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Human evolution has led to immense scientific and technological progress. Global development, however, raises new challenges, especially in the field of environmental protection and conservation. Technological ingenuity has enhanced the potential for improving industrial development and rapid progress is being made not only in the field of electronics but also in biological, medical and pharmaceutical applications. In recent decades, increasingly precise knowledge of basic biological functions has brought about biotechnological advances. The possibility to produce transgenic organisms has opened up new fields of experimentation and perspectives for scientific and technological development which go beyond the limits of natural evolution.
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Human evolution has led to immense scientific and techno-
logical progress. Global development, however, raises new
challenges, especially in the field of environmental protec-
tion and conservation. Technological ingenuity has en-
hanced the potential for improving industrial development
and rapid progress is being made not only in the field of
electronics but also in biological, medical and pharmaceu-
tical applications. In recent decades, increasingly precise
knowledge of basic biological functions has brought about
biotechnological advances. The possibility to produce
transgenic organisms has opened up new fields of experi-
mentation and perspectives for scientific and technological
development which go beyond the limits of natural evolu-
In summary, the beginning of the XXI century is witness to
an irreversible dimension of power, with global concern, in
all fields: politics, economics, social and cultural affairs,
science and technology. Technological potential and deve-
lopment, however, have not always had beneficial effects
[15]. Social and cultural progress fall far behind technologi-
cal evolution and the over-exploitation of natural resources
with short-term, fast profit-oriented management systems
has severely damaged the environment.
Acute water and soil pollution are evident consequences
that call for rapid and efficient solutions. However, in addi-
tion, diffuse contamination of large expanses of land [56] is
an ever-growing problem that requires sustainable correc-
tion measures.
Remediation of contamination
The cleanup of soils contaminated by hazardous chemical
substances is a cost-intensive, technically complex proce-
dure. Conventional methods of in situ or ex situ remediation
are based on a number of techniques such as [122]:
Leaching of pollutant by flushing with water or a
chelate. The leachate is recovered and treated on– or
Solidification/stabilization by either physical inclusion
or chemical interactions between the stabilizing agent
and the pollutant.
Vitrification using thermal energy for soil fusion, allow-
ing physical or chemical stabilization
Electrokinetical treatment: ionic species of the pollutant
migrate to electrodes inserted into the soil.
Chemical oxidation or reduction of the pollutant to at-
Acute and diffuse contamination of soil and water by heavy
metals and metalloids cause wide, environmental and social
concern. Among the techniques used to cleanup affected
sites, phytoremediation has recently emerged as a new,
cost-effective, environment-friendly alternative. After a short
introduction to the types of plant-based cleanup techniques,
this review focuses on metal hyperaccumulator plants and
their potential use in phytoextraction technology.
Hi ha una preocupació social i científica creixent per la con-
taminació ambiental, aguda i difusa, dels sòls i de l’aigua
per metalls pesants. Entre la diversitat de tècniques disponi-
bles per a la neteja dels llocs afectats, la fitoremediació ha
emergit recentment com una nova alternativa, efectiva de
costos i sostenible ambientalment. Després d’una breu in-
troducció als diferents tipus de tècniques basades en les
plantes, aquesta revisió se centra principalment en les plan-
tes hiperacumuladores de metalls i considera el seu poten-
cial per a les tecnologies de fitoextracció.
CONTRIBUTIONS to SCIENCE, 2(3): 333-344 (2003)
Institut d’Estudis Catalans, Barcelona
Phytoremediation: principles and perspectives
Joan Barceló* and Charlotte Poschenrieder
Laboratori de Fisiologia Vegetal, Facultat de Ciències, Universitat Autònoma de Barcelona
Keywords: Contamination, heavy metal,
hyperaccumulator plant, phytoremediation.
* Author for correspondence: J. Barceló, Laboratori de Fisiologia
Vegetal, Facultat de Ciències, Universitat Autònoma de Barcelona.
08193 Bellaterra, Catalonia (Spain). Tel. 34 935811267. Fax: 34
935812003. Email:
334 Joan Barceló and Charlotte Poschenrieder
tain chemical species with lower toxicity that are more
stable and less mobile.
