Archives of Environmental Protection PL ISSN 2083-4772

Vol. 41 no. 4 pp. 104–114 DOI 10.1515/aep-2015-0045

© Copyright by Polish Academy of Sciences

and Institute of Environmental Engineering of the Polish Academy of Sciences,
Zabrze, Poland 2015

Mechanisms of stress avoidance and tolerance by plants

used in phytoremediation of heavy metals
Anna Małachowska Jutsz*, Anna Gnida

Silesian University of Technology

Department of Environmental Biotechnology, Poland

* Corresponding author’s e-mail: [email protected]

Keywords: phytoremediation, soil, heavy metals, stress avoidance, stress tolerance

Abstract: Heavy metal pollution of soil is a significant environmental problem and has a negative impact on
human health and agriculture. Phytoremediation can be an alternative environmental treatment technology, using
the natural ability of plants to take up and accumulate pollutants or transform them. Proper development of plants
in contaminated areas (e.g. heavy metals) requires them to generate the appropriate protective mechanisms against
the toxic effects of these pollutants. This paper presents an overview of the physiological mechanisms of stress
avoidance and tolerance by plants used in phytoremediation of heavy metals.

Introduction role in metabolic processes and the mechanisms of absorption,

accumulation and excretion by living organisms. Ability of
Natural sources of heavy metal pollution associated with heavy metals to penetrate into higher plants depends on the soil
migration and circulation of metals in the environment properties and the conditions prevailing in the environment as
are associated with such processes as volcanic eruptions, well as physico-chemical form in which the element occurs.
weathering of rocks, forest fires, and evaporation from the Usually edible parts of the plant, roots and leaves, have an
surface of the oceans. However, more important is the role of ability of increased accumulation of heavy metals. From this
the processes related to human activities resulting from rapid it follows that the carrot, radish, beetroot, parsley and lettuce
development of civilization (anthropogenic sources of heavy will have a greater degree of metal contamination than plants
metals). Metals introduced into the environment undergo whose fruits are edible. Plants also have developed a system for
a variety of processes. selective accumulation of trace elements from the surrounding
Metals in the soil may have various forms, have environment. Some plants possess a predisposition to
a high ability to form sparingly soluble salts and oxides, are accumulate certain trace elements. Since contamination of soils
adsorbed on the surface of minerals and may be bind with and water with toxic heavy metals is a serious environmental
organic acids and humic substances. This is conducive to problem, therefore effective remediation methods are
a long period of residual metals in the soil, and the time of its necessary. Physical and chemical methods for cleanup and
removal, e.g. by water leaching, may be up to several hundred restoration of heavy metal-contaminated soils have serious
years. In contrast to organic substances, heavy metals do not limitations, such as high cost, irreversible changes in soil
undergo decomposition. Heavy metals cannot be destroyed properties, destruction of native soil microflora and creation of
biologically; they can only be transformed from one oxidation secondary pollution problems. In contrast, phytoremediation
state or organic compound to another. Remediation of soil is a better solution to the problem. It is a technology for
contaminated with heavy metals is more difficult than the treatment of the environment (soil, groundwater and surface
remediation of other contaminations (De Jing et al. 2007). water, sediments and air), using the natural ability of plants
Plants are the most important link in the food chain resulting to collect and accumulate unwanted substances or cause their
from the transfer of metals from soil to animal organisms. The degradation and transformation (Cunningham and Berti 1993,
increased content of heavy metals in soils pose a real danger of Cunningham and Ow 1996, McGrath et al. 2001, Garbisu et al.
penetration into the plant, which in turn means turning metals 2002, Kamnev 2003, Małachowska-Jutsz et al. 2011).
into food chain of the ecosystem. Heavy metals can easily get This technology is based on such properties of certain
from the surface layers of soil into the plants and then to each plants as:
link in the food chain, causing carcinogenic and mutagenic – tolerance to high concentrations of toxic compounds,
effects in living organisms. The accumulation is significantly – assimilation, accumulation and metabolism of toxic
higher in the walls and cell membranes, resulting in inhibition substances in plant organelles,
of proper growth. Metal toxicity depends not only on its – conversion of toxic substances present in the
concentration in the environment, but also on their biochemical environment into non-toxic compounds.
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 Mechanisms of stress avoidance and tolerance by plants used in phytoremediation of heavy metals 105

Phytoremediation is a method, which has great Rhizofiltration

potential for application; its greatest advantage is low cost (even Rhizofiltration is a type of phytoremediation that uses plant
1000-fold cheaper in comparison with conventional methods). roots to absorb, concentrate and precipitate contaminants
The area of the European Union is approx. 52 million hectares, present in the soil through the plant root system into the
of which 16% are contaminated. The north-western part of harvestable parts of the roots and above-ground shoots
Europe and areas around the urban agglomerations are the (Verma et al. 2006, Lee et al. 2010). The plants are raised
most polluted. It is estimated that over the next 20–25 years, hydroponically and transplanted into metal-polluted water
the EU will spend about 100 billion euros for the treatment where they absorb and concentrate the metals in their roots and
of the most degraded areas. These data indicate the need to shoots. Root exudates and changes in rhizosphere pH may also
intensify research on phytoremediation, which is cheap and cause metals to precipitate onto root surfaces. Roots or whole
alternative method of land treatment. plants are harvested for disposal after they become saturated
The aim of the study was a brief presentation of with the metal contaminants (Padmavathiamma and Li 2007).
avoidance mechanisms and stress tolerance mechanisms in This method is mainly used to remove such heavy metals
plants related to the excessive presence of heavy metals based as lead, cadmium, zinc and uranium isotopes (mass number
on the available literature data. This paper summarizes the of 230, 234, 235, and 238, respectively) from contaminated
strategies of metal inactivation or immobilization, strategies of groundwater.
absorption limitation and transformation of metals by plants.
This review article comprehensively discusses the background, Phytostabilisation
concepts and future trends in phytoremediation of heavy The next course of action to be taken in the case of
metals. phytoremediation of soil contaminated with heavy metals is
phytostabilisation. Certain plant species are used to immobilise
Phytoremediation of heavy metal the contaminants in the soil by absorption and accumulation
by roots, adsorption on the surface of roots, or precipitation
contaminated soil
in the zone adjacent to the plant roots. The phytostabilisation
Depending on the nature of the biological processes used uses abilities of exudates of some plant roots for reduction in
in the environmental treatment the following types of the bio-availability of toxic substances (Cheraghi et al. 2011)
phytoremediation may be distinguished: phytoextraction, as the primary purpose of phytoremediation is to prevent the
rhizofiltration, phytostabilisation, phytodegradation, migration of metals in the environment. Root exudates may
rhizodegradation or phytoevaporation. Phytoextraction, act in two ways: toxic metal ions precipitate as insoluble
phytostabilisation, rhizofiltration and phytoevaporation are salts (e.g. lead in the form of lead phosphate) or reduce the
usually used for treatment of soil contaminated with heavy harmful ions (such as CrO42- and CrO72- to Cr3+) by changing
metals (HM). Table 1 presents selected examples of field the soil redox (reduction-oxidation) potential. Plants used in
studies performed while phytoremediation of soil contaminated phytostabilisation should have an extensive root system and
with one or more heavy metals. The most popular type of a low degree of metal translocation from roots to shoots (for
phytoremediation is phytoextraction, sometimes combined example the grass studied by a group of British researchers
with phytostabilization. (Wong and Bradshaw 2002) – Agrostis teniuis sp. Goginan
and Parys and Festuca rubra sp. Merlin). There are several
Phytoextraction parameters that predestine some plants to a particular technique.
Phytoextraction, also called phytoaccumulation, refers to Biological absorption coefficient (BAC) is the ratio of an
the uptake and translocation of metal contaminants in the element concentration in plants to its concentration in soil. Bio-
soil by plant roots into above-ground components of the -concentration factor (BCF) is a ratio of metal concentration
plants. Certain plants, called hyperaccumulators, absorb in plant roots to its concentration in soil. Translocation factor
unusually large amounts of metals compared to other (TF) is a metal concentration ratio of plant shoots to roots.
plants and the ambient metals concentration. Natural metal Plants with a high biological absorption coefficient (BAC >
hyperaccumulators are plants that can accumulate and tolerate 1) are suitable for phytoextraction. Plants with a high bio-
greater metal concentrations in shoots than those usually found -concentration factor (BCF > 1) and low translocation factor
in non-accumulators, without visible symptoms. Examples of (TF < 1) have the potential for phytostabilisation (Yoon et al.
commonly reported hyperaccumulators are given in Table 2 2006).
(Padmavathiamma and Li 2007).
The success of phytoextraction depends primarily on the Phytoevaporation
choice of the plant, which should have a high tolerance to high Phytoevaporation is associated with the phenomena of
concentrations of heavy metals and a substantial degree of HM contaminants assimilation and transpiration by a plant, and
accumulation, as well as a high degree of movement of metals its further release into the atmosphere in the same or modified
from roots to parts exposed to air. A very important feature of form. This method is applicable for treatment of soils and
a plant used for phytoextraction is the abundant production of water contaminated with such inorganic compounds as arsenic,
biomass and a high cut top for easy harvesting. Phytoextraction mercury, selenium and their volatile derivatives (Zayed et
efficiency is measured by the accumulation of the metal per unit al. 1998). The best-known example of phytoevaporation
of mass, thus plants that produce a large amount of biomass, is remediation of soil and groundwater contaminated with
such as crop plants (e.g. Brassica juncea (L.) Czern.) may be an selenium. Selenium is taken up by plants in the form of
alternative to a hyper-accumulators (Kumar et al. 1995, Bricker soluble ions SeO42- and SeO32- and secreted in the form of
et al. 2001, Lasat 2002, Tomović et al. 2013). dimethyl selenide (de Souza et al. 1999). Phytoevaporation of
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106 A. Małachowska Jutsz, A. Gnida

