PHOTOSYNTHETICA 46 (4): 481-489, 2008

481 

REVIEW 

Toxic metal ions in photoautotrophic organisms

T. KUČERA, H. HORÁKOVÁ, and A. ŠONSKÁ*

Department of Biochemistry, Faculty of Science, Charles University in Prague, 

Albertov 2030, 128 43 Prague, Czech Republic 

Abstract

We summarize the contemporary understanding of the effects of metal stress on various photosynthetic processes in 

photoautotrophic organisms and of the defence strategies employed by these organisms to avoid such stress. Cadmium is 

in the centre of interest of this review, as a non-essential element and important environmental pollutant, but Al, Pb, Hg, 

As, Cu, and Zn are also considered. Toxic metal ions pollute the environment through anthropogenic activities and affect 

the quality of plant crop. They represent one of the main abiotic stress factors influencing the health of plants and, as 

a secondary effect, of animals including man. The review summarizes the generally accepted answers to the questions: 

How do the toxic metal ions enter the photosynthetic organisms? How are they accumulated in plants? Which 

mechanisms do plants develop to tolerate metal stress and protect themselves? 

Additional key words: abiotic stress; Al; As; Cd; Cu; Hg; photosynthesis; phytoremediation; toxic metals; Zn.

Introduction

Metal ions are essential in low concentrations in the 

maintenance and development of all organisms. Many 

molecules and reactions in plants require essential 

elements. Macrobiogenic elements include magnesium 

for functional chlorophyll (Chl), activation of ATP-synthase, synthesis of nucleic acids and proteins, and 

activation of enzymes such as ribulose-1,5-bisphosphate 

carboxylase/oxygenase (RuBPCO), iron for electron 

transporters or catalysis of Chl biosynthesis, and calcium 

for signalling pathways or photoactivation of photosystem 2 (PS2). Microbiogenic elements involve manganese (e.g. for oxygen evolving complex, OEC), copper 

(e.g. for plastocyanin), and cobalt (e.g. for vitamin B12)

(Bertrand and Poirier 2005). Zinc and copper are also 

required as cofactors by many key enzymes involved 

in metabolic pathways [superoxide dismutase (SOD), 

δ-aminolevulinic acid (ALA) dehydratase]. Zinc plays a 

significant structural role as a stabilizer of some proteins, 

e.g. DNA-binding proteins in structural motives of Znfingers (Aravind and Prasad 2004). When essential ions 

are not available, plants develop specific deficiency 

symptoms. Absence of iron causes a decrease in the 

photosynthetic rate, chlorosis of leaves, and their 

abscission. 

However, metals present in excessive amounts may 

interfere with the usual cellular metabolism and become 

toxic. Uncontrolled binding of metals can result in 

inactivation of proteins (Clemens et al. 2002). Excess 

metals reach plants as a result of environmental pollution 

due to mining, smelting, manufacturing, agricultural and 

waste disposal technologies, and military practices 

(Bertrand and Poirier 2005). Such metals are released in 

the biosphere through air, water, and soil, taken up by 

root systems or leaves, or absorbed by the whole surface 

of unicellular organisms. They accumulate in various 

parts of plants and migrate along the food chain into 

animal and human tissues. The most toxic to higher 

plants and microorganisms even at low concentrations are 

the non-essential metal ions such as Cd2+, Hg+,2+, As3+,5+, 

AsO3

3–, AsO43–, Pb2+,4+, Ag+

, Al3+, Cr6+, Se4+, SeO4

2–, 

——— 

Received 13 August 2008, accepted 8 October 2008. *

Corresponding author; fax: +420 221 951 283, e-mail: alalice@natur.cuni.cz 

Dedicated to Prof. Dr. Danuše Sofrová.

Abbreviations: AA – ascorbate; ALA – δ-aminolevulinic acid; AP – ascorbate peroxidase; Asc-GSH cycle – ascorbate-glutathione 

cycle; Car – carotenoids; CAT – catalase; CDF – cation diffusion facilitators; Chl – chlorophyll; DHA – dehydroascorbate; DHAR – 

dehydroascorbate reductase; Fd – ferredoxin; GR – glutathione reductase; GSH – reduced glutathione; GSSG – oxidized glutathione; 

JA – jasmonic acid; LHC2 – light-harvesting complex of photosystem 2; MDHA – monodehydroascorbate radical; MDHAR – 

monodehydroascorbate reductase; MT – metallothionein; Nramp – natural resistance associated macrophage proteins; OEC – oxygen 

evolving complex; PC – phytochelatin; PEPC – phosphoenolpyruvate carboxylase; PS – photosystem; ROS – reactive oxygen 

species; RuBPCO – ribulose-1,5-bisphosphate carboxylase/oxygenase; SOD – superoxide dismutase; YCF1 – yeast cadmium factor.
T. KUČERA et al.