Excavation and off-site treatment or storage at a more
appropriate site (“dig and dump”)
In most cases, these techniques are expensive and tech-
nically limited to relatively small areas. These technical diffi-
culties, together with improved knowledge of the mecha-
nisms of uptake, transport, tolerance and exclusion of heavy
metals and other potentially hazardous, contaminants in mi-
croorganisms and plants, have recently promoted the devel-
opment of a new technology, named bioremediation. Biore-
mediation is based on the potential of living organisms,
mainly microorganisms and plants, to detoxify the environ-
ment [2]. The capacity of plants to clean the environment
has been known since the XVIII century when experiments
by Joseph Priestley, Antoine Lavoissier, Karl Scheele and
Jan Ingenhousz demonstrated that, in light, plants purify the
atmosphere. The importance of green zones for the mainte-
nance of air quality is universally accepted, albeit not always
The use of plants for purifying contaminated soils and wa-
ter has been developed much more recently. In the 1970s,
reclamation initiatives of mining sites developed technolo-
gies for covering soil with vegetation for stabilization purpos-
es and reduction of visual impact [142]. It was not until the
1990s that the concept of phytoremediation emerged as a
new technology that uses plants for cleaning or decreasing
the toxicity of soils and surface and waste waters contami-
nated by metals, organic xenobiotics, explosives or radionu-
clides [4, 34, 36, 40, 47, 80, 89, 98, 115, 121]. In this com-
prehensive review, we mainly refer to phytoremediation of
soils contaminated by heavy metals.
Phytoremediation of soils contaminated by heavy
Plants show several response patterns to the presence of
potentially toxic concentrations of heavy metal ions. Most
are sensitive even to very low concentrations, others have
developed resistance and a reduced number behave as hy-
peraccumulators of toxic metals [5, 16, 21, 27, 120, 123, 128].
This particular capacity to accumulate and tolerate large
metal concentrations has opened up the possibility to use
phytoextraction for remediation of polluted soils and waters
[58, 131].
Plants with metal resistance mechanisms based on exclu-
sion can be efficient for phytostabilization technologies. Hy-
peraccumulator plants, in contrast, may become useful for
extracting toxic elements from the soil and thus decontami-
nate and restore fertility in polluted areas. In 1885, the Ger-
man botanist A. Baumann had already found that the leaves
of certain plant species grown on soils with high Zn levels
concentrated high amounts of this metal. However, it was
not until the end of the last century that metal hyperaccumu-
lation was studied in detail. In recent years, improved knowl-
edge of the mechanisms of uptake, transport and tolerance
of high metal concentrations in these plants [3, 62, 74, 75,
81, 106, 107, 127, 135, 136] has opened up new avenues for
remediation by phytoextraction.
In practice, to be operative, phytoextraction requires the
fulfillment of several basic conditions. An ideal plant species
for remediation purposes should grow easily on soils conta-
minated by metals, have high soil-to-shoot transfer factors,
tolerate high shoot metal concentrations, and produce high
biomass quickly [1,12, 13, 17, 23, 24, 55, 59, 60,111].
Unfortunately, most metal hyperaccumulator plants grow
quite slowly and have a low biomass, while plants that pro-
duce a high biomass quickly are usually sensitive to high
metal concentrations. The energy costs of metal tolerance
mechanisms are responsible for this phenomenon (trade-off
hypothesis). There are, however, exceptions (e.g. the Ni hy-
peraccumulator Berkheya coddii) that indicate that the ca-
pacity to accumulate and tolerate high metal concentrations
in shoots and to produce high amounts of dry matter are not
always mutually exclusive [117]. The cost of Cu tolerance in
the non-hyperaccumulator Mimulus guttatus is very small
and no consistent effects on growth or competitiveness are
observed [64]. These data indicate that there is no intrinsic
reason why metal-tolerant plants produced for phytoremedi-
ation should be competitively inferior or slow-growing [90].
As this is a crucial point for developing efficient plants for
metal extraction from polluted soils, the mechanisms of met-
al tolerance in hyperaccumulators are addressed later in
more detail.