Table 1. Selected phytoremediation field studies (based on: Green and Hoffnagle 2004)

Country Mechanism Contaminant Plant Reference

USA PhExt 1
cadmium Festuca aerundinacea MSE 2001
lead MSE 2004
zinc
USA PhStb2 lead Mix of herbaceous species: Western Brown and Chaney 2000
zinc wheat grass
cadmium
Poland PhExt1 cadmium Brassica sp, Sinapis alba, Helianthus Institute for Ecology
lead sp, Ricinus communis, Zea mays of Industrial Areas 1998
zinc
Switzerland PhExt1 cadmium Basket willow (Salix viminalis) Hammer et al. 2003
copper
zinc
Canda PhExt1 lead Garden Pea (Pisum sativum) and Environment Canada 2000
copper Indian Mustard (Brassica juncea)
USA RhDg3 diesel fuel, lead, TPH Bermuda grass, rye grass, white Banks et al. 1998
clover, tall fescue
USA PhStb2 PhExt1 lead Hybrid poplars Pierzynski et al. 2002a
zinc
cadmium
USA PhExt1 lead Indian mustard, sunflower Blaylock 2000
Switzerland PhExt 1
cadmium Basket willow (Salix viminalis) Hammer et al. 2003
copper
zinc
USA PhExt1 arsenic Eucalyptus, Tamarisk Geomatrix 2004
sodium
China PhExt1 cadmium Vetiver grass Chen et al. 2000
lead
zinc
USA PhExt1 lead Indian mustard (Brassica juncea) and FRTR 2000
PhStb2 sunflower (Helianthus annus)
USA PhExt1 lead Indian mustard, sunflower, mixed Rock and Steve 2003
grasses
USA PhStb2 PhExt1 cadmium tall fescue Pierzynski et al. 2002b
lead
zinc
China PhExt1 zinc Vetiver grass (V. zizanioides), Yang et al. 2003
lead Sesbiana species (S. sesban,
copper S. rostrata)
cadmium
USA PhExt1 lead Indian Mustard (Brassica juncea) and US EPA 2001
sunflower
USA PhExt1 cadmium Bush beans (Phaseolus vulgaris) Martin and Kaplan 1998
chromium
vanadium
1
phytoextraction; 2 phytostabilization; 3 rhizodegradation

mercury is connected with the breeding of transgenic plants redox potential, organic matter content and the presence of
(Arabidopsis thaliana) with the insertion of bacterial genes other elements. The form of the metal is a very important factor.
– merA from E. coli (encoding mercury reductase) and merB Free ions are taken the most quickly. Metals enter the interior
from Salmonella typhimurium (encoding methylmercury of the plant cells by diffusion, endocytosis, or with the aid of
lyase). These enzymes reduce toxic ions Hg2+ to less toxic, phytochelatins and metallothioneins characterized by high
volatile metallic mercury Hg0. Despite the attractiveness of the affinity for heavy metal. After penetration into the cytoplasm
phytoevaporation process (no waste) it poses a major threat the metal ions are bound by the low molecular weight ligands,
to the environment and human life (Cargnelutti et al. 2006). and then transported to the vacuole, which protects the plant
Intake of heavy metals by plants depends mainly on soil pH, from serious physiological disorders. Plants have evolved
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 Mechanisms of stress avoidance and tolerance by plants used in phytoremediation of heavy metals 107

Table 2. Accumulation of heavy metals by selected plants (Maciak 2003, Padmavathiamma and Li 2007, Boyd 2009)

Metal content in the plant,

Plant species Metal Reference
mg/kg dry mass
39600 Reeves and Brooks 1983
Thlaspi caerulescens Zn 51600 Cunningham et al. 1997
34000 Jhee et al. 1999
1800 Cunningham et al. 1997
Thlaspi caerulescens Cd
1900 Jiang et al. 2005
Reeves and Brooks 1983
Thlaspi rotundifolium Pb 8200–8500
Blaylock et al. 1997
Brassica juncea Pb 16000 Blaylock et al. 1997
Alyssum murale Ni 30000 Angle et al. 2003
Berkheya coddii Ni 37000 Augustyniak et al. 2002
Haumaniastrum robertii Co 10200 Brooks 1998
Asparagus racemosus Se 14900 Beath et al. 1937
Pteris vittata
As 27000 Wang et al. 2002
Berkheya coddii

a number of mechanisms protecting them from adverse effects of phytostabilisation. AM hyphae were able to accumulate
of heavy metals presence. 10–20 times higher rates of Cd in comparison to plant roots.
Małachowska-Jutsz (2010) found that the colonisation of
Plants mechanisms of stress avoidance rhizosphere by mycorrhizal fungi had a beneficial effect on plant
root growth and development, as well as on the hydrocarbons
Success of phytoremediation depends on specific mechanisms degradation by accompanying organisms, e.g. efficiency of
of stress avoidance and stress tolerance in plants resulting heavy fractions removal increased 15 times in comparison with
from the presence of high concentrations of heavy metals in control without AM. An important protective mechanism that
soil. It also depends on the physico-chemical properties of enables plants to survive in an environment contaminated with
the soil itself, the form of the metal, as well as the presence heavy metals is immobilisation of metals within the mycelium
of microorganisms, also the mycorrhizal fungi. The most and inhibition of their movement to plant tissues (Bradley et al.
important mechanisms to avoid stress include: synthesis of 1982, Dueck et al. 1986, Killham and Firestone 1983, Heggo
callose, mycorrhizae, limitation the metal assimilation by the et al. 1990, Gucwa-Przepiora et al. 2007, Chen et al. 2008,
root, the removal of excess metals and binding metal in the Miransari 2011). Mycorrhizal fungi reduce the penetration of
cell wall. metal into the cells by:
 release of metal chelating agents, such as citric acid
Synthesis of callose and oxalic acid (Zn, Pb, Cu, Cd, Ni, Mn), phenolic
In the plant cell, the earliest defence reaction in the case of compounds, siderophores (Fe) and phosphate ions
heavy metal presence is a synthesis of callose (β-1, 3 glucan). forming insoluble metal salts,
This polysaccharide is deposited on the outside of the cell  metal adsorption on the surface of fungal cells by
membrane, thereby reducing the diffusion of metal ions into precipitation of sulphides and hydrated iron oxides,
the cell. The enzyme, which is involved in the synthesis of  immobilisation and accumulation inside the
callose, is β-1, 3-glucan synthetase (Wójcik and Tukiendorf different fungal structures including arbuscules,
1995, Woźny and Przybył 2004, Miransari 2011). vesicles and hyphae,
 detoxification within the cells – binding by
Mycorrhizae cytoplasm metallothionein and binding by vacuole
Another mechanism, known as mycorrhizae, enables symbiotic polyphosphates.
relationships between non-pathogenic fungi and bacterial
biocenosis of higher plant roots. Mycorrhizae increases survival Limitation of the metal assimilation by the roots
of plants in harsh conditions by reducing the stress associated Another defence mechanism is to limit the metal assimilation
with the availability of water and some nutrients (phosphorus), from the environment by the roots. Literature data (Driouich
increasing their resistance to pathogens and modifying the et al. 2007, Guo et al. 2009, Cai et al. 2011, Miransari 2011,
structure of the roots and the medium, in which they grow (Liu Meier et al. 2012) indicate that in an environment contaminated
et al. 2000, Turnau et al. 2002, Miransari 2011, Malachowska- with heavy metals plant roots secrete a number of substances
Jutsz et al. 2010). Research studies have shown that arbuscular that can bind ions and limit their assimilation by plants.
mycorrhizae (AM) fungi are able to alleviate the stress of heavy Among such compounds are organic acids, and substances
metals and petroleum substances (Tam 1995, Davies et al. 2001, present in root extracellular matrix composed mainly of e.g.
Turnau and Mesjasz--Przybyłowicz 2003). Janouskova et al. simple sugars, phenols, amino acids and polysaccharide gels.
(2006) found that AM fungi are able to alleviate the unfavourable Reduction of the availability of metal ions occurs also through
effects of cadmium (Cd) on plant growth by the process the production of an oxidizing zone around the roots. As
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108 A. Małachowska Jutsz, A. Gnida

a result a reduced form of metals are oxidized and become less such as enzymes. A relatively well-known example is the
soluble and therefore less available to plants. Another way to binding and transport of copper ions that occurs in the cells of
reduce the toxicity of metals is the ability of roots to change Arabidopsis thaliana. In this case the chaperone CCH delivers
the rhizosphere pH. The increased pH causes a decrease in the copper ions to the chloroplasts. Another chaperon AtCOX17
availability of metals (Yang et al. 2005, Siwek 2008a, Siwek conducts the copper atoms to the mitochondrial cytochrome
2008b, Miransari 2011). oxidase and cytosolic Cu/Zn superoxide dismutase. Its synthesis
is a response to the disruption of mitochondrial functioning
The removal of excess metals (Hall and Williams 2003, Woźny and Przybył 2004).
Another strategy is the ability of plants to remove excess metals
in the form of crystals by salt glands of the leaf epidermis. Glutathione
For example, copper, nickel, zinc, iron and manganese can be Glutathione (GSH; γ-glu-cys-gly) is the most common low
removed in such a way by the plant Armeria maritima ssp halleri. molecular weight thiol compound in nature. It occurs in all
The removal of metal excess may also be performed through prokaryotic and eukaryotic cells. GSH is produced by the
hydathodes (e.g. in Minuartia verna) and ectoderms (e.g. in synthesis of glutamate (Glu), cysteine (Cys) and glycine
Silene vulgaris). Metals may also be transported to the ageing (Gly) (Meister and Anderson 1983). It is synthesized in two
leaves and removed along with them. Such a phenomenon has stages and the reactions are catalyzed by g-glutamylcysteine
been observed for example in Anthyllis vulnenaria L. (Zn) and synthetase (γ-ECS) and glutathione synthetase (γ -ECS).
Biscutella laevigata L. (Zn). The literature data (Baranowska- In bacteria, yeasts, plants and animals GSH inhibits γ-ECSs
Morek 2003, Olko 2009) confirm that heavy metals can also through feedback inhibition that was considered as the
be accumulated in fibres and idioblasts. There are examples of prime regulation mechanism of the pathway (Meister 1995,
sequestration of lead by Nicotiana tabacum, nickel by Alyssum Mendoza-Cozatl and Moreno-Sanchez 2006). In plants and
lesbiactum, cadmium by Brassica juncea (L.) Czern. and zinc some of the yeast cells GSH is the precursor of phytochelatins
by Avicennia marina (Baranowska-Morek 2003, Olko 2009). synthesis. It has a unique structure, because an a-amino group
of cysteine is bound to a γ-carboxy group of glutamate (not
Binding metal in the cell wall α-carboxy group as usually), thereby forming an unusual
Another plant defence mechanism against the toxic effects of peptide bond (isopeptide bond). This bond protects glutathione
heavy metals is its binding in the cell wall. For some species, against intracellular peptidases. The only enzyme able to break
80–95% of the metal taken up by the cells can be fixed (this down the structure is positioned on the outer side of the cell
particularly applies to ions of lead, copper and zinc). The cell membrane, γ-glutamyl transferase, also called glutathionase
walls are composed of pectins, which contain galacturonic acid (Gilbert 1990).
molecules and many of the methylated (COOCH3) carboxyl Another feature of GSH is the presence of a thiol
groups, hemicelluloses and cellulose. Their dissociation leads group (-SH) in the structure belonging to a cysteine moiety.
to the appearance of negatively charged groups, which are The presence of this group is directly associated with its
typically saturated with calcium. In the presence of heavy biological function as they are the most reactive chemical
metals (Cd2+, Pb2+, Cu2+) calcium ions may be competitively groups which are present in the cell (Gilbert 1990). Glutathione
replaced by metals cations. In this way, toxic metal ions are is an antioxidant. Its presence determines the detoxification of
immobilised in the cell wall. Phenolic compounds present in hydrogen peroxide, organic peroxide and other reactive oxygen
a cell wall may act similarly. Under stress conditions induced forms, as well as exogenous and endogenous electrophilic
by the presence of metals, the physical properties of the cell compounds. The redox potential of the GSSG/GSH fosters
wall can be changed. The amount of transverse bonds between reactions between reduced glutathione and oxidized forms of
wall constituents – protein molecules, saccharides and phenols other antioxidants. It has the ability to chelate hazardous metal
is increased. It can also lead to lignification or suberisation of ions, participates in reconstructing damaged cell components,
the cell wall, which causes the wall to become more compact especially proteins and lipids, and DNA cell membranes
and stiffer, and thus less permeable (Woźny and Przybył 2004, (Pastore et al. 2003). In addition, the compound is involved
Miransari 2011). in maintaining the proper redox potential of cells (Cotgreave
and Gerdes 1998), which is important in the regulation of
Mechanisms of stress tolerance intracellular metabolism (Pastore et al. 2003), apoptosis (Hall
1999a, b) and in the growth and differentiation of cells (Poot at
In some cases the metal ions may overcome the plant protective al. 1995, Hall 1999).
barrier and penetrate into their cells. Factors responsible for Gupta et al. (2002) have shown that exposition of
the rapid and effective detoxification of the metals affect the plants to cadmium results in increase of cysteine as well as
tolerance of plants to metal. These factors are: binding the metal other thiol compounds. This suggests that Cd activates first step
complexes with different ligands (chelation) and transportation in the GSH biosynthesis, probably synthesis of cysteine. These
and accumulation of the complexes in vacuoles. These processes observations can be used to assess the oxidative stress of plants
take place with the participation of associated proteins, growing in soils contaminated with cadmium, and perhaps with
chaperones, phytochelatins, metallothioneins and organic and other heavy metals. Bruns et al. (2001) have shown that after
amino acids (Hall and Williams 2003, Miransari 2011). exposure of plants to the 100 mmol Cd/L the concentration
of GSH significantly increased in the plants cells, as well as
Chaperones cysteine and γ-glutamyl-cysteine. The authors showed that
Chaperones are special proteins that transport ions into the complexes GSH/Cd are transported to the cytoplasm. It
places in the cell, where they are incorporated into molecules suggests that GSH plays a key role in the detoxification of
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 Mechanisms of stress avoidance and tolerance by plants used in phytoremediation of heavy metals 109

heavy metals during their transport to the cytoplasm. From small peptides with the general structure (γ-Glu-Cys) n-Gly,
there they could be downloaded by the vacuole and degraded, where n is from 2 to 11 (usually 2–5). Phytochelatins can
and cadmium is accumulated in the form of phosphates. be produced enzymatically as a consequence of presence
of many metals (Cobbett 2000, Rauser 2000). They are
Metallothioneins synthesized from reduced glutathione (GSH) and catalysed
Tolerance and ability of plant cells to accumulate large amounts by phytochelatin synthetase (PCS) (Grill et al. 1989), which
of heavy metals is concerned with the presence of proteins that is activated by Cd2+, Ag+, Bi3+, Pb2+, Zn2+, Cu2+, Hg+ and Au+.
bind metal ions (metallothionein and phytochelatins). Intake They are not encoded by genes directly, but the products of
of metal ions by the roots and its transport to shoots requires a biosynthetic pathway (reactions 1 to 4).
the participation of specific transport proteins (e.g. P-ATPase
– subfamily P1B, CDF – Cation Diffusion Facilitator, Nramp Gly + Cys → GCS (1)
– Natural resistance associated macrophage protein, ZIP – Zinc
regulated transporter, Iron – regulated transporter-like protein, γ-Glu-Cys + Glu → GS (2)
YSL – Yellow Stripe1-like and family ABC – ATP Binding GSH → PCS+Cd (3)
Cassette). Biotransformation enzymes are required for changing
the oxidation state of the elements. Plants do not have enzymes PC → PC–Cd → HMT1 vacuole (4)
that enable reduction of e.g. mercury ions to gaseous form
(Hussein et al. 2007). Metallothioneins (MTs) are cysteine- where GCS – γ-glutamylcysteine synthetase, GS – GSH
-rich proteins of low molecular weight which bind the metal synthetase, PCS – phytochelatin synthase, HMT1 – a vacuolar
ions with thiol groups. They are involved in the detoxification membrane transporter of PC-Cd complexes.
of copper and cadmium ions, and buffer the concentration of There is number of structural variants of PCs in plants,
zinc in the cytoplasm. Probably they also provide zinc ions such as (γ-Glu-Cys)n-β-Ala, (γ-Glu-Cys)n-Ser, and (γ-Glu-
to zinc-dependent enzymes. They are products of mRNA Cys)n-Glu (Cobbett 2000, Rauser 2000).
translation found in animals and plants. MTs play a role in Research performed on more than 200 plant species
detoxification of heavy metals in animals and fungi, although showed their ability to detoxify cadmium and other heavy
their exact function is not completely understood (Robinson metals. The mechamism of detoxication was chelation of heavy
et al. 1993, Hall 2002). In plants they may participate in metal metals to peptides (Gekeler et al. 1989). Grill et al. (1987) and
homeostasis since correlation between MT RNA levels and Le Faurcheur et al. (2005) created a series of heavy metals
naturally occurring differences in tolerance to heavy metals in according to their strength of PCs production. It is as follows:
Arabidopsis ecotypes were observed (Murphy and Taiz 1995, Cd>Pb>Zn>Sb>Ag>Hg>As>Cu>Sn>Au>Bi. Cadmium is
Murphy et al. 1997, Guo et al. 2008). Other proposed functions known to be the strongest inducer of PC in plants and algae
of MTs in plants are: metal detoxification (Domenech et al. (Maitani et al. 1999, Grill et al. 1987).Some heavy metals as
2006, Roosens et al. 2008), senescence (Coupe et al. 1995, Ni, Te W or Se were found not to be able for activation of PC
Hsieh et al. 1995) and protection against abiotic stress (Zhou et synthesis (Zenk 1996).
al. 2005). In different organisms, the MT expression correlates
with metal concentration what suggests that they can be Metal binding
effective markers of environmental conditions (Morris et al. Metal ions present in the cytoplasm can also attach directly
1999). Scientists (Morris et al. 1999, Zhu et al. 1999a 1999b, to the thiol groups of glutathione and be transported to the
Cobbett and Goldsbrough 2002, Zimeri et al. 2005) report that vacuole (Zhu et al. 1999a, Miransari 2011). There, the complex
isolation and characterisation of MTs in model bio-indicator undergoes decomposition and the metal ions are bound to
organisms could also contribute to understanding of the phosphates. This mechanism is similar to phytochelatins
biological response to pollutants in the environment. functioning with such a difference that reduced glutathione
is the complexing agent (Dixon et al. 1998, Freeman et al.
Phytochelatins 2004, Freeman et al. 2005). Organic acids such as malic,
The principal role of phytochelatins (PC) is transport of citric, oxalic acid can bind metal ions. Metal is associated to
divalent metal from the cytoplasm into the vacuole, where an acid molecule through a carboxyl group (COOH) and in
in low pH conditions the PC-metal complex undergoes this form transported to the vacuole. The complex of acid and
dissociation, and the metal ions are combined with organic metal possesses a form of transport of metal through the xylem
acids (Clemens et al. 1999, Clemens 2006). They take part vessels. For example, iron is transported in the form of citrate
in maintaining a homeostasis of the divalent ions in the cells that results in reduction of the binding of the metal by ion-
which, depending on requirements, can be released from the -exchange structures. Citric acid is also likely to be the main
complexes and used, for example, to produce metalloenzymes compound which binds cadmium ions (at low concentration
(Bar-Ness et al. 1991, Cobbett and Goldsbrough 2002, Hirata of the element), nickel and zinc. In turn, malic acid binds
et al. 2005, Gasic and Korban 2007a, Gasic and Korban zinc ions (Singla-Pareek et al. 2006). Histidine is an amino
2007b). Phytochelatins are considered to play a major role acid involved in metal binding. It forms a complex with the
in metal detoxification (Le Faucheur et al. 2005). They ions, in particular nickel, but also with zinc and copper. In the
play role in homeostasis of heavy metals in plants, and this plant that hyper-accumulates nickel Alyssum lesbiacum the
is the mechanism that regulates the metal ions availability concentration of histidine in xylem juice after exposure to this
in plant cells (Guo et al. 2008). In majority of plants they metal was 36-fold higher. Another amino acid – nicotianamine
are composed of three types of amino acids: glutamic acid has an ability to chelate iron ions and copper, and zinc to
(Glu), cysteine (Cys) and glycine (Gly). Phytochelatins are a lesser extent (Singla-Pareek et al. 2006).
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110 A. Małachowska Jutsz, A. Gnida

Plants or metabolic pathways engineering Conclusions

Singla-Pareek et al. (2006) reported a novel mechanism of
heavy metal tolerance in plants that involved engineering of Phytoremediation is environment-friendly and ecologically
the glyoxalase pathway. This pathway comprises two steps. responsible solar-driven technology with good public
One is catalysed by glyoxalase I while the other by glyoxalase acceptance. It is a relatively recent technology and is mostly in
II. The engineering strategy has been found to be suitable research stage. Its research is highly interdisciplinary in nature
for improvement of heavy-metal tolerance in transgenic and requires background knowledge in soil chemistry, plant
tobacco (N. tabacum). The glyoxalase transgenics were able biology, ecology and soil microbiology as well as environmental
to grow, flower, and set normal viable seeds in the presence engineering. Research is in progress to screen native plants for
of 5 mM ZnCl2 without any yield penalty. The concentration phytoremediation of heavy metals and to evaluate the effect
of endogenous ions revealed that roots were the major sinks of different parameters on phytoremediation efficiency. An
for excess Zn accumulation while its amount in transgenic improved understanding of heavy metal uptake by plants from
plants seeds was negligible. It is suggested that glyoxalase soil will also help in promoting phytomining – a plant-based
over-expression might confer tolerance to other heavy metals, eco-friendly mining of metals, which can be used for extraction
such as Cd and Pb. Transgenic plants over-expressing both of metals even from low-grade ores. Phytoextraction of heavy
glyoxalase I and II had reflected better relative tolerance than metals is expected to be a commercially viable technology
transgenic plants over-expressing either glyoxalase I or II for phytoremediation and phytomining of heavy metals in the
individually. Biochemical investigations of such transgenics future. Plants have evolved a number of mechanisms by which
have indicated the control over methylglyoxal (MG) and they can survive in soils contaminated with metals. Generally,
malodialdehyde (MDA) accumulation under high levels these mechanisms represent two strategies: avoiding stress
of Zn exposure. Usage of glutathione biosynthetic inhibitor and stress tolerance. The first relies on reduction of metal
(buthionine sulphoximine) caused an increase in PCs level accumulation and prevention of its penetration into a symplast.
and maintenance of GSH/GSSG redox ratio in transgenic The stress tolerance mechanisms begin to function when the
plants. This provided tolerance to Zn stress (Singla-Pareek metal crosses the cell membrane. The most important role in
et al. 2006). Depending on the specific features of the plants, the whole process is that of the plants and rhizosphere micro-
they are useful in a particular technique of phytoremediation. -organisms. Without their participation the phytoremediation
Such plants should have a very well developed root system, process does not proceed. There are a number of species in
rapid growth, produce large amounts of biomass, be able nature which are capable of growing in soils contaminated with
to accumulate and tolerate high concentrations of heavy high concentrations of heavy metals. The role of rhizosphere
metals (Eapen et al. 2005). None of the many natural microorganisms in the resistance of plants to stress caused
phytoremediators meets all of these requirements. Recognition by the presence of heavy metals cannot be ignored. In recent
and understanding of the phytoremediation mechanisms years transgenic plants have become more and more popular
enables the obtaining of transgenic specimens that are almost and used in phytoremediation processes. Research is being
perfect phytoremediators. Thlaspi caerulescens is a plant that conducted to genetically modify some suitable plants for better
is often used in studies focused on the natural resistance of phytoremediation of heavy metals and other xenobiotics.
plants to high concentrations of heavy metals. Comparison Studies are also being done to identify and characterize different
of its detoxification mechanisms with mechanisms presented proteins involved in cross-membrane transport and vacuolar
by other plants from the cabbage family Thlaspi arvense sequestration of heavy metals. Advancement and achievements
enabled selection of the genes potentially useful in the in such molecular studies will greatly help in understanding the
designing of plants eligible in phytoremediation. Frequently mechanism and enhancing the efficiency of phytoremediation.
used transporter genes are genes encoding heavy metals or the However, the problem is not just the acquisition of such
heavy metal binding ligands (Milner et al. 2008). plants, but also the need to change the existing legislation and
Tolerance and ability of plant cells to accumulate overcome the reluctance of public opinion to accept transgenic
large amounts of heavy metals is concerned with the presence organisms. Despite the obvious advantages such as: low cost of
of proteins that bind metal ions (metallothionein and the process, the minimum level of violations of environmental
phytochelatins). However, it is possible to create transgenic homeostasis, visual attractiveness, and phytoremediation,
plants with bacterial genes, since some bacteria have mercury each technology has also disadvantages. The most important
resistance genes typically located in the mer operon. Such disadvantage is the long-lasting treatment, the limited scope of
operon consists of gene merA coding mercury reductase, gene the roots, too high concentrations of metals which can cause
merB coding lyase of organic derivatives of mercury and genes bending of plants. Therefore, it is necessary to conduct intensive
merP, merT, merC, merE, merG coding enzymes involved in research on phytoremediation which may result in elimination
the transport of mercury ions (Milner and Kochian 2008). of its limitations in the near future and then phytoremediation
will become the primary method of treatment of soil.
Repair of cell damage
Tolerance of stress caused by toxic heavy metals also relies
on the fast and effective repair of damage caused in the cell. References
Repair functions are helped by the heat shock protein (HSPs), Angle, J.S., Baker, A.J.M., Whiting, S.N. & Chaney, R.L. (2003). Soil
whose expression was first observed in plant cells exposed to moisture effects on uptake of metals by Thlaspi, Alyssum,
high temperatures. They are also synthesized in the case of and Berkheya, Plant Soil, 256, pp. 325–332.
stress caused by other factors, including heavy metals (Singla- Augustyniak, M., Mesjasz-Przybylowicz, J., Nakonieczny, M.,
Pareek et al. 2006). Dybowska, M., Przybylowicz, W. & Migula, P. (2002).
Unauthenticated
Download Date | 2/19/16 2:12 PM
 Mechanisms of stress avoidance and tolerance by plants used in phytoremediation of heavy metals 111

Food relations between Chrysolina pardalina and Berkheya Clemens, S., Kim, E.J., Neumann, D. & Schroeder, J.I. (1999).
coddii, a nickel hyperaccumulator from South African Tolerance to toxic metals by a gene family of phytochelatin
ultramafic outcrops, Fresenius Environmental Bulletin, 11, synthases from plants and yeast, EMBO Journal, 18,
pp. 85–90. pp. 3325–3333.
Banks, M.K., Schwab, A.P., Govindaraju, R.S., Lewis, S., Rathbone, Clemens, S. (2006). Toxic metal accumulation, responses to exposure
K. & Kulakow, P. (1998). Phytoremediation of soil and mechanisms of tolerance in plants, Biochimie, 88,
contaminated with hazardous chemicals: a field assessment pp. 1707–1719.
at the Craney Island fuel terminal. In: Final Report of DOD Cobbett, C.S. (2000). Phytochelatin biosynthesis and function in
AATDF project. Rice University Publishing, USA 1998. heavy metal detoxification, Current Opinion in Plant
Baranowska-Morek, A. (2003). Mechanisms of plants tolerance to toxic Biology, 3, pp. 211–216.
influence of heavy metals, Kosmos, 52 (2–3), pp. 283–298. Cobbett, C. & Goldsbrough, P. (2002). Phytochelatins and
(in Polish) metallothioneins: roles in heavy metal detoxification
Bar-Ness, E., Chen, Y., Hadar, Y., Marchner, H. & Romheld, V. and homeostasis, Annual Review of Plant Biology, 53,
(1991). Siderophores of Pseudomonas putida as an iron pp. 159–182.
source for dicot and monocot plants, Plant Soil, 130 (1–2), Cotgreave, I.A. & Gerdes, R.G. (1998) Recent trends in glutathione
pp. 231–241. biochemistry – glutatione-protein interactions: a molecular
Beath, O.A., Eppsom, H.F. & Gilbert, G.S. (1937). Selenium link between oxidative stress and cell proliferation?
distribution in and seasonal variation of vegetation type Biochemical and Biophysical Research Communications,
occurring on seleniferous soils, Journal of American 242, pp. 1–9.
Pharmacists Association, 26, pp. 394–405. Coupe, S.A., Taylor, J.E. & Roberts, J.A. (1995) Characterization
Blaylock, M.J., Salt, D.E., Dushenkov, S., Zakharova, O., Gussman, of an mRNA encoding a metallothionein-like protein that
C., Kapulnik, Y., Ensley, B. & Raskin, I. (1997). Enhanced accumulates during ethylene-promoted abscission of
accumulation of Pb in Indian mustard by soil-applied Sambucus nigra L., Planta, 197, pp. 442–447.
chelating agents, Environmental Science & Technology, 31 Cunningham, S.D. & Berti, W.R. (1993). Remediation of contaminated
(3), pp. 860–865. soils with green plants: an overview, In Vitro Cellular &
Boyd, R.S. (2009). High-nickel insects and nickel hyperaccumulator Developmental Biology, 29 (4), pp. 207–212.
plants: A review, Insect Science, 16, pp. 19–31. Cunningham, S.D. & Ow, D.W. (1996). Promises and prospects of
Bradley, R., Burt, A.J. & Read, D.J. (1982). The biology of phytoremediation, Plant Physiology, 110 (5), pp. 715–719.
mycorrhizae in the Ericaceae. VIII. The role of mycorrhizal Cunningham, S.D., Shann, J.R., Crowley, D.E. & Anderson, T.A.
infection in heavy metal resistance, New Phytologist, 91 (2), (1997). Phytoremediation of contaminated water and soil. In:
pp. 197–202. Kruger EL, Anderson TA, Coats JR (ed.) Phytoremediation
Bricker, T.J., Pichtel, J., Brown, H.J. & Simmons, M. (2001). of soil and water contaminants. ACS Symposium series
Phytoextraction of Pb and Cd from superficial soil: effects 664. American Chemical Society, pp. 2–19, Washington DC
of amendments and croppings, Journal of environmental 1997.
science and health. Part A, Toxic/hazardous substances & Davies, F.T.Jr., Puryear, J.D. & Newton, R.J. (2001). Mycorrhizal
environmental engineering, 36, pp. 1597–1610. fungi enhance accumulation and tolerance of chromium in
Brooks, R.R. (ed.) (1998). Plants that hyperaccumulate heavy metals. sunflower (Helianthus annuus), Journal of Plant Physiology,
CAB International, pp. 384, Wallingford 1998. 158 (6), pp. 777–786.
Brown, S.L. & Chaney, R.L. (2000). Combining residuals to achieve De Jing, Y., He, Z. & Yang, X. (2007). Role of soil rhizobacteria
specific soil amendment objectives, In: Bartels J. (ed.) in phytoremediation of heavy metal contaminated soils,
Land Application of Agricultural, Industrial and Municipal Journal of Zhejiang University SCIENCE B, 8, pp. 192–207.
By-Products. Soil Science Society of America, WI, Dixon, D.P., Cummins, L., Cole, D.J. & Edwards, R. (1998).
pp. 343–360, Madison 2000. Glutathione-mediated detoxification systems in plants,
Bruns, I., Sutter, K., Menge, S., Neumann, D. & Krauss, G.J. (2001) Current Opinion in Plant Biology, 1, pp. 258–266.
Cadmium lets increase the glutathione pool in bryophytes, Domenech, J., Mir, G., Huguet, G., Capdevila, M., Molinas, M. &
Journal of Plant Physiology, 158, pp. 79–89. Atrian, S. (2006). Plant metallothionein domains: functional
Cai, M.Z., Wang, F.M., Li, R.F., Zhang, S.N., Wang, N. & Xu, insight into physiological metal binding and protein folding,
G.D. (2011). Response and tolerance of root border cells Biochimie, 88, pp. 583–593.
to aluminum toxicity in soybean seedlings, Journal of Driouich, A., Durand, C. & Vicre-Gibouin, M. (2007). Formation
Inorganic Biochemistry, 105, pp. 966–971. and separation of root border cells. Review, Trends in Plant
Cargnelutti, D., Tabaldi, L.A., Spanevello, R.M., de Oliveira Jucoski, Science, 12 (1), pp. 14–19.
G., Battisti, V., Redin, M., Linares, CEB, Dressler, V.L., de Dueck, T.A., Visser, P., Ernst, W.H.O. & Schat, H. (1986). Vesicular
Moraes Flores, E.M., Nicoloso, F. & Morsch, V.M. (2006). arbuscular mycorrhizae decrease zinc toxicity to grasses
Mercury toxicity induces oxidative stress in growing in zinc polluted soil, Soil Biology & Biochemistry, 18 (3),
cucumber seedlings, Chemosphere, 65, pp. 999–1006. pp. 331–333.
Chen, B., Roos, P., Zhu, Y.G. & Jakobsen, I. (2008). Arbuscular Eapen, S. & D’souza, S. (2005). Prospects of genetic engineering of
mycorrhizas contribute to phytostabilization of uranium plants for phytoremediation of toxic metal, Biotechnology
in uranium mining tailings, Journal of Environmental Advances, 23, pp. 97–114.
Radioactivity, 99, pp. 801–810. Freeman, J.L., Persans, M.W., Nieman, K., Albrecht, C., Peer, W.,
Chen, H.M., Zheng, C.R., Tu, C. & Shen, Z.G. (2000). Chemical Pickering, I.J. & Salt, D.E. (2004). Increased glutathione
methods and phytoremediation of soil contaminated with biosynthesis plays a role in nickel tolerance in Thlaspi
heavy metals, Chemosphere, 41, pp. 229–234. nickel hyperaccumulators, Plant Cell, 16, pp. 2176–2191.
Cheraghi, M., Lorestani, B., Khorasani, N., Yousefi, N. & Freeman, J.L., Garcia, D., Kim, D., Hopf, A. & Salt, D.E.
Karami, M. (2011). Findings on the phytoextraction and (2005). Constitutively elevated salicylic acid signals
phytostabilization of soils contaminated with heavy metals, glutathione-mediated nickel tolerance in Thlaspi nickel
Biological Trace Element Research, 144, pp. 1133–1141. hyperaccumulators, Plant Physiology, 137, pp. 1082–1091.
Unauthenticated
Download Date | 2/19/16 2:12 PM
112 A. Małachowska Jutsz, A. Gnida

FRTR (2000). Phytoremediation at the open burn and open detonating Hall, J.L. & Williams, L.E. (2003). Transition metal transporters in
area. In: Abstracts of Remediation Case Studies, Volume 4. plants, Journal of Experimental Botany, 54, pp. 2601–2613.
Ensign-Bickford Company, Simsbury, USA 2000. Hammer, D., Kayser, A. & Keller, C. (2003). Phytoextraction of Cd
Garbisu, C., Hernandez-Allica, J., Barrutia, O., Alkorta, I. & Becerril, and Zn with Salix viminalis in field trials, Soil Use and
J.M. (2002). Phytoremediation: a technology using green Management, 19, pp. 187–192.
plants to remove contaminants from polluted areas, Reviews Heggo, A., Angle, J.S. & Chaney, R.L. (1990). Effect of vesicular-
on Environmental Health, 17 (3), pp. 173–188. -arbuscular mycorrihyza fungi on heavy metal uptake by
Gasic, K. & Korban, S.S. (2007a). Expression of Arabidopsis soybeans, Soil Biology & Biochemistry, 22 (6), pp. 865–869.
phytochelatin synthase in Indian mustard (Brassica juncea) Hirata, K., Tsuji, N. & Miyamoto, K. (2005). Biosynthetic regulation
plants enhances tolerance for Cd and Zn, Planta, 225, of phytochelatins, heavy metal-binding peptides, Journal of
pp. 1277–1285. Bioscience and Bioengineering, 100, pp. 593–599.
Gasic, K. & Korban, S.S. (2007b). Transgenic Indian mustard Hsieh, H.M., Liu, W.K. & Huang, P.C. (1995). A novel stress-inducible
(Brassica juncea) plants expressing an Arabidopsis metallothionein-like gene from rice, Plant Molecular
phytochelatin synthase (AtPCS1) exhibit enhanced As and Biology, 28, pp. 381–389.
Cd tolerance, Plant Molecular Biology, 64, pp. 361–369. Hussein, H.S., Ruiz, O.N., Terry, N. & Daniell, H. (2007).
Gekeler, W., Grill, E., Winnacker, E.-L. & Zenk, M.H. (1989). Survey Phytoremediation of mercury and organomercurials in
of the plant kingdom for the ability to bind heavy metals chloroplast transgenic plants: enhanced root uptake,
through phytochelatins, Zeitschrift für Naturforschung, 44c, translocation to shoot and volatilization, Environmental
pp. 361–369. Science & Technology, 41, pp. 8439–8446.
Geomatrix Consultants, Inc. (prepared in association with S.S. Institute for Ecology of Industrial Areas (1998). Final Report for
Papadopulos and Associates Inc.) (2004). Five Year Status Bytom, Poland laboratory and site phytoremediation project.
Report, East Palo Alto, USA 2004. Institute for Ecology of Industrial Areas, Katowice, Poland
Gilbert, H.F. (1990). Molecular and cellular aspects of thiol-disulfide 1998.
exchange, Advances in Enzymology and Related Areas of Janouskova, M., Pavlikowa, D. & Vosatka, M. (2006). Potential
Molecular Biology, 63, pp. 69–172. contribution of arbuscular mycorrhiza to cadmium
Green, C. & Hoffnagle, A. (2004). Phytoremediation field studies immobilisation in soil, Chemosphere, 65, pp. 1959–1965.
database for chlorinated solvents, pesticides, explosives, Jhee, E.M., Dandridge, K.L., Christy, A.M. & Pollard, A.J.
and metals. Environmental Protection Agency Office (1999). Selective herbivory on low-zinc phenotypes of the
of Superfund Remediation and Technology Innovation, hyperaccumulator Thlaspi caerulescens (Brassicaceae),
Washington, USA 2004. Chemoecology, 9, pp. 93–95.
Grill, E., Löffler, S., Winnacker, E.L. & Zenk, M.H. (1989). Jiang, R.F., Ma, D.Y., Zhao, F.J. & McGrath, S.P. (2005). Cadmium
Phytochelatins, the heavy metals-binding peptides of hyperaccumulation protects Thlaspi caerulescens from leaf
plants, are synthesized from glutathione by a specific feeding damage by thrips (Frankliniella occidentalis), New
γ-glutamilcysteine dipeptidyl transpeptidase (phytochelatin Phytologist, 167, pp. 805–914.
synthase), Proceedings of the National Academy of Sciences, Kamnev, A.A. (2003). Phytoremediation of heavy metals: An overview.
USA, 86, pp. 6838–6842. In: Fingerman, M, Nagabhushanam, R. (ed). Recent
Grill, E., Winnackert, E. & Zenk, M.H. (1987). Phytochelatins, Advances in Marine Biotechnology 8: Bioremediation.
a class of heavy-metal-binding peptides from plants, are Science Publishers Inc, Enfield, USA, pp. 269–317.
functionally analogous to metallothioneins, Proceedings of Killham, K. & Firestone, M.K. (1983). Vesicular arbuscular
the National Academy of Sciences, USA, 84, pp. 439–443. mycorrhizal mediation of grass response to acidic and heavy
Gucwa-Przepiora, E., Ma1kowski, E., Sas-Nowosielska, A., metal deposition, Plant Soil, 72 (1), pp. 39–48.
Kucharski, R., Krzyzak, J., Kita, A. & Romkense, O. (2007). Kumar, P.B.A., Dushenkov, V., Motto, H. & Raskin, I. (1995).
Effect of chemophytostabilization practices on arbuscular Phytoextraction: the use of plants to remove heavy metals
mycorrhiza colonization of Deschampsia cespitosa ecotype from soils, Environmental Science & Technology, 29 (5),
Warynski at different soil depths, Environmental Pollution, pp. 1232–1238.
150, pp. 338–346. Lasat, H.A. (2002). Phytoextraction of toxic metals: a review of
Guo, W.J., Meetam, M. & Goldsbrough, P. (2008). Examining biological mechanisms, Journal of Environmental Quality,
the specific contributions of individual Arabidopsis 31 (1), pp. 109–120.
metallothioneins to copper distribution and metal tolerance, Le Faucheur, S., Behra, R. & Sigg, L. (2005). Phytochelatin induction,
Plant Physiology, 164 (4), pp. 1697–1706. cadmium accumulation, and algal sensitivity to free
Guo, B., Liang, Y. & Zhu, Y. (2009). Does salicylic acid regulate cadmium ion in Scenedesmus vacuolatus, Environmental
antioxidant defense system, cell death, cadmium uptake and Toxicology and Chemistry, 24 (7), pp. 1731–1737.
partitioning to acquire cadmium tolerance in rice?, Journal Lee, M. & Yang, M. (2010). Rhizofiltration using sunflower
of Plant Physiology, 166, pp. 20–31. (Helianthus annuus L.) and bean (Phaseolus vulgaris L. var.
Gupta, D.K., Tohoyama, H., Joho, M. & Inouhe, M. (200) Possible vulgaris) to remediate uranium contaminated groundwater,
roles of phytochelatins and glutathione metabolism in Journal of Hazardous Materials, 173, pp. 589–596.
cadmium tolerance in chickpea roots, Journal of Plant Liu, A., Hamel, C., Hamilton, R.I., Ma, .B.L. & Smith, D.L. (2000).
Research, 115, pp. 429–437. Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize
Hall, A.G. (1999a). Glutathione and the regulation of cell death, (Zea mays L.) grown in soil at different P and micronutrient
Advances in Experimental Medicine and Biology, 457, levels, Mycorrhiza, 9 (6), pp. 331–336.
pp. 199–203. Maciak, F. (2003). The protection and restoration of the environment,
Hall, A.G. (1999b). The role of glutathione in the regulation of SGGW Ed., Warsaw 2003. (in Polish)
apoptosis, European Journal of Clinical Investigation, 29, Maitani, T., Kubota, H., Sato, K. & Yamata, T. (1999). Phytochelatins
pp. 238–245. (class III metallothioneins) and their desglycyl peptides
Hall, J.L. (2002). Cellular mechanisms for heavy metal detoxification induced by cadmium in root cultures of Rubia tinctorum L.
and tolerance, Journal of Experimental Botany, 53, pp. 1–11. Advances in Life Sciences, Metalothionein, 4, pp. 201–205.
Unauthenticated
Download Date | 2/19/16 2:12 PM
 Mechanisms of stress avoidance and tolerance by plants used in phytoremediation of heavy metals 113

Małachowska-Jutsz, A. (2008). Plant mycorrhization effectiveness Olko, A. (2009). Physiological aspects of plant tolerance to heavy
of phytoremediation of soil polluted with hydrocarbons, metals, Kosmos, 58 (1–2), pp. 221–228. (in Polish)
Zeszyty Naukowe Politechniki Śląskiej, 1782. (in Polish) Padmavathiamma, P.K. & Li, L.Y. (2007). Phytoremediation
Małachowska-Jutsz, A., Kalka, J., Baczyński, T. (2010). Influence of Technology, Hyper-accumulation metals in plants, Water,
mycorrhizal fungi on remediation of soil contaminated by Air, & Soil Pollution, 184, pp. 105–126.
petroleum hydrocarbons, Fresenius Environmental Bulletin, Pastore, A., Federici, G., Bertini, E. & Piemonte, F. (2003) Analysis of
19(12b), pp. 1–7. glutatione: implication in redox and detoxification, Clinica
Małachowska-Jutsz, A., Rudek, J., Janosz, W. (2011). The effect of Chimica Acta, 333, pp. 19–39.
ribwort (Plantago lanceolata) and its myrorrhizas on the Pierzynski, G.M., Schnoor, J.L., Youngman, A., Licht, L. &
growth of microflora in soil contaminated with used engine Erickson, L.E. (2002a). Poplar trees for phytostabilization
oil, Archives of Environmental Protection, 37(1), pp. 99–113. of abandoned zinc-lead smelter, Practice Periodical of
Martin, H.W. & Kaplan, D.I. (1998). Temporal changes in cadmium, Hazardous, Toxic, and Radioactive Waste Management,
thallium, and vanadium mobility in soil and phytoavailability 6(3), pp. 177–183.
under field conditions, Water, Air, & Soil Pollution, 101, Pierzynski, G.M., Lambert, M., Hetrick, B.A.D., Sweeney, D.W.
pp. 399–410. & Erickson, L.E. (2002b). Phytostabilization of metal
McGrath, S.P., Zhao, F.J. & Lombi, E. (2001). Plant and rhizosphere mine mailings using Tall Fescue, Practice Periodical of
processes involved in phytoremediation of metal- Hazardous, Toxic, and Radioactive Waste Management,
contaminated soils, Plant Soil, 232 (1–2), pp. 207–214. 6(4), pp. 212–217.
Meier, S., Alvear, M., Borie, F., Aguilera, P., Ginocchio, R. & Cornejo, Poot, M., Teubert, H., Rabinovitch, P.S. & Kavanagh, T.J. (1995) De
P. (2012). Influence of copper on root exudate patterns in novo synthesis of glutathione is required for both entry into
some metallophytes and agricultural plants, Ecotoxicology and progression through the cell cycle, Journal of Cellular
and Environmental Safety, 75, pp. 8–15. Physiology, 163, pp. 555–560.
Meister, A. & Anderson, M.E. (1983). Glutathione, Annual Review of Rauser, W.E. (2000). Roots of maize seedlings retain most of
Biochemistry, 52, pp. 711–760. their cadmium through two complexes, Journal of Plant
Meister, A. (1995). Glutathione metabolism, Methods in Enzymology, Physiology, 156, pp. 545–551.
251, pp. 3–13. Reeves, R.D. & Brooks, R.R. (1983). Hyperaccumulation of lead and
Mendoza-Cozatl, D.G., Moreno-Sanchez, R. (2006). Control of zinc by two metallophytes from a mining area of Central
glutathione and phytochelatin synthesis under cadmium Europe, Environmental Pollution Series A, 31, pp. 277–287.
stress. Pathway modeling for plants, Journal of Theoretical Robinson, N.J., Tommey, A.M., Kuske, C. & Jackson, P.J. (1993).
Biology, 238, pp. 919–936. Plant metallothioneins, Biochemical Journal, 295, pp. 1–10.
Milner, M.J. & Kochian, L.V. (2008). Investigating heavy-metal Rock, S. (2003), Field evaluations of phytotechnologies. In:
hyperaccumulation Thaspi caerulescens as model system, McCutcheon SC, Schnoor JL, Phytoremediation:
Annals of Botany, 102, pp. 3–13. Transformation and Control of Contaminants. John Wiley
Miransari, M. (2011). Hyperaccumulators, arbuscular mycorrhizal and Sons, Inc., New Jersey 2003.
fungi and stress of heavy metals, Biotechnology Advances, Roosens, N.H.C.J., Willems, G. & Saumitou-Laprade, P. (2008). Using
29, pp. 645–653. Arabidopsis to explore zinc tolerance and hyperaccumulation,
Morris, C.A., Nicolaus, B., Sampson, V., Harwood, J.L. & Kille, P. Trends in Plant Science, 13, pp. 208–215.
(1999). Identification and characterization of a recombinant Singla-Pareek, S.L., Yadav, S.K., Pareek, A., Reddy, M.K. & Sopory,
metallothionein protein from a marine alga Fucus S.K. (2006). Transgenic tobacco overexpressing glyoxalase
vesiculosus, Biochemical Journal, 338, pp. 553–560. pathway enzymes grow and set viable seeds in zinc-spiked
MSE Technology Applications, Inc. (2001). Interim report for the soils, Plant Physiology, 140, pp. 613–623.
revegetation of mining waste using organic amendments Siwek, M. (2008a). Plants in industrial environment contaminated
and the potential for creating attractive nuisances for with heavy metals. Part II. Mechanisms of detoxication and
wildlife demonstration project. MWTP Activity III, Project adaptation strategies to high concentrations of heavy metals
23 Report prepared by MSE for the U.S. EPA’s National , Wiadomości Botaniczne, 52 (3/4), pp. 7–23. (in Polish)
Risk Management Laboratory (NRMRL), Cincinnati, OH Siwek, M. (2008b). Plants in industrial environment contaminated
and U.S. DOE: National Energy Technology Laboratory with heavy metals. Part I. Uptake, transport and toxicity
(NETL), Pittsburgh, PA as document number MWTP-189, of trace heavy metals, Wiadomości Botaniczne, 52 (1/2),
July 2001. pp. 7–22. (in Polish)
MSE Technology Applications, Inc (2004) Final Report for the de Souza, M.P., Chu, D., Zhao, M., Zayed, A.M., Ruzin, S.E.,
revegetation of mining waste using organic amendments Schichnes, D. & Terry, N. (1999). Rhizosphere bacteria
and the potential for creating attractive nuisances for enhance selenium accumulation and volatilization by Indian
wildlife demonstration project. MWTP Activity III, Project mustard, Plant Physiology, 119 (2), pp. 565–573.
23 Report prepared by MSE for the U.S. EPA’s National Tam, P.C.F. (1995). Heavy metal tolerance by ectomycorrhyzal fungi
Risk Management Laboratory (NRMRL), Cincinnati, OH and metal amelioration by Pisolithus tinctorium, Mycorrhiza,
and U.S. DOE: National Energy Technology Laboratory 5 (3), pp. 181–187.
(NETL), Pittsburgh, PA as document number MWTP-239, Tomović, G.M., Nevena Lj. Mihailović, N.Lj., Tumi, A.F., Gajić, B.,
March 2004. Mišljenović T.D., Niketić, M.S. (2013). Trace metals in soils
Murphy, A. & Taiz, L. (1995). Comparison of metallothionein gene and several Brassicaceae plant Species from serpentine sites
expression and non-protein thiols in 10 Arabidopsis ecotypes of Serbia, Archives of Environmental Protection, 39(4), pp.
correlation with copper tolerance, Plant Physiology, 109, 29–49.
pp. 1–10. Turnau, K., Jurkiewicz, A. & Grzybowska, B. (2002). The role of
Murphy, A., Zhou, J., Goldsbrough, P.B. & Taiz, L. (1997). Purification miccorhizae in bioremediation of contaminated areas,
and immunological identification of metallothioneins 1 Kosmos, 51 (2), pp. 185–194. (in Polish)
and 2 from Arabidopsis thaliana, Plant Physiology, 113, Turnau, K. & Mesjasz-Przybyłowicz, J. (2003). Arbuscular
pp. 1293–1301. mycorrhizal fungi diversity in the rhizosphere of Viola
Unauthenticated
Download Date | 2/19/16 2:12 PM
114 A. Małachowska Jutsz, A. Gnida

calaminaria and effect of these fungi on heavy metal uptake phytoremediation, Journal of Trace Elements in Medicine
by clover, Mycorrhiza, 10, pp. 161–168. and Biology, 18 (4), pp. 339–353.
US EPA (2001). Phytoextraction of lead in soils at Magic Marker and Yoon, J., Cao, X. & Zhou, O. (2006). Accumulation of Pb, Cu, and Zn
Ft. Dix. Innovative Technology Evaluation Report, US EPA. in native plants growing on a contaminated, Science of the
National Risk Management Research Laboratory, Cincinatti Total Environment, 368, pp. 456–464.
2001. Zayed, A.M., Lytle, C.M. & Terry, N. (1998). Accumulation and
Verma, P., George, K.V., Singh, H.V., Singh, S.K., Juwarkar, A. volatilization of different chemical species of selenium by
& Singh, R.N. (2006). Modeling rhizofiltration: heavy- plants, Planta, 206 (2), pp. 284–292.
-metal uptake by plant roots, Environmental Modeling & Zenk, M.H. (1996). Heavy metal detoxification in higher plants
Assessment, 11, pp. 387–394. – a review, Gene, 179, pp. 21–30.
Wang, J., Zhao, F., Meharg, A.A., Raab, A., Feldmann, J. & McGrath, Zhou, G.K., Xu, Y.F. & Liu, J.Y. (2005). Characterization of a rice
P.S. (2002). Mechanisms of arsenic hyperaccumulation class II metallothionein gene: tissue expression patterns and
in Pteris vittata. Uptake kinetics, interactions with induction in response to abiotic factors, Science of the Total
phosphate, and arsenic speciation, Plant Physiology, 130, Environment, 162, pp. 686–696.
pp. 1552–1561. Zhu, Y.L., Pilon-Smits, E.A.H., Jouanin, L. & Terry, N. (1999a).
Wong, M.H. & Bradshaw, A.D. (2002). The restoration and Over expression of glutathione synthetase in Indian mustard
management of derelict land. Modern approaches, World enhances cadmium accumulation and tolerance, Plant
Scientific Publishing, Singapore, Japan 2002. Physiology, 119, pp. 73–79.
Wójcik, A. & Tukiendorf, A. (1995). Strategy of stress avoidance in Zhu, Y.L., Pilon-Smits, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L.
resistance of plants to heavy metals, Wiadomości Botaniczne, & Terry, N. (1999b). Cadmium tolerance and accumulation
39 (3/4), pp. 33–40. (in Polish) in Indian mustard is enhanced by overexpressing
Woźny, A. & Przybył, K. (2004). Plant cells under stress conditions, – glutamylcysteine synthatase, Plant Physiology, 121, pp.
Wydawnictwo Naukowe PWN, Poland 2004. (in Polish) 1169–1177.
Yang, B., Shu, W., Ye, Z., Lan, C. & Wong, M. (2003). Growth and Zimeri, A.M., Dhankher, O.M., McCaig, B. & Meagher, R.B.
metal accumulation in vetiver and two Sesbania species on I (2005). The plant MT1 metallothioneins are stabilized
tailings, Chemosphere, 52, pp. 1593–1600. by binding cadmium and are required for cadmium
Yang, X., Feng, Y., He, Z. & Stoffella, P.J. (2005). Molecular tolerance and accumulation, Plant Molecular Biology, 58,
mechanisms of heavy metal hyper accumulation and pp. 839–855.

Mechanizmy unikania i tolerowania stresu przez rośliny używane w fitoremediacji

metali ciężkich

Streszczenie: Zanieczyszczenie gleb metalami ciężkimi jest poważnym problemem środowiska naturalnego, po-
nieważ ma negatywny wpływ m.in. na zdrowie ludzi i rolnictwo. Fitoremediacja może być alternatywną tech-
nologią oczyszczania środowiska, wykorzystującą naturalną zdolność roślin do pobierania, gromadzenia lub
przekształcania zanieczyszczeń. Dla zapewnienia prawidłowego wzrostu i rozwoju roślinom na terenach zanie-
czyszczonych (np. przez metale ciężkie) konieczne jest wykształcenie przez rośliny odpowiednich mechanizmów
ochronnych przed toksycznym działaniem tych zanieczyszczeń. W artykule przedstawiono przegląd najważniej-
szych fizjologicznych mechanizmów unikania stresu i tolerancji przez rośliny wykorzystywane w fitoremediacji
metali ciężkich.

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