482 

SeO3

2–, and Sn4+. Essential elements Cu2+, Zn2+, Co2+ are 

toxic at high concentrations only (Kučera and Sofrová 

2004). The most common overall toxicity sequence of 

elements decreases in order Hg2+>Cu2+>Cd2+>Ag+

> 

Pb2+>Zn2+ (Backor and Vaczi 2002). In particular cases, 

the relative effects of some of them may be reversed. Zn 

was more toxic than Cu to Scenedesmus acutus having 

different sensitivity to Cr (Abd-El-Monem et al. 1998). 

Coordinate function of uptake, transport, distribution, and 

regulation of cytosolic concentrations of essential metals 

in various tissues and compartments within the narrow 

physiological limits is clearly important to normal plant 

growth and development. However, organisms have to 

cope with exposure to unwanted elements, because of 

imperfect control of accumulation. A lack of specificity 

of uptake and distribution systems leads to the accumulation of toxic metal ions (Clemens et al. 2002). 

Metal uptake 

Metals penetrate into unicellular organisms through the 

whole surface of the cell. In higher plants and lichens the 

main contact surface of the organisms is constituted by 

the root and rhizine systems (Wisniewski and Dickinson 

2003). The uptake of metal ions comprises two phases. 

The first phase consists of a rapid and non-specific 

binding of the cations to negatively charged cell wall 

components (sugar residues) located at the cell surface 

(Prasad 1995) and mobilization of the soil-bound metals 

by secretion of organic acids (malate, citrate) (Clemens et 

al. 2002). The potential mobilization of metals in soil 

depends primarily on metal content, its solubility in 

water, soil pH, redox potential, and other soil characteristics (Bertrand and Poirier 2005). The actual bioavailability of some metals is limited because of low solubility 

in water and strong binding to soil particles. Iron, the 

most extreme example, is mainly present as Fe3+, which 

forms insoluble hydroxides. With the notable exception 

of Fe, which is solubilised by either reduction to Fe2+ by 

ferric chelate reductase or secretion of Fe3+ chelators, 

little is known about active mobilization of trace elements 

by plant roots (Clemens et al. 2002). 

The second phase consists of energy-dependent 

intracellular uptake of the metal ions across the plasma 

membrane mediated by transport systems and intracellular high-affinity binding sites (Prasad 1995). The 

membrane potential in root epidermal cells, that is 

negative on the inside of the plasma membrane, provides 

a strong driving force for the uptake of cations through 

transporters (Clemens et al. 2002). Most of metals enter 

the cell as cations (e.g. Zn2+), whereas others cross the 

plasma membrane as anionic groups (e.g. AsO4

3–) or are 

included in small organic compounds (e.g. CH3Hg+

) 

(Mendoza-Cozatl and Moreno-Sanchez 2005). The 

metals are taken up as hydrated ions and in metal-chelate 

complexes (Clemens et al. 2002). Uptake of metal ions 

takes place through channel proteins and/or H+

-coupled 

carrier proteins. At the protein level, five families have 

been implicated in heavy metal transport: 

(1) C P x - t y p e A T P a s e s , a subgroup of P-type 

ATPases, pump essential and non-essential metals such 

as Cu2+, Zn2+, Cd2+, and Pb2+ across the plasma 

membrane. 

(2) C a t i o n / H + antiporters – physiologically 

exchange Na+

 or H+ with Ca2+ or Cd2+. 

(3) N r a m p f a m i l y (natural resistance associated 

macrophage proteins) – H+

-coupled transporters involved 

in the transport of Cd2+, Mn2+, and Cu2+. 

(4) C D F f a m i l y (cation diffusion facilitators) – 

involved in Zn2+, Co2+, Mn2+, and Cd2+ transport in 

bacteria, fungi, plants, and animals. 

(5) Z I P f a m i l y – plant transporters of Fe2+, Mn2+, 

Cd2+, and Zn2+ with biochemical properties similar to 

CDF but with different topology and highly conserved 

histidine motif for metal binding. 

Most of the transporters thought to be involved in the 

uptake of micronutrients are in the ZIP and the Nramp 

family. CDF and ZIP proteins have also been implicated 

in the intracellular transport of heavy metals to the 

vacuole (Mendoza-Cozatl and Moreno-Sanchez 2005). 

For more information about CPx-type ATPases, Nramp, 

and CDF family see review of Williams et al. (2000). 

The amounts of metal absorbed by a plant depend on 

the concentration and chemical form of the metal in the 

soil, metal mobilization, and efficiency of uptake from 

the soil to the root, sequestration within the root, efficiency of xylem loading and transport from the root to the 

shoot, sequestration and storage in leaf cells, and the 

presence of other ions in the environment. In the case of 

strongly adsorbed ions, absorption depends more upon 

the amount of roots produced. In general, effects are more 

pronounced at higher concentrations and at longer 

duration of exposure. Once absorbed, the metal can be 

either stored in the root or exported to other organs. In 

soybean, about 98 % of the accumulated Cd is strongly 

retained by roots, and only 2 % is transported to the shoot 

system (Prasad 1995). The xylem is important for metal 

distribution through the whole plant. The metal 

transporters involved in xylem loading and distribution 

between leaf cells have yet to be identified (Clemens 

et al. 2002). 