Phytoremediation of soils contaminated by heavy metals
can be achieved by a number of techniques [122]:
1. Phytoextraction: This technique reduces soil metal
concentrations by cultivating plants with a high capac-
ity for metal accumulation in shoots. Plants used for
Table 1. Some examples of metal hyperaccumulators. Detailed in-
formation can be found in refs. [2, 8, 29, 46]
Species Shoot metal Reference
µg g–1
Arabidopsis halleri 13,600 Zn Ernst, 1968[44]
(Cardaminopsis halleri)
Thlaspi caerulescens 10,300 Zn Ernst, 1982[46]
Thlaspi caerulescens 12,000 Cd Mádico et al., 1992[91]
Thlaspi rotundifolium 8,200 Pb Reeves & Brooks, 1983 [116]
Minuartia verna 11,000 Pb Ernst 1974[1974]
Thlaspi goesingense 12,000 Ni Reeves & Brooks, 1983[116]
Alyssum bertholonii 13,400 Ni Brooks & Radford, 1978[31]
Alyssum pintodasilvae 9,000 Ni Brooks & Radford, 1978[31]
Berkheya codii 11,600 Ni Brooks, 1998[27]
Psychotria douarrei 47,500 Ni Baker et al., 1985[6]
Miconia lutescens 6,800 Al Bech et al., 1997[24]
malabathricum 10,000 Al Watanabe et al., 1998[7]
Phytoremediation: principles and perspectives 335
this purpose should ideally combine high metal accu-
mulation in shoots and high biomass production. Many
hyperaccumulator species fulfill the first (see Table 1
for examples), but not the second condition.
Therefore, species that accumulate lower metal con-
centrations but are high biomass producers may also
be useful (for examples see Table 2). When plants are
harvested, the contaminants are removed from the
soil. Recovery of high-price metals from the harvested
plant material may be cost effective (e.g. phytomining
[30] of Ni, Tl or Au.). If not, the dry matter can be
burnt and the ash disposed of under controlled con-
2. Rhizofiltration: This technique is used for cleaning con-
taminated surface waters or wastewaters by adsorp-
tion or precipitation of metals onto roots or absorption
by roots or other submerged organs of metal-tolerant
aquatic plants. For this purpose, plants must not only
be metal-resistant but also have a high adsorption sur-
face and must tolerate hypoxia [42, 65]. Some exam-
ples are listed in Table 2.
3. Phytostabilization: Plants are used for immobilizing
contaminant metals in soils or sediments by root up-
take, adsorption onto roots or precipitation in the rhi-
zosphere. By decreasing metal mobility, these
processes prevent leaching and groundwater pollu-
tion. Bioavailability is reduced and fewer metals enter
the trophic web.
4. Phytodegradation: Elimination of organic pollutants by
decomposition through plant enzymes or products.
5. Rhizodegradation: Decomposition of organic pollu-
tants by means of rhizosphere microorganisms [138].
6. Phytovolatilization: Organic pollutants absorbed by
plants are released into the atmosphere by transpira-
tion, either in their original form or after metabolic mod-
ification. In addition, certain metals can be absorbed
and volatilized by certain organisms. Several species
of the genus Astragalus accumulate and volatilize Se.
Uptake and evaporation of Hg is achieved by some
bacteria. The bacterial genes responsible have al-
ready been transferred to Nicotiana or Brassica
species, and these transgenic plants may become
useful in cleaning Hg-contaminated soils [13, 101].
7. Hydraulic control: This technique uses plants that ab-
sorb large amounts of water and thus prevent the
spread of contaminated wastewater into adjacent un-
contaminated areas. Phreatophytes can be used for
cleaning saturated soils and contaminated aquifers
8. Phytorestauration: Revegetation of barren areas by
fast-growing resistant species that efficiently cover the
soil, thus preventing the migration of contaminated soil
particles and soil erosion by wind and surface water
run-off. This technique reduces the spread of contami-
nants and also visual impact. However, previous soil
conditioning is required (e.g. liming or berengerite-
amendments) to enable plants to colonize the polluted
substrate [102, 133, 134,]
In recent years, the scientific and social interest in phy-
toremediation techniques has increased substantially for
several reasons: extensive soil contamination, advanced
scientific knowledge of the mechanisms and functions of liv-
ing organisms and ecosystems, the pressure of public opin-
ion, and political and economical concerns. Twenty years
ago, studies on this subject were scarce, while today many
scientists, especially in the USA and Europe are involved in
basic and applied research projects aimed to make phytore-
mediation a commercially viable technique. Given the inher-
ent limitations of biological systems and the diversity of
problems present at polluted sites, it is unrealistic to con-
ceive phytoremediation as an instant, high-profit, universal
solution for contaminated soil. However, site-specific adap-
tation of general strategies developed in basic scientific re-
search programs can provide sustainable, environment-
friendly solutions for the cleanup of contaminated soils and
sediments. The challenge of contamination cleanup and the
crucial contribution of research in this field can be put into
perspective by considering some statistic and economic
data. In 1998, the European Environmental Agency estimat-
Species Extracted contaminant/substrate References
Salix Heavy metals/soil, water Greger and Landberg, 1999 [60]
Populus Ni/ soil, water, groundwater Punshon and Adriano, 2003[112]
Brassica napus, B. juncea, B. nigra Radionuclides, heavy metals, Se/soil Brown, 1996[32], Bañuelos et al.,1997[12]
Cannabis sativa Radionuclides, Cd/soil Ostwald 2000[105]
Helianthus Pb,Cd /soil EPA, 2000[130] Elkatib et al., 2001[43]
Typha sp. Mn, Cu, Se/mine wastewater Horne, 2000 [65]
Brassica juncea Se/saline drainage effluent Bañuelos et al.1997[14]
Phragmites australis Heavy metals/mine tailings-wetland Massacci et al., 2001[95]
Glyceria fluitans Heavy metals/mine tailings-wetland MacCabe and Otte, 2000[97]
Lemna minor Heavy metals/water Zayed et al., 1998[143]
Table 2. Some examples of high biomass-producing species with potential use in phytoextraction or rhizofiltration
336 Joan Barceló and Charlotte Poschenrieder
ed a total of 1,400,000 contaminated sites in Western Eu-
rope. A comparison of the economic costs between conven-
tional, physical-chemical, decontamination procedures and
new, plant-based, phytoremediation technology clearly fa-
vors the latter. According to several authors [39, 100], con-
ventional procedures raise the average cost per contaminat-
ed hectare of soil from 0.27 to 1.6 million $, while
phytoremediation costs from about 10 to 1000 times less.
From the period 1998-2000 to 2005, the market for phytore-
mediation in the USA is estimated to increase from $16-29
million to $214-370 million The time factor is by far the most
critical point in plant-based cleanup techniques. However,
the long persistence of heavy metal contamination in soils
(residence times of thousands of years) makes even long-
term cleaning strategies attractive.
The complex scenario of acute or diffuse soil contamina-
tion by heavy metals therefore deserves attention by the sci-
entific, economic, social, and politic authorities in order to
provide the means to study successful mechanisms for soil
remediation. Only with a sustainable focus of this kind will
harmony between nature and human evolution be restored.
Metal hyperaccumulator plants
At least 400 species distributed in 45 botanical families are
considered metal hyperaccumulators [27]. By definition, hy-
peraccumulators are herbaceous or woody plants that accu-
mulate and tolerate without visible symptoms a hundred
times or greater metal concentrations in shoots than those
usually found in non-accumulators. Baker and Brooks estab-
lished 0.1% as the minimum threshold tissue concentrations
for plants considered Co, Cu, Cr, Pb or Ni hyperaccumula-
tors, while for Zn or Mn the threshold is 1% [5, 7].
Hyperaccumulators are metallophytes and belong to the
natural vegetation of metal-enriched soils [48, 49, 108].
These species have evolved internal mechanisms that allow
them to take up and tolerate large metal concentrations that
would be extremely toxic to other organisms [37, 79]. These
plants are perfectly adapted to the particular environmental
conditions of their habitat and high metal accumulation may
contribute to their defense against herbivores and fungal in-
fections [26, 94, 127]. However, usually, the metabolic and
energetic costs of their adaptation mechanisms do not allow
them to compete efficiently on uncontaminated soil with non-
Metal hyperaccumulation has evolved in plants all over
the world and important sites for collecting germplasm are,
among others, New Caledonia, Australia, Central and South
Europe, the Mediterranean Area, South-East Asia, Cuba,
Dominican Republic, California, Zimbabwe, Transvaal in
South Africa, Goiàs in Brazil, Hokkaido in Japan, and New-
foundland in Canada [5, 45].
Several hypotheses have been proposed to explain the
mechanisms of metal hyperaccumulation and the evolution-
ary advantage of this strategy.
1. Complex formation and compartmentation: Hyperac-
cumulators synthesize chelators that detoxify metal
ions by complex formation. The soluble, less-toxic,
organic-metal complex is transported to cell compart-
ments with low metabolic activity (cell wall, vacuole)
where it is stored in the form of a stable organic or in-
organic compound. [18, 19, 20, 54, 62, 129, 135,
2. Deposition hypothesis: Hyperaccumulators separate
metals from the root, accumulating them in plant parts
that are abscised (old leaves), leached by rain (epider-
mis, hairs) or burnt.
3. Inadverted uptake: Hyperaccumulation of the metal is
thought to be the by-product of an adaptation mecha-
nism to other adverse soil characteristics (e.g. Ni hy-
peraccumulation in serpentinophytes)
4. Hyperaccumulation as a defense mechanism against
abiotic or biotic stress conditions. Metal effectiveness
against certain pathogenic fungi and bacteria and on
leaf-consuming herbivores has been reported [25].
Phloem parasites [53], however, are unaffected, prob-
ably because of low phloem mobility of the metals.
High metal concentrations in leaves can act as feeding
deterrents or, after ingestion, may reduce the repro-
duction rate of herbivores or poison them. Trade-off of
organic defenses by metal hyperaccumulation may
also confer advantage [127]. It has been suggested
that high leaf metal concentrations may be used in os-
motic adjustment under drought stress [8, 109]. Exten-
sive studies in Alyssum murale (Ni hyperaccumulator)
and Thlaspi caerulescens (Zn hyperaccumulator)
have not confirmed this hypothesis [141].
At present, the adaptive advantages of the hyperaccumu-
lation strategy are unclear. The strategy probably involves
complex interactions of diverse factors and mechanisms
that cannot be ascertained by a single, reductionistic inter-
pretation. From both the scientific and practical viewpoint,
however, the way in which plants achieve metal hyperaccu-
mulation is of much greater interest than the raison d’être of
the mechanism. Only by studying the basic mechanisms of
hyperaccumulation will phytoextraction technologies be
successfully developed.
Mechanisms of metal tolerance and
hyperaccumulation in plants
Metal hyperaccumulators are highly specialized models of
plant mineral nutrition. Seventeen elements are considered
essential for all higher plants (C, H, O, N, S, P, K, Ca, Mg, Fe,
Mn, Cu, Zn, B, Mo, Cl, and Ni). Macronutrients are those
necessary in high concentrations (mM level) while micronu-
trients are required only in µM tissue concentrations. Hyper-
accumulators concentrate, in a specific way, certain trace
metals or metalloids that may be essential (Cu, Mn, Zn, or Ni)
or not (e.g. Cd, Pb, Hg, Se, Al, As) at amounts that would be
Phytoremediation: principles and perspectives 337
extremely toxic to other plants [3, 5, 27, 62, 67, 93, 110,128].
Some examples are given in Table 1.
Most metallophytes that can colonize metal-polluted soils
base their metal resistance on efficient exclusion of metal
ions from root tip meristems and shoots [16, 18, 20, 50, 54,
82]. In contrast, hyperaccumulators, preferentially accumu-
late the metal in shoots and, in the case of hyperaccumula-
tion of essential trace elements, this capacity is frequently
accompanied by plant requirement for unusually high sub-
strate availability of the metal in order to avoid deficiency
[128, 129]. This may be the result of a constitutively active
mechanism that inactivates incoming metal ions in hyperac-
cumulators. Rapid complexation and compartmentation not
only detoxify metal ions but also make them less available
for essential metabolic processes. To understand the physi-
ological, biochemical and molecular mechanisms that un-
derlie metal hyperaccumulation in plants, it is necessary to
consider metal uptake, transport and metabolic processes
involved in the entire organism, from the rhizosphere to the
leaf cell compartment.
Rhizosphere interactions
The availability of metals in the soil around roots is strongly
affected by root exudates and root depositions (mucilage
and border cells) but also by microbial activities such as
siderophore release and redox reactions [41, 70, 84, 93].
The mutual influence of plants and soil microorganisms and
the selective force of soil metal concentrations on microbe
populations make research on this topic very difficult. Given
the possible environmental problems associated with metal
mobilization by synthetic chelators [22, 61, 85, 110, 118],
enhancement of metal availability in the rhizosphere by hy-
peraccumulators would be a useful mechanism for improv-
ing phytoextraction technologies. At present, however, data
on the role of root exudates from hyperaccumulators in met-
al mobilization are contradictory. While in acidic and cal-
careous soils some authors found that Thlaspi caerulescens
tends to decrease rhizosphere pH [63, 71], others observed
a decrease [99]. However, pH changes do not appear to be
a relevant mechanism for metal mobilization by this kind of
plant. Release of histidine and citrate into the rhizosphere
may play a crucial role in the reduction of Ni uptake and tox-
icity in the Ni sensitive Thlaspi arvense, while in the Ni hyper-
accumulator Thlaspi goesingense no Ni-enhanced release
of these chelators into the rhizosphere was found [119]. The
involvement of bacteria in Zn mobilization in the rhizosphere
of Thlaspi caerulescens has been reported [140]; bacterial
production of siderophores may be responsible for en-
hanced bioavailability [83].
Metal uptake and root-to-shoot transport
Metal resistance in species with exclusion strategy is fre-
quently based on reduced metal uptake into roots, preferen-
tial storage of metals in root vacuoles and restricted translo-
cation into shoots. Hyperaccumulators, in contrast, take up
more metals, store a lower proportion of them in root vac-
uoles, and export higher amounts to shoots (Figure 1).
Comparative studies on Zn uptake and transport in the
non-hyperaccumulator Thlaspi arvense and the Zn– hyper-
accumulator Thlaspi caerulescens indicate that these differ-
ences are caused by altered tonoplast Zn transport in roots
and stimulated Zn uptake into leaves [77, 78]. Stimulation of
ZNT1 expression, a genes that encodes a Zn transporter
that belongs to the ZIP family of plant micronutrient trans-
porters, was higher in Thlaspi caerulescens than in Thlaspi
arvense. Other transporter systems of special interest in hy-
peraccumulators are the cation diffusion facilitators (CDF
type), the ABC transporters for phytochelatins and the metal
chaperones [38, 81, 103, 104, 106, 125, 132]. Detailed stud-
ies on the characterization and the differential distribution of
these transporter systems in hyperaccumulators and non-
hyperaccumulators will clarify the basic genetic and molec-
ular mechanisms responsible for metal hyperaccumulation.
The results from this research may lead to the development
of specific strategies to produce efficient plants for metal ex-
Epidermis/cortex Xylem
To Shoot
Endodermis with
Casparian band
Thlaspi arvense
Epidermis/cortex Xylem
To Shoot
Endodermis with
Casparian band
Figure 1. Differences in Zn transport in roots of the Zn hyperaccu-
mulator Thlaspi caerulescens and the non-accumulator Thlaspi ar-
vense. Thin arrows, low transport; thick arrows, high transport.
(modified after Lasat and Kochian, 2000 [76].)
338 Joan Barceló and Charlotte Poschenrieder
traction technologies by molecular engineering and conven-
tional breeding [10].
The pathways of radial root transport of metals and their
entrance into the vascular cylinder are a further issue of de-
bate in hyperaccumulation research. It has been proposed
that apoplastic transport of Zn to the xylem is required for
sustaining rapid Zn transport to the leaves [106], while facto-
rial experiments with Zn and Cd [86, 92] support the hypoth-
esis of a common, but Cd-preferent, symplastic transport
system for Zn and Cd to the xylem [52].
Formation of less toxic metal complexes is essential in
metal hyperaccumulation in plants. The toxicity of metal
cations is mainly due to their tendency to form organic com-
plexes with distinct ligands, which interfere with membrane
functions, enzyme reactions, electron transport etc. Uptake
and root-to-shoot transport of high metal concentrations is
only possible when these toxic interactions are avoided by
the synthesis of strong chelators that efficiently bind the met-
als in a non-toxic form, thereby allowing flux to and through
the xylem up to the leaves. Organic acids, aminoacids, phy-
tochelatins have been implied in metal detoxification The Zn
and Cd hyperaccumulator Thlaspi caerulescens contains
constitutively high organic acid levels [129]. Many Al hyper-
accumulators contain high concentrations of either or both
organic acids and flavonoid-type phenolics, which form
strong complexes with the metal [18, 19]. High concentra-
tions of organic acid anions in leaf tissues are a crucial,
widely distributed, mechanism that allows plants to maintain
cation/anion homeostasis under conditions of excess ion
stress. The ability to accumulate high organic acid levels in
tissues may be considered a prerