarly, tobacco plant cuttings expressing
CYP2E1 degraded VC, while the wild type did not demonstrate
statistically significant degradation (Figure 1B). There was
no removal of PCE by any of the plants tested (data not
shown). Analysis of the log-transformed data indicated that
transformation kinetics were first-order for TCE (r 2 ) 0.93,
P < 0.05) and VC (r 2 ) 0.99, P < 0.05).
Haloalkanes. Chloroform (Figure 2A) and BDCM (Figure
2B) were degraded in vials containing the CYP2E1-transformed plant cuttings, while there was no significant removal
in vials with either the wild type or vector control plant
cuttings. The rate of removal of CT (Figure 2C) by plant
cuttings expressing CYP2E1 was significantly greater than
that of either the no-plant or vector controls assuming firstorder kinetics (P < 0.05). The normalized degradation rate
of CT was 3.3 times greater for the plant cuttings expressing
CYP2E1 compared to the vector controls. Analysis of the logtransformed data indicated that chloroform (r 2 ) 0.88, P <
0.05) and CT (r 2 ) 0.98, P < 0.05) degradation followed firstorder kinetics. The experimental method used to measure
BDCM precluded analysis of uptake kinetics.
Neither plant cuttings expressing CYP2E1 nor vector
control cuttings significantly degraded TCA in any of the
experimental runs (Figure 2D). To determine whether any
TCA was degraded to TCOH, free TCOH was measured in
plant tissues following exposure of CYP2E1-transformed plant
cuttings to TCA or TCE for 7 days. TCE transformation was
used as a positive control. Plant cuttings expressing CYP2E1
exposed to TCE had an average TCOH concentration of 0.226
µg per g wet plant while the TCA-exposed plants had no
detectable levels of TCOH.
Aromatic Hydrocarbons. Benzene and toluene were
almost completely removed within 4 days from vials containing CYP2E1-transformed plants (Figure 3A and B). The
control plant cuttings did not show any activity toward
benzene. Toluene was degraded by the vector control plant
cuttings, though at a significantly lower rate than the CYP2E1transformed plant cuttings (P < 0.05). The first-order removal
rate was 10.4 times higher for the CYP2E1-transformed plant
cuttings compared to the vector control plant cuttings.
Analysis of the log-transformed data indicated that benzene
(r 2 ) 0.97, P < 0.05) and toluene (r 2 ) 0.98, P < 0.05)
degradation followed first-order kinetics.
Discussion
These results demonstrate the increased degradation of a
wide variety of VOCs by genetically modified plants that
express mammalian CYP2E1. For most of the chemicals
investigated, the transgenic plant cuttings displayed either
increased activity, or were able to degrade pollutants that
were otherwise recalcitrant to the wild type or vector control
tobacco plant cuttings. The greater activity conferred by
CYP2E1 expression has the potential to improve the effectiveness of phytoremediation in the cleanup of soil,
groundwater, and indoor air.
The enhanced metabolism of TCE by plants expressing
CYP2E1 has been previously reported (11). The replication
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FIGURE 3. Degradation of aromatic hydrocarbons toluene (A)
and benzene (B) by CYP2E1-expressing and vector control
tobacco plant cuttings over time. Chemical dosing occurred at
time zero. Sample collection began 2 h after initial dosing to
allow air–liquid equilibrium. Points are the average mass of
individual vial tests (n ) 4); error bars indicate ( 1 standard
deviation.
of these results herein suggests that utilizing plant cuttings
is an appropriate method for comparing metabolic activity.
Wolfe and Hoehamer (13) reported the degradation of TCE
and CT by cell-free extracts of Canadian Waterweed, suggesting that certain plants express native enzymes capable
of degrading these compounds. Here, we demonstrated a
marked increase in the metabolism of both TCE and CT by
transgenic plant cuttings indicating the potential for accelerated remediation. To our knowledge, no other reports
have shown the metabolism of VC by plants. The ability of
these transgenic plants to degrade both TCE and VC may be
valuable in areas of mixed contamination.
1,1,1-Trichoroethane was not significantly degraded by
the transgenic tobacco plants despite the fact that it is a
known substrate for mammalian CYP2E1 (12). To confirm
that TCA was not metabolized by transformed plants, we
looked for the production of TCOH in CYP2E1-transformed
plants exposed to TCA. Trichloroethanol has been shown to
be a metabolite of CYP2E1 in mammalian tissues and hepatic
microsomes exposed to TCA (12). However, no TCOH was
detected, which was surprising considering the wide range
of activity displayed by CYP2E1 in this plant system.
Cytochrome P450 enzymes function with the accessory
proteins NADPH-P450 reductase (NPR) and Cytochrome b5
(b5). Several of the P450 enzyme isoforms, including 2E1,
require b5 to carry out their full range of activities, though
the mechanism appears to differ depending on the P450 (14).
While other P450s can be stimulated by either holo-b5 or
apo-b5, or even through protein–protein interactions with
other P450s, CYP2E1 may only be enhanced by holo-b5,
suggesting a more stringent requirement for the enhance292
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ment interactions (15). The pSLD3 plasmid used to transform
the tobacco contained only genes for human CYP2E1, but
not NPR or b5. The results of this work indicate that the
CYP2E1 still catalyzes a wide range of activity against
xenobiotics, likely utilizing native plant homologues to NPR
and b5 to facilitate electron transport. However, differences
between the homologous versions found in plants compared
to those in humans possibly causes conformational changes
that inhibit catalytic activity toward TCA.
Benzene and toluene can be taken up by plants and
released to the atmosphere with limited transformation (16).
Toluene volatilization through leaves can be reduced by
inoculating plants with endophytes expressing the toluenedegrading pTOL plasmid, thereby increasing in planta
degradation (17). Similarly, the improved degradation of
benzene and toluene by CYP2E1-transformed plants shown
here could also reduce transpiration and increase phytoremediation effectiveness.
The trihalomethanes (THMs) chloroform and BDCM were
degraded by the transgenic plant cuttings. Trihalomethanes,
which may be present as disinfection byproduct in chlorinated drinking water, can volatilize into indoor air. In
preliminary work, we found a 9-fold increase in average daily
chloroform concentration in the air with shower use (data
not shown; BDCM was not measured). Studies have looked
at the potential of wild type household plants for the
remediation of contaminants such as formaldehyde, benzene,
and TCE, from indoor air (18, 19). Assuming that plant
degradation was limited by the endogenous enzymatic
activity, transgenic plants similar to those described in this
paper may have application in the remediation of indoor air.
Overall, our findings suggest potential applications for
genetically modified plants in the field. The CYP2E1transformed tobacco plants have demonstrated activity
against broad classes of environmental pollutants such as
chlorinated solvents (both alkenes and alkanes) and aromatic
hydrocarbons suggesting that CYP2E1-transformed plants
could be used to remove pollutants faster in environments
contaminated by single or mixed contaminants, particularly
when cleanup is limited by planting area or time. It is
important, however, to acknowledge the limitations of this
study, which was designed specifically to investigate differences in plant metabolism. Field applications are complex;
plant metabolism alone may not be the determining measure
of success. Further, field applications may require plants
with higher biomass production and deeper root systems
than the tobacco to effectively reach contaminated areas.
The spread of transgenic material may be a concern,
particularly with plants with an annual reproductive cycle,
such as the tobacco. Transgenic trees that express CYP2E1
could combine the higher metabolic activity with deeper
root systems, while having a more controlled reproductive
cycle. This is potentially quite desirable. This study and others,
which have reported on various applications of genetically
modified plants for detoxification of polluted environments
(9, 10), demonstrate the potential of transgenic modifications
to increase the range and utility of phytoremediation.
Acknowledgments
This work was funded by NIEHS grant 2P42-ES004696-19,
DOE grant DE-FG02-03ER63663, and the Valle Fellowship
and Exchange Program at the University of Washington. C.A.J.
and G.X. should be considered co-first authors on this
manuscript.
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