The penetration from air to the aerial parts of plant 

body, particularly leaves, represents a substantial part of 

the uptake for some toxic metals. The absorption of 

organic and inorganic mercury from soil by plants is low. 

Hg emitted to the atmosphere thus seems to contribute 

significantly to the Hg content in crops (Patra et al.

2004). Hg-containing pesticide spray residues are absorbed by plant leaves and migrate to humus through 

fallen leaves, where they are taken up by plants and 
TOXIC METAL IONS IN PHOTOAUTOTROPHIC ORGANISMS

483 

translocated to edible portions. However, the removal of 

Hg2+ from organic Hg compounds catalysed by organomercurial lyase and reduction of Hg2+ to the elemental 

form Hg0 by mercuric ion reductase using NADPH as an 

electron donor results in transport through the leaves and 

volatilization (Prasad 1995). 

The main exposure to lead takes place through the air, 

too (Graeme and Pollack 1998). Pb gets deposited on the 

leaves and other exposed surfaces of plants. Plant roots 

are able to extract some of this metal from soil but 

translocation to aerial part is generally limited. The roots 

may accumulate higher amount of the metal than the 

shoot and leaves (Singh et al. 1997). 

Heavy metal tolerance in plants

Plants growing on metal-contaminated sites need to 

develop some degree of tolerance to metal toxicity in 

order to survive. Metal tolerance and homeostasis in cells 

is achieved by controlling transport processes (Meharg 

2005) and by metal compartmentation with specific 

metal-binding biomolecules such as phytochelatins (PCs) 

and metallothioneins (MTs) (Clemens et al. 2002, Hall 

2002). The common mechanisms for metal tolerance 

proposed are: 

(1) M e t a l i m m o b i l i z a t i o n – the most common 

mechanism of plant adaptation by which a plant is 

protected externally from the influence of the stress is 

avoidance of metal stress by metal exclusion, e.g. deposition in cell wall components by extracellularly secreted 

organic compounds (polysaccharides, amino acids, 

organic acids). 

(2) O r g a n i c l i g a n d e x u d a t i o n ( m o b i l i z a -

t i o n ) – secretion of organic acids (citrate, malate, oxalacetate), acidification of the rhizosphere, and reduction of 

some elements to enhance metal accumulation. 

(3) M e t a l i o n e f f l u x – joining metal uptake to 

achieve ionic balance, e.g. loss of K+

 (Prasad 1995). 

(4) C h e l a t i o n – phytochelatin and metallothionein 

synthesis. 

(5) C o m p a r t m e n t a t i o n ( s e q u e s t r a t i o n ) – 

involves transport of toxic ions into a vacuole. 

Ad (1): Formation of organo-copper complexes by the 

herb Silene vulgaris in the cell walls as well as in the 

medium near the cells acts as a barrier to Cu uptake and 

prevents Cu from affecting cell metabolism (Ernst et al.

2000). 

Ad (2): Most of Al occurs as harmless oxides and 

aluminosilicates. However, when soils become acidic as a 

result of natural processes or human activities, Al is 

solubilized into the toxic trivalent cation, Al3+. Al toxicity 

is a major limiting factor of plant productivity on acidic 

soils, which now account for about 40 % of the Earth’s 

arable land. Transgenic tobacco plants, that express 

bacterial citrate synthase, show elevated citrate secretion, 

which results in protection of plant roots from Al toxicity 

(de la Fuente et al. 1997, López-Bucio et al. 2000). Pellet 

et al. (1996) demonstrated in Al-sensitive and Al-resistant wheat cultivars differing in malate and phosphate 

exudation from root apices, that these features both 

confer the Al resistance and that the malate exudation is 

triggered by Al3+. There may be a specific transporter for 

the organic acid anions in the plasma membrane, 

probably an anion channel (Ryan et al. 1997, Kollmeier 

et al. 2001, Piñeros and Kochian 2001, Zhang et al. 

2001). Al3+ activates an anion channel in the plasma 

membrane that is permeable to malate and chloride. It is 

not known how Al activates these anion channels but 

three possibilities have been proposed: (a) Al interacts 

directly with the channel protein to trigger its opening. 

(b) Al interacts with a specific receptor on the membrane 

surface or with the membrane itself to initiate a 

secondary-messenger cascade which then activates the 

channel. (c). Al enters the cytoplasm and activates the 

channel either directly or indirectly via secondary 

messengers (Ma et al. 2001). 

Ad (4): Inside cells, polypeptides such as MTs and 

PCs participate in excess metal storage and detoxification 

together with organic molecules of low molecular mass, 

mainly organic acids, amino acids, and their derivatives. 

When these systems are overloaded, oxidative stress 

defence mechanisms are activated (Bertrand and Poirier 

2005). MTs are cysteine-rich, gene-encoded, 8–14 kDa 

polypeptides that sequester excess amounts of certain 

toxic ions via thiol groups and thus keep them from circulating in the cytosol. PCs [γ-glutamyl-cysteinyl glycine 

complexes (γGlu-Cys)nGly, n = 2–11, 1.5–4.0 kDa 

cytosolic peptides] are synthesized from glutathione 

(GSH) in the presence of phytochelatin synthase (γGluCys dipeptidyl transferase) in higher plants. PC synthase 

removes a γGlu-Cys residue from one molecule of GSH 

(γGlu-Cys-Gly) and couples it to another GSH. PC 

synthesis is induced by toxic metal ions and proceeds as 

long as the metal ions are available. The production of 

PCs and MTs is the principal mechanism of metal 

detoxification in higher plants, fungi, and apparently also 

in certain animals. The PC-metal complexes, less toxic to 

cellular plant metabolism than free metal ions, are 

transported to the vacuole. In Datura innoxia, 80 % of Cd 

is bound to low molecular mass PCs and about 15 % to 

high molecular mass MTs. About 60 % of Cu is bound to 

MTs and only about 25 % to PCs. These collective results 

suggest co-occurrence of MTs and PCs in plants. Sulphate salts afford protection to Cd toxicity by enhancing 

sulphate uptake, leading to increased synthesis of GSH 

(Prasad 1995). 

Ad (5): In plants and some yeasts, Cd2+ is 

accumulated in the vacuole. In plants, Cd2+ may be 

transported as free ion or as a PC-Cd complex. In yeast, 

Cd2+ is also transported as a free ion and, depending on 
T. KUČERA et al.

484 

the species, it may also be transported as a PC-Cd complex or as a bis(glutathionato)-Cd complex. The transport 

of free Cd2+ ion requires H+

 gradient across the vacuole 

membrane. The transport of thiol-metal complexes into 

vacuoles requires an ABC-type transporter specific for 

each kind of complex. Expression of the Saccharomyces 

cerevisiae protein YCF1 identified in yeast confers salt 

tolerance in Arabidopsis thaliana (Koh et al. 2006). 

Finally, for a complete Cd2+ inactivation and storage 

inside the vacuole, thiol-Cd complexes, Cd2+ and inorganic sulfide (S2−

) form high molecular mass complexes 

around a CdS core. Cells unable to form these complexes 

become Cd2+-sensitive. Euglena gracilis lacks a plantlike vacuole and thus more than 60 % of the accumulated 

Cd2+ is located inside the chloroplast. PCs are also 

present inside the chloroplast, suggesting that this organelle is involved in the Cd2+ resistance mechanism, but 

the origin of PCs and the mechanism by which Cd2+ is 

transported into the chloroplast are unknown (MendozaCozatl and Moreno-Sanchez 2005). 

Several of these mechanisms may be employed by 

a plant species against a particular metal, as in the case of 

arsenate in Holcus lanatus (Hartley-Whitaker et al. 

2001). The adaptive tolerance seems to be controlled by 

a limited number of genes (Macnair 1993). However, 

distinct metal-specific mechanisms are involved in the 

tolerance to individual metals (Hall 2002). 

Metal stress

When the metal excess reaches sub-lethal amounts, the 

production of free radicals (reactive oxygen species, 

ROS) that are triggered by toxic metals leads to the 

oxidative stress. Molecules are destroyed and metabolism 

is highly disturbed (Bertrand and Poirier 2005). 

Excessive concentrations of metals result in phytotoxicity 

through: (1) reactions of sulfhydryl groups and nitrogenrich ligands with cations; (2) affinity for reacting with 

phosphate groups of ADP or ATP; and (3) replacement 

and deficiency of essential metal ions (Mendoza-Cozatl 

and Moreno-Sanchez 2005). The consequences of 

Cannabis sativa exposed to Cd are inhibition of Chl 

synthesis (chlorosis), decrease in Chl content and Chl a/b

ratio, inhibition or decreased activity of enzymes, high 

ATP content, lipid peroxidation, increase in plasma 

membrane permeability, imbalance in ionic transport and 

homeostasis, loss of turgor, altered stomatal action, and 

DNA damage. Metal interference with chloroplast 

replication and cell division causes the reduction in the 

number of chloroplasts per cell (chlorosis) and a change 

in cell size. The disorganized thylakoids impair the 

photosynthetic efficiency: the cells and therefore whole 

photosynthetic organisms grow slowly (Linger et al.

2005). In bean plants exposed to Cd, leaf cell growth and 

relative water content of leaves decreased by about 10 % 

compared to the control (Prasad 1995). 

Effects on pigments: A low Chl content (chlorosis) can 

signalize Fe deficiency or an inhibition of Chl synthesis 

by the toxic metal. Cd inhibits Chl synthesis through 

ALA dehydratase and protochlorophyllide reductase by 

its interference with the sulfhydryl site leading to the 

lower production of porphobilinogen. Metals such as Cd, 

Cu, Hg, Ni, Pb, or Zn can replace Mg within Chl leading 

consequently to a breakdown in photosynthesis (Bertrand 

and Poirier 2005). According to Prasad (1995), Cd 

primarily affected the photosynthetic pigments in higher 

plants: total Chl content and the Chl a/b ratio decreased, 

but carotenoids (Car) were less affected than Chl resulting in a lower Chl/Car ratio. In another study, the 

Chl a/b ratio increased suggesting that Cu affected the 

light-harvesting complex 2 (LHC2) where Chl b is located, rather than the Chl a containing reaction centres. 

This contradicts other studies where the reverse has been 

found. The effects of Cd and Zn on chlorosis also depend 

on leaf age (Ebbs and Uchil 2008); sensitivity of genotype to the toxic metal is also very important (He et al. 

2008, Mihailovic et al. 2008). The small increase in 

β-carotene content in Quercus robur exposed to Cu may 

be due to its resistance to degradation, since it is a 

relatively stable pigment with a protective role. The 

activity of xanthophyll cycle (particularly zeaxanthin), 

implicated as a mechanism that protects the photosynthetic apparatus by the non-photochemical quenching 

of excited triplet Chl, evidently declines (Wisniewski and 

Dickinson 2003). A reduction of xanthophyll cycle pigments of nearly 50 % was observed in rape leaves, 

supporting an unfortunate effect of Cd on zeaxanthin 

synthesis causing changes in the quenching properties. In 

addition, tomato and soybean plants also undergo 

a reduction of Car contents when treated with Cd (Linger 

et al. 2005). This is in contradiction with another study, 

where an increase of the zeaxanthin content was found, 

higher than could be accounted for by the light-induced 

de-epoxidation of violaxanthin (Mendez-Alvarez et al.

1999). According to Mendez-Alvarez et al. (1999), 

hydroxylation of β-carotene into zeaxanthin under high 

irradiance could be an additional source for zeaxanthin 

that might be involved in non-photochemical quenching. 

Metal ions block the electron flow in PS2 leading to 

the formation of excited triplet Chl (3

Chl*), whose life 

time is long enough to react with a molecule of oxygen 

with triplet electronic configuration. During the interaction, Chl gets over to the ground state and oxygen in 

turn is changed into highly reactive singlet oxygen. 

Oxidative stress leads to an imbalance in the regeneration 

and removal of ROS including singlet oxygen (1

O2), 

superoxide radical (O2−

), hydrogen peroxide (H2O2), and 

the most damaging and reactive hydroxyl radical (OH.

). 

These reactive molecules are, in the absence of protective 
TOXIC METAL IONS IN PHOTOAUTOTROPHIC ORGANISMS

485 

mechanisms, capable of damaging membranes, proteins, 

and nucleic acids leading to altered membrane fluidity, 

loss of enzyme function, and genomic damage. Thiobarbituric acid reactive substances, the cytotoxic products 

of lipid peroxidation, are normally the major compounds 

that indicate the magnitude of oxidative stress. Susceptibility to oxidative stress depends on the overall 

balance between the factors that increase oxidant 

generation and the cellular components that exhibit an 

antioxidant capability (Cho and Seo 2005).

The synchronous action of GSH reductase (GR), 

ascorbate peroxidase (APX), superoxide dismutase 

(SOD), and catalase (CAT) is part of the antioxidative 

system that protects various compartments in the cell 

against ROS. The CAT, localized in peroxisomes and 

chloroplasts, converts the most stable of all ROS H2O2

into H2O and O2. Peroxidase decomposes H2O2 by 

oxidation of co-substrates such as phenolic compounds 

and/or antioxidants in vacuoles, cell walls, and cytosol. 

Increase in peroxidase activity is generally considered as 

an indication of plant ageing and might initiate 

senescence. SOD is a metalloprotein with Zn that 

catalyzes the dismutation of superoxide to less dangerous 

H2O2 and O2 in the cytosol, mitochondria, and chloroplasts (Cho and Seo 2005). 

The ascorbate-glutathione cycle (Asc-GSH cycle) is 

essential in removing ROS and maintaining the cellular 

homeostasis by keeping the reduced forms of GSH and 

ascorbate in cells on a suitable level and thus to adjust a 

cellular redox potential. It is localized in various 

subcellular compartments including the chloroplast, 

mitochondrion, peroxisome, glyoxisome, and the plasma 

membrane. The activities of ascorbate peroxidase (AP) 

and GR are crucial in the operation of Asc-GSH cycle. 

APX reduces H2O2 into H2O using ascorbate (AA) as the 

electron donor, resulting in the formation of monodehydroascorbate radical (MDHA). Monodehydroascorbate 

reductase (MDHAR) reduces MDHA into AA using 

NAD(P)H as electron donor. Under limiting supply of 

NAD(P)H, MDHAs are dismutated into AA and dehydroascorbate (DHA). Dehydroascorbate reductase (DHAR) 

using GSH as an electron donor generates AA from 

DHA. Oxidized GSH (GSSG) is converted to GSH by 

NAD(P)H-dependent GR (Drazkiewicz et al. 2003, 

Gorinova et al. 2007). 

AA takes part in growth processes, electron transport, 

photoprotection, regulation of photosynthesis, and 

preservation of the enzyme activities that contain 

prosthetic transition metal ions. It is also active in regeneration of the lipophilic antioxidant α-tocopherol and in 

antioxidant processes by reacting directly with ROS. 

GSH is used in the detoxification of xenobiotics and in 

PC synthesis. It affects also expression of defence genes 

and is associated with stress resistance. As a component 

of the Asc-GSH cycle, GSH is involved in the control of 

H2O2 concentration in plant cells. GSH reacts also nonenzymatically with singlet oxygen, superoxide and 

hydroxyl radicals (Drazkiewicz et al. 2003). Car quench 

the oxidizing species and triplet state of Chl. The decreased Car content in Cd-treated freshwater macrophyte 

Ceratophyllum demersum and thus an increase in the 

membrane damage due to the loss of ROS scavenging 

function has been observed by Aravind and Prasad 

(2004). In the same plant, at high Pb concentrations the 

enhanced PC synthesis may result in decrease of GSH 

content and the consequent oxidative stress (Mishra et al.

2006). 

Nagalakshmi and Prasad (2001) observed with 

increasing concentrations of Cu progressive depletion of 

GSH content in the cells of Scenedesmus bijugatus. Cu 

stress increased the activities of PC synthase, APX, and 

decreased the activity of GR. This suggests that Cu alters 

the equilibrium between synthesis and utilization of GSH 

either due to its antioxidant role or by serving as a 

precursor in the synthesis of PCs. The increase in the 

activities of enzymes of GSH metabolism and the 

activities of antioxidant enzymes suggests that Asc-GSH 

cycle has a pivotal role in Cu detoxification, apart from 

the role of PCs in the chelation of metals. In another 

experiment, A. thaliana exposed to Cu stress for a day 

showed elevated DHAR activity accompanied by the 

decrease of GSH level to counteract DHA accumulation. 

In plants exposed to the metal for three days, GR and 

MDHAR were especially active to maintain large pool of 

GSH and AA. However, at seven-day exposition, a 

suitable level of AA was maintained due to enhanced 

activity of MDHAR or DHAR depending on Cu 

concentration. Increase of AP and DHAR activities was 

observed at 5 μM Cu and increase of MDHAR activity 

occurred at 25 μM Cu. Moreover, decrease of AP activity 

at 50 μM Cu, but increase of MDHAR and decrease of 

DHAR activity under exposition to 100 μM Cu were 

characteristic of plants treated with the metal for seven 

days (Drazkiewicz et al. 2003). According to Cho and 

Seo (2005), H2O2 accumulation is the major reason 

causing Cd phytotoxicity in A. thaliana seedlings. It can 

result from inefficient quenching by the altered antioxidant enzymes, particularly those involved in the AscGSH pathway and lowered CAT activity. Cd-resistant 

plants respond to an increased ROS production by 

increasing the synthesis of antioxidant enzymes (SOD, 

APX, GR) and GSH that can partly counteract the 

accumulation of H2O2. The Asc-GSH cycle might be 

operating at higher rate in order to detoxify the ROS in 

these cultivars, or it is essential to maintain reduced GSH 

pool at higher levels so that it does not become limiting 

for the synthesis of PCs. These results are in agreement 

with studies of responses of Nicotiana tabacum with 

injected MT gene to elevated Cd, where the increased 

SOD and AP activities and the enlarged AA pool 

indicated a mobilization of the Asc-GSH cycle. The 

control plants showed the inhibition of photosynthesis 

due to the decreased CAT activity (Gorinova et al. 2007). 

In another experiment, different Brassica juncea cultivars 
T. KUČERA et al.

486 

were exposed to various concentrations of Cd and the 

changes in the rate of lipid peroxidation, Cd accumulation, and activities of CAT, SOD, AP, and GR along 

with AA and GSH contents were studied. In all the 

cultivars, a reduction in the CAT activity and AA content 

was noted. The cultivar with the least increase in the lipid 

peroxidation rate, the highest Cd and GSH contents, and 

increased activities of SOD, AP, and GR possessed better 

Cd-sequestering and antioxidant system. High increase in 

the content of GSH suggests its possible incorporation in 

the synthesis of PCs and MTs to sequester Cd (Qadir et 

al. 2004). According to Maksymiec et al. (2007), heavy 

metals may act either directly on oxidative processes or 

through induction of the signalling pathways. Jasmonic 

acid (JA) is formed from lipid peroxides as a consequence of enhanced lipoxygenase activity, but the 

formation may also be a prolonged consequence of heavy 

metal induction of oxidative stress. JA can enhance the 

inhibitory effects on A. thaliana by Cu and Cd stress. 

High concentrations of antioxidative enzymes, together 

with enhanced pigment synthesis may allow a plant to 

overcome completely the harmful action of a toxic metal 

and to show normal healthy growth, as shown for spinach 

and chromium. However, the plant still accumulates 

fairly high amounts of the metal, a feature that can be 

useful for phytoremediation but dangerous in case of 

edible plants (Sinha et al. 2007). 

Effects on light reactions: Metal stress impairs electron 

transport activity by inducing peroxidation and loss of 

thylakoid membrane integrity. The disorganization of the 

chloroplast structure and the substitution of Mn by Zn or 

Cd leads to the inactivation of OEC and as a consequence 

electron donation to PS2 is inhibited. Induced changes in 

the arrangement and structure of LHC2 decrease the 

efficiency of excitation energy capture by PS2 and reduce 

the rate of photosynthetic oxygen evolution. Photophosphorylation rates decrease due to PS2 dysfunction 

without evidence for a direct inhibition by the metal of 

the ATP-synthase (Bertrand and Poirier 2005). Cd affects 

the lipid structure around LHC2 in C. demersum leading 

to the loss of major fatty acids and lipid peroxidation. 

This induces the release of several pigment-protein 

complexes, OEC, and plastocyanin. An impaired plastocyanin blocks further electron transport. This severe 

extent of peroxidative protein loss is ultimately responsible for the impaired photosynthetic process. Cd forms 

complexes with aromatic amino acid residues (tryptophan) of D1 protein, which are degraded by a protease 

leading to an impaired PS2 activity (Aravind and Prasad 

2004). These results are in agreement with another study 

(Kráľová et al. 2006) according to which Cd interacts 

with the tyrosine radicals, the primary donor of PS1, and 

with the Mn cluster in OEC. The interruption of the 

photosynthetic electron transport occurs due to these 

interactions. The formation of Cd2+ complexes with 

amino acid residues constituting photosynthetic polypeptides was suggested as possible mechanism of Cd 

inhibitory action. Faller and Krieger-Liszkay (2005) 

proved that Cd2+ is a competitive inhibitor of the Ca2+ site 

in the catalytic centre in PS2 during photoactivation 

inhibiting oxygen evolution in C. reinhardtii. This 

mechanism is a serious candidate for the involvement of 

Cd2+ toxicity in photosynthetic organisms in general, at 

least in unicellular ones, where Cd2+ has ready access to 

the chloroplast. Ca2+ can abolish the toxic effects of 

heavy metal ions, especially of Cd, in Kirchneriella 

lunaris (Issa et al. 1995). Cd may inhibit PS2 (Tůmová 

and Sofrová 2002, Nováková et al. 2004), possibly 

affecting OEC and photophosphorylation in spinach 

chloroplasts. PS1 is less affected (Tůmová and Sofrová 

2002). Cd-induced protein phosphorylation changes in 

rice and maize (Prasad 1995). Regulation of energy distribution of PS2 is affected in plants caused by structural 

alterations of PS2 and/or antenna complexes and impairment of the xanthophyll cycle (Linger et al. 2005). 

Effects on dark reactions: Inhibition of carbon 

metabolism due to Zn pollution has been reported in 

Datura innoxia. Increasing stomatal and mesophyll 

resistance leads to reduced CO2 uptake, because of a 

reduced number of stomata or stomata closing (Vaillant 

et al. 2005). Metals may oxidize sulfhydryl groups of 

proteins and modify the spatial conformation of enzymes, 

inhibiting enzyme activity or protein function, and 

lowering the pool of reducing antioxidant agents such as 

GSH. Metals may also react with nitrogen-rich ligands 

such as histidine. Metal-sensitive plant enzymes are 

RuBPCO, PEPC, alcohol dehydrogenase, glyceraldehyde-3-phosphate dehydrogenase, 3-phosphoglycerate 

kinase, and nitrate reductase. At moderate pollution, the 

enzymatic activities appear stimulated as part of defence 

mechanisms, while they seem inhibited at higher concentrations (Williams et al. 2000). Heavy metal treatment 

inhibits RuBPCO capacity in C3 plants and cyanobacteria 

(Nováková et al. 2004) and PEPC capacity in C4 plants. 

Furthermore, high Cd2+ concentrations can also lead to 

irreversible dissociation of small and large subunits of 

RuBPCO, with the consequence of total inhibition of the 

enzyme (Bertrand and Poirier 2005). Cu2+ and Cd2+ affect 

glyceraldehyde-3-phosphate dehydrogenase and 3-phosphoglycerate kinase at an early stage of stress development (Stiborová et al. 1986, Sheoran et al. 1990, 

Burzyński and Żurek 2007). 

Cd interference with other metal ions: When an essential metal is administered together with a harmful one of 

similar properties, the damages are less severe than with 

the toxic element alone (Ernst et al. 2000). Moderate Fe 

excess has a beneficial influence on Cd treated plants 

resulting in more intensive growth, accumulation of 

photosynthetic pigments, and more efficient light phase 

of photosynthesis. Nutrient-medium Fe deficiency results 

in increased uptake and accumulation of Cd. Strong Fe 
TOXIC METAL IONS IN PHOTOAUTOTROPHIC ORGANISMS

487 

excess, toxic itself, enhances Cd toxicity (Siedlecka and 

Krupa 1999). When toxic metals and beneficial elements 

enter the cell together, the beneficial part may be too 

weak because of competition. It happens actually for Fe 

that when Cd is given in excess to a growth medium, it 

causes Fe deficiency because both metals have partly 

common pathways.

