Acta Biotechnologica - 2002 - SCH Ffner - Genes and Enzymes For in Planta Phytoremediation of Air Water and Soil

Acta Biotechnol.
22 (2002) 1--2, 141--152
Short Review
Genes and Enzymes for In-Planta

Phytoremediation of Air, Water and Soil
SCHÄFFNER*, A., MESSNER, B., LANGEBARTELS, C., SANDERMANN, H.
GSF – Forschungszentrum für Umwelt und Gesundheit * Corresponding author

Institut für Biochemische Pflanzenpathologie Phone: + 49 89 3187 2930
85764 Neuherberg, Germany Fax: + 49 89 3187 2726
E-mail: schaeffner@gsf.de
Summary
Plants harbour highly versatile enzymatic machineries to attack and detoxify pollutants. Similarities
to the mammalian detoxification led to the coining of the term “green liver” for plant xenobiotic
metabolism. Important enzyme classes such as cytochrome P450 monoxygenases, glutathione
S-transferases, glycosyltransferases and transporters are involved in both kingdoms. The availability
of the first whole plant genome sequence of Arabidopsis thaliana revealed an unforeseen complexity
of these enzyme classes. Genetic and biochemical diversity, by far exceeding at least single
microorganisms, seems to exist in plants. In agreement with previous investigations at the enzymatic
level both terrestrial and aquatic plants possess an enormous potential for phytoremediation of soil,
water and air if limitations due to insufficient uptake into plants can be overcome. This is exemplified
by the detoxification of herbicides, halogenated phenols and anilines, and formaldehyde by the action
of plant enzymes. Two examples are discussed at the biochemical and genetic level. Plants can
detoxify airborne formaldehyde by a glutathione-dependent formaldehyde dehydrogenase. Recombi-
nant expression of an Arabidopsis UDP-glucose dependent glucosyltransferase showed activity
towards both endogenous and xenobiotic substrates by a single enzyme. Plants frequently do not
completely degrade xenobiotics, but rather form conjugated metabolites and “bound” residues.
However, these potential contaminants can be easily removed by harvesting. In order to exploit this
enormous potential of plants, promising approaches extending their endogenous capacity have been
initiated. Transgenic organisms that express heterologous enzymes in order to specifically degrade
compounds or to increase the mobility and uptake of recalcitrant xenobiotics are being pursued to
make phytoremediation procedures useful in practice.
Introduction
Phytoremediation of air, water and soil is based on many different strategies. Pollutants
are usually divided into three major classes, heavy metals (e.g. Cd2+, Ni2+, Hg2+), small
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142 Acta Biotechnol. 22 (2002) 1--2
volatile molecules (e.g. O3, CO, HCHO) and numerous organic chemicals. Whilst there
are several promising strategies to remediate metal contaminants, widespread views
argue that organic xenobiotics cannot be efficiently removed or detoxified. In addition,
rhizosphere microorganisms are thought to be mostly responsible for the removal and
degradation of organics. However, biochemical studies and recent genome projects
have revealed an enormous diversity of plant enzymes that may be capable of attacking
and detoxifying organic chemicals. This capacity may exceed the possibilities present
in microorganisms. This fact is also illustrated by the finding that plants are able to
colonize heavily contaminated soils that are almost sterile with regard to microbes [1].
Although limited uptake may be in part responsible for that capability of plants,
microbes, on the other hand, may be limited in their capacity of detoxification by a
restricted supply with e.g. conjugating, detoxifying enzyme activities.
Nevertheless, there are several constraints and bottlenecks to the use of plants. In par-
ticular, the strong adsorption of hydrophobic contaminants to soil and plant surfaces
may limit the overall metabolic rates and efficacy of detoxification; in particular recal-
citrant chemicals such as PAHs or PCBs are affected. Furthermore, environmental
mobility and potential uptake into plants is dependent on factors such as soil or water
composition, pH and temperature. Whereas a compound with log kOW values larger
than 3 may be rather immobile in humic soil it may partition efficiently to roots in
hydroponic, aqueous systems. On the other hand, plants may lack active uptake sys-
tems for hydrophilic substances that rapidly permeate through soil. Uptake may
strongly depend on the plant species and the related further metabolism in that plant.
Interestingly, there are a few reports on the uptake of PAHs through stomata or the
hydrophobic phase of the leaf cuticle or on the mobilization and uptake of hydrophobic
and recalcitrant chemicals such as PCB/PCFs or trinitrotoluene (TNT). Their degrada-
tion or uptake is mediated by a probably proteinaceous agent likely secreted by
Cucurbitaceae roots or by transgenic expression of enzymes ([2–5]; see also below). In
addition, the plant transpiration stream may assist in the translocation of hydrophobic
compounds like pyrene from the soil towards the roots [6]. Root exudates may also
contain enzymatic activities such as oxidoreductases that are able to alter the chemical
structure, reactivity or mobility of organic compounds in soil [7]. Active research
programmes are engaged in identifying new plants, agents and mechanisms for mobi-
lization and uptake [8, 9].
In this paper, however, the focus will be on phytoremediation in planta, this means the
genetic diversity and versatility of detoxifying plant enzymes that endow plants with a
high potential for decontamination of air, water and soil. A few selected examples will
be discussed.
Enzymes and Phases of Detoxification
Biological detoxification of exogenous organic chemicals is based on a machinery of

metabolic enzymes in living cells. Besides a plethora of toxins produced by other
organisms, anthropogenically released compounds may constitute a major concern and
threat to living beings and to ecosystems. Detoxification has often been shown to
involve the subsequent action of enzymes leading to a classification into three phases
SCHÄFFNER, A. et al., Genes and Enzymes for Phytoremediation of Air, Water and Soil 143
[10, 11]. First, conversion or transformation may alter the chemical structure by oxida-
tions catalyzed by cytochrome P450 monooxygenases, reduction (e.g. dehydrogenases)
or hydrolysis (e.g. esterases). This is followed by conjugation to glutathione or sugars
due to the action of glutathione-S-transferases or glycosyltransferases leading to
conjugated and frequently less toxic metabolites. Finally, phase III is characterized by
compartmentation of these compounds involving ATP- or proton-dependent trans-
porters or exocytosis (Tab. 1). In mammals, the liver is the major site of detoxification.
After the discovery of similar enzymes and metabolic products in plants, the term
“green liver” was coined to illustrate that plants had similar metabolite classes,
enzymes and genes as those found in animal livers [10].
Tab. 1. Phases of detoxification in plants

___________________________________________________________________________________________________________________________________________________________________
Phase I Transformation Oxidation, reduction Cytochrome P450 mono-

or hydrolysis oxygenases, esterases,
reductases, dehalogenases
___________________________________________________________________________________________________________________________________________________________________
Phase II Conjugation with carbohydrates, Glycosyltransferases,

glutathione, glutathione-S-transferases,
carboxylic acids acyltransferases
___________________________________________________________________________________________________________________________________________________________________
Phase III Compartmen- into vacuole Exocytosis, ATP binding

tation or apoplast cassette (ABC) and multidrug
and toxic compound
extrusion (MATE) transporters
___________________________________________________________________________________________________________________________________________________________________
At the levels of enzymes, all important metabolic enzyme classes of the liver have also
been demonstrated in plants. In detail, however, the chemical reactions may differ, e.g.
mammalian livers usually attach a charged moiety, glucuronic acid to reactive
hydroxyl groups during phase II, whereas the major reaction in plants involves
glucosylation and a possible subsequent acylation, e.g. by malonyl transferases, that
introduce a charged residue. Furthermore, plants are usually not able to eliminate the
detoxified metabolites. Instead, they are found associated with polymeric molecules or
stored in the vacuole where further metabolism may occur.
Plants and plant cells have been shown to metabolize numerous pollutants ranging
from highly polar chemicals such as glyphosate to highly non-polar chemicals such as
DDT and di-(2-ethylhexyl)-phthalate [12–15]. Thus, at the metabolite level, a large
versatility of plants to detoxify has been already demonstrated [1, 10, 11].
Enzymes for Phytoremediation of Volatile Pollutants

The accumulation of volatile toxic substances in the air of poorly ventilated office
rooms and energy-efficient homes has been recognized for many years as a potential
indoor health hazard. In particular, the suspected carcinogen formaldehyde is currently
a common air pollutant with usually higher indoor than outdoor concentrations. Studies
by NASA scientists have provided evidence that common indoor plants can assimilate
formaldehyde [16]. Adsorption to plant surfaces and microbial processes were in large
part responsible for the observed “assimilation” [17, 18].
Studies with radiolabelled formaldehyde have demonstrated that intact indoor plants
catalyze the conversion of formaldehyde to sugars, amino acids, cell wall components
and other natural compounds [19]. Chlorophytum leaves contained a glutathione-
dependent formaldehyde dehydrogenase (FDH; EC 1.2.1.1), the key enzyme of
formaldehyde detoxification. Similar results were recently obtained for various com-
mon indoor plants, including Ficus benjamina, Schefflera arboricola and Spathiphyl-
lum wallisii [17]. FDH cDNA, as well as the purified protein, has since been isolated
from Arabidopsis thaliana [20] and maize [21, 22]. It was shown that the plant FDH
sequences were highly homologous to those of microbial and animal FDHs, with FDH
being a progenitor of the large alcohol dehydrogenase gene family [21].
Recent studies in our laboratory with continuously exposed intact plants revealed that
F. benjamina and S. arboricola have led to a pronounced formaldehyde reduction, but
no complete elimination of formaldehyde under typical indoor conditions was detected
(G. THOMAS, C. LANGEBARTELS, unpubl. results). These effects persisted over several
months in plants exposed to daily re-current formaldehyde treatments, and were well
correlated with stomatal uptake. It can be concluded that optimized plant systems
including sufficient light supply and root ventilation may provide long-term reduction
of volatile pollutants in indoor air.
Enzymes for Phytoremediation of Water and Soil
The potential of plants to decontaminate soil and water is best illustrated by the appli-
cation of pesticides in agriculture. In most cases, the specific action of pesticides to kill
weeds or pathogens but leave the crop plant undamaged is due to the selective metabo-
lism of the pesticide by the crop plant. The finding that plants are able to colonize
heavily contaminated, almost sterile soils, may point to a more effective exclusion of
contaminants by plants than by microorganisms and/or to a more versatile plant
detoxification.
The most important and most widely studied detoxifying plant enzymes include cyto-
chrome P450 monooxygenases, glutathione-S-transferases, glucosyl-O-transferases
and acyltransferases. Toxic compounds released intentionally or accidentally in the
environment that are decontaminated by the action of these enzymes include penta-
chlorophenol, PAHs such as pyrene or benzo[a]pyren, trinitrotoluene, various indus-
trial chemicals and many plant protection agents [23–26]. Transporters driven by ATP
or by proton gradients are probably involved in compartmentation [27, 28].
Based on knowledge concerning the metabolic fate of xenobiotics more than two dec-
ades ago, many research groups began to identify the responsible enzymes via purify-
ing enzymatic activities from various sources, mainly wheat and soybean cell culture
cells. Here, the focus will be on conjugating UDP-glucose-dependent glucosyl-
transferases because they represent an interesting class that has very divergent tasks in
plants. A huge variety of endogenous secondary metabolites as well as plant signalling
molecules exist as glucosides to regulate their endogenous toxicity, activity and/or
compartmentation. It is presumed that this endogenous variability of glucosyl transfer
forms the basis of their potential for glucosylating and thereby detoxifying many
chemically different, exogenous compounds. In contrast, glutathione-S-transferases in
their role as true transferases may represent a class of enzymes that is mainly involved
in detoxification per se, at least with respect to oxidative damages to the cells.
Several glucosyltransferase activities have been studied that are active towards phenols
and anilines, DDT or herbicide metabolites, for example. A pentachlorophenol conju-
gating O-glucosyltransferase was identified in both soybean and wheat cell cultures.
The purified soybean isoenzyme exhibited only little activity when tested with a few
potential endogenous phenolic substrates [29, 30]. N-glucosyltransferase activities
conjugating the amino group of 3,4-dichloroaniline were found in both cell cultures as
well [31, 32]. In addition, O-glucosyltransferases active towards the hydroxy or
carboxy groups of the metabolites derived from the herbicide bentazone or the
insecticide DDT, respectively, could be purified [14, 31, 3]. Although the majority of
these glucosyltransferases are soluble in the cytosol, a membrane-bound activity has
also been identified [33].
It is important to note that these activities are not cryptic and not only detectable when
testing isolated enzymes. Studies with plant cell suspension cultures, i.e. an experi-
mental system to minimize any uptake barriers, have shown that the in-vivo
metabolism of chloroanilines, pentachlorophenol and di-(2-ethylhexyl)-phthalate cor-
responded to the rates predicted from the enzyme levels present in the plant cells.
However, from these studies – based on current knowledge – it is not clear whether
these activities originate from single and substrate-specific enzymes responsible for the
glucosylation of the respective xenobiotic compound, whether a mixture of very simi-
lar enzymes had been purified, or whether the correct “main”' substrates had been
tested at all. Cloning of individual genes and finally whole genome analyses are at
present time major steps providing the opportunity to study and answer these
questions.
The first genes for these metabolic reactions were discovered when asking specific
questions of plant secondary metabolism. With respect to UDP-glucose-dependent glu-
cosyltransferases, a number of genes have been identified so far following the initial
cloning of a flavonol-3-O-glucosyltransferase from the bronze locus of maize [34–36].
Similarly, genes encoding other classes of detoxifying enzymes have been cloned. In
addition to these studies, information on related enzymes from other organisms accu-
mulated allowed amino acid motifs as signature sequences to be identified by
comparison in order to classify certain classes of enzymes. For these gluco-
syltransferases acting on plant secondary products, an amino acid signature motif
WAPQXXXXXHXXXXXFVTHCGWNSXXEXXXXGVPMXXXPFFGDQ (single letter
amino acid code) has been established [36]. With the advent of the Arabidopsis
thaliana genome sequence [37] as the first complete genome of a plant, it was feasible
by simply searching the whole sequence database to compile all putative UDP-
glucose-dependent secondary product glucosyltransferases. Although it had been
suspected that there would be numerous genes, it was surprising to discover an
enormous genetic diversity. A total of 119 related sequences were collected ([38];
www.biobase.dk/P450/UGT.shtml; O. THULKE and A. SCHÄFFNER, unpublished results).
More than 270 Arabidopsis thaliana members of cytochrome P450 mono-
oxygenases suggest an even more complex genetic background ([39];
www.biobase.dk/P450/p450.shtml). Similarly, glutathione-S-transferases or ATP-de-
pendent ABC-transporters constitute an enormous additional complexity ([40, 41];

www.arabidopsisabc.net/). Thus, very high genetic and encoded biochemical diversity
exists in plants.
The availability of all Arabidopsis thaliana coding sequences now offers the opportu-
nity to investigate any individual enzymes void of a contamination with other isoen-
zymes by recombinant expression of the genes in Escherichia coli or yeast. With
respect to their activity towards xenobiotics, potential substrates can be tested and
compared in vitro. In addition, the easy genetic transformation of the model plant
Arabidopsis and huge mutant collections facilitate the subsequent analysis in planta.
As an example, the activities towards various xenobiotics were tested for glucosyl-
transferase UGT75D1 from Arabidopsis expressed in yeast. UGT75D1 is closely
homologous to maize and Arabidopsis indole-3-acetic acid glucosyltransferases [42,
43]. Indeed, glucosylation of indole-3-acetic but also other potential endogenous sub-
strates could be observed. Such a broad substrate specificity has been also demon-
strated for other recombinant plant glucosyltransferases [36]. Surprisingly, however,
the same enzyme was catalyzing the conjugation of various xenobiotics in a similar or
even better manner than the natural compounds (Fig. 1). The most active substrate was
2,4,5-trichlorophenol but also various other moieties, including sulphhydryl groups,
were accepted. Importantly, the metabolizing pattern of an individual enzyme like
UGT75D1 is different from the activities of a glucosyltransferase preparation from
A. thaliana leaves towards the same xenobiotics. This leads to the conclusion that the
plant cells contain a complex mixture of different overlapping isoenzymes with various
substrate specificities (B. MESSNER, A. SCHÄFFNER, unpublished results).
According to ongoing genome projects, this genetic diversity is probably reiterated in
other plant species as well. Thus, extrapolating to a diversity of more than
100 members in Arabidopsis and an even higher diversity including other plant
species, may be an enormous potential for conjugating and detoxifying “any” xeno-
biotic substrates that at least exceeds the capabilities of individual microorganisms.
However, the actual biochemical activity needed to detoxify or degrade a specific
compound may not be present in any plant. Therefore, targeted classical searches for
plant species and enzymes will remain a powerful approach, in particular, if it will be
combined with genetic engineering (see below). Regarding aquatic plants and their
potential for aquatic phytoremediation a survey at the enzymatic level of glucosyltrans-
ferases, glutathione-S-transferase and cytochrome P450 monoxygenase was performed
on a large subset of plant species including several algae and mosses [44–46].
Although such a survey using standardized, non-optimized extraction procedures
would not discover all enzymatic activities harboured in that species and therefore
would underestimate the activities present in toto, these studies emphasize the enor-
mous potential of the enzymatic machinery provided by algae and plants in general.
With respect to the glucosyltransferases, a wide range of activities towards different
chemical groups was found by testing pentachlorophenol, different trichlorophenols,
2,2-(bis)-4-chlorophenyl-acetic acid, 3-chloroaniline, 3,4-dichloroaniline or 4-chloro-
thiophenol as potential xenobiotic substrates, and indole-3-acetic acid as a potential
endogenous substrate [44].
Fig. 1. Glucosyltransferase activities of UGT75D1 from Arabidopsis expressed in

yeast
A diverse spectrum of endogenous and xenobiotic substrates was tested: 1) salicylic
acid, 2) ferulic acid, 3) indole-3-acetic acid, 4) coniferyl alcohol, 5) phenyl acetothio-
hydroxamate, 6) 2,4,5-trichlorophenol, 7) pentachlorophenol, 8) 3,5-dibromo-4-hydro-
xy-benzoic acid, 9) 3,4-dichloroaniline, 10) 4-nitrophenol, 11) 4-chlorothiophenol.
The O-, N- and S-glucosyltransferase activities were assayed according to [30].
Long-Term Fate of Pollutants
With the exception of a few specialized cells and root exudation, plants are not able to
excrete catabolites of xenobiotics on a large scale and, in addition, xenobiotics are
often not completely degraded into basic chemical moieties fed into primary
metabolism. Instead, in many cases the detoxified xenobiotic metabolites are
incorporated into the plant-bound residue fraction. Differences in the chemical nature
and the plant species association with cellular polymers such as hemicellulose, pectin,
lignin and protein have been found [47, 48]. Thus, with respect to the long-term fate of
such bound residues, detoxification and complete removal may not be finished after
growing remediating plants. Nevertheless, harvesting offers an easy and cost effective
way to remove potentially contaminated material from a polluted site. Besides safe
deposition or incineration of that material, additional biological treatments may offer
alternatives. Almost two decades ago, several groups tested the ability of the lignin-
degrading fungus, Phanerochaete chrysosporium and other related white-rot fungi to
degrade persistent organic chemicals in addition to the complex lignin polymer that is
a natural substrate for the fungus. Indeed, an enormous metabolic potential of this and
related fungi to completely mineralize many persistent and toxic compounds was
discovered [49, 50].
Perspectives
In conclusion, biochemical studies and genome projects have revealed versatile

enzymatic machineries of plants to attack and detoxify xenobiotics. En lieu of the
enormous biomass of terrestrial and aquatic plants, these organisms considerably
contribute to detoxification of pollutants. Importantly, the intrinsic degradative and
detoxifying capabilities of plants may be substantially increased through genetic
engineering. As soon as there is knowledge of critical rate-limiting steps in a degrada-
tion pathway, or of the properties of a specific enzyme targeted towards an organic
pollutant from any organism, transgenic expression of that trait across species may be
tested. Of course, safety regulations have to be obeyed and carefully checked
depending on the plant species and/or trait to be transferred. Indeed, there are some
recent examples that successfully highlight these strategies. The expression of a human
cytochrome P450 enzyme in tobacco increased the metabolism of trichloroethylene by
two orders of magnitude [51]. HANNINK et al. (2001) [52] could achieve a spectacular
success by expressing a bacterial nitroreductase in tobacco that reduces trinitrotoluene
in a NAD(P)H-dependent manner. The transgenic plant grew on highly concentrated
trinitrotoluene. Interestingly, they did not accumulate the toxic reaction product amino-
dinitrotoluene suggesting that further degradation is mediated by an effective endoge-
nous detoxification machinery. In addition to the potential for detoxification in planta
discussed in this contribution, new strategies for phytoremediation ex planta are being
pursued by several laboratories. Genetic fusions of degradative enzymes such as
dehalogenases with signalling peptides allow their secretion to the apoplast and root
environment where they may attack recalcitrant compounds. Similarly, proteinaceous
compounds with the ability to complex and solubilize immobile organic molecules
might enhance their bioavailability and uptake [53, 54]. Thus, phytoremediation proce-
dures may be significantly improved for more efficient practical applications.
Acknowledgement
The authors would like to thank two anonymous reviewers for their helpful suggestions.
Received 15 June 2001

Received in revised from 4 March 2002
Accepted 6 March 2002
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Acta Biotechnol.

22 (2002) 1--2, 141--152

Genes and Enzymes for In-Planta

SCHÄFFNER*, A., MESSNER, B., LANGEBARTELS, C., SANDERMANN, H.

GSF – Forschungszentrum für Umwelt und Gesundheit * Corresponding author

© WILEY-VCH Verlag Berlin GmbH, 13086 Berlin, 2002 0138-4988/02/01-205-0141 $ 17.50+.50/0

Enzymes and Phases of Detoxification

Biological detoxification of exogenous organic chemicals is based on a machinery of

Tab. 1. Phases of detoxification in plants

Phase I Transformation Oxidation, reduction Cytochrome P450 mono-

Phase II Conjugation with carbohydrates, Glycosyltransferases,

Phase III Compartmen- into vacuole Exocytosis, ATP binding

Enzymes for Phytoremediation of Volatile Pollutants

Enzymes for Phytoremediation of Water and Soil

pendent ABC-transporters constitute an enormous additional complexity ([40, 41];

Fig. 1. Glucosyltransferase activities of UGT75D1 from Arabidopsis expressed in

Long-Term Fate of Pollutants

In conclusion, biochemical studies and genome projects have revealed versatile

Received 15 June 2001

[21] FLIEGMANN, J., SANDERMANN, H.: Maize glutathione-dependent formaldehyde dehydrogenase

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