However, in some cases the beneficial element is an 

antidote against the toxic element when it is given in 

excess (Bertrand and Poirier 2005). Zn protects chloroplasts and associated photochemical functions from Cd 

toxicity in C. demersum. Since both Cd and Zn belong to 

the same group of transition elements with similar 

electronic configuration and valency, they have similar 

geochemical and environmental properties. Zn antagonizes Cd toxicity by counteracting the inhibition of 

photosynthetic pigment synthesis by maintaining the 

contents of pigments. Zn probably maintains Chl 

synthesis through sulfhydryl group protection of enzymes 

from thiol oxidation and disulfide formation either by 

direct binding to a site close to the sulfhydryl group or by 

conformational change resulting in apparent stability of 

the enzymes. It maintains the contents of Car, but the 

mechanism has not been clarified yet. Zn has a stabilizing 

and protective effect on the biomembranes against oxidative and peroxidative damage by inducing active antioxidant enzyme system to control the destructive oxygen 

species. Zn replaces the toxic Cd, maintains the OEC 

integrity, prevents oxidative burst at antenna Chl 

molecules, and probably prevents binding of Cd to the 

major thylakoid proteins like D1 of the PS2 (Aravind and 

Prasad 2004). 

Phytoremediation

Phytoremediation is a method used to decontaminate and 

remediate the polluted environment by the plants capable 

of hyperaccumulating the toxic metal ions in their roots 

and shoots far more than in either soil or water which 

surrounds them (Masarovičová et al. 1999). In wealthy 

industrialized countries contamination is often highly 

localized, and the pressure to use contaminated land and 

water for agricultural food production or for human consumption is minimal. However, soil and water contamination is widespread in Eastern Europe, and is increasingly recognized as dramatic in large parts of the 

developing world, primarily in India and China (Prasad 

1995). Metal hyperaccumulating plants have been defined 

as plants that accumulate more than 10 000 mg kg−1

 Zn or 

Mn, 1 mg kg−1

 Co or Cu, and 100 mg kg−1 Cd. To date, 

only Thlaspi caerulescens and Arabidopsis halleri, both 

belonging to Brassicaceae, have been identified as Cdhyperaccumulators. More recently, Zn hyperaccumulator 

Sedum alfredii, which belongs to Crassulaceae, has been 

found in an old Zn/Pb mining area in China to hyperaccumulate Cd (Zhou and Qiu 2005). Surface exposure 

and the contaminated soils associated with mining have 

provided a long period of exposure for plants to evolve 

physiological tolerance to the toxic effects of metals. 

Some trees, such as Salix caprea, Betula pubescens, and 

Quercus robur readily colonize contaminated soils and 

possess tolerance traits (Wisniewski and Dickinson 

2003). The herb Silene vulgaris is characteristic for many 

metal-enriched soils in Europe (Ernst et al. 2000). Aquatic plants, e.g. Lemna trisulca and L. minor (duckweeds) 

or Spirodela polyrrhiza, accumulate and bio-concentrate 

heavy metals (Prasad et al. 2001, Hou et al. 2007, Seth 

et al. 2007). Some lichen photobionts accumulate large 

quantities of metals, e.g. Trebouxia erici (Backor and 

Vaczi 2002). Tolerance of algae to heavy metals has been 

demonstrated for the green algae Chlorella and 

Scenedesmus (Abd-El-Monem et al. 1998). 

Plants ideal for phytoremediation should posses 

multiple traits. They must be fast growing, have high 

biomass, deep roots, be easy to harvest, and should 

tolerate and accumulate a range of heavy metals in their 

aerial and harvestable parts (Kramer 2005). To date, no 

plant has been described that fulfils all these criteria. 

However, a rapidly growing non-accumulator could be 

engineered so that it achieves some of the properties of 

hyperaccumulators (Salt et al. 1998). As already mentioned, the tolerance to individual metals is conferred by 

individual distinct mechanisms (Hall 2002). Co-tolerance 

is rather rare and thus preparing a species tolerant to 

a wide range of metals would mean multiple genetic 

changes (Macnair et al. 2000). 

Phytoremediation technologies are currently available 

for only a small subset of pollution problems, such as As 

and Hg by engineering of transgenic A. thaliana plants 

that over-express an Escherichia coli arsenate reductase 

and PC synthase. A novel approach in phytoremediation 

is phytovolatilization, whereby the contaminant organic 

mercury compounds and Hg2+ are not primarily accumulated in shoot tissues, but are instead transformed by 

the plant into a volatile compound Hg0

 that is released 

into the atmosphere. For this purpose, modified bacterial 

genes were introduced into several plant species including Arabidopsis, tobacco, and poplar, which induce 

expression of organomercurial lyase and mercuric ion 

reductase (Kramer 2005). Kramer (2005) also showed 

that transgenic A. thaliana plants expressing a selenocysteine methyltransferase isolated from the Se hyperaccumulator Astragalus bisulcatus accumulated methylselenocysteine and contained up to eightfold higher Se 

contents than wild-type plants, when grown on a soil 

supplemented with selenite (SeO3

2−

). 
T. KUČERA et al.

488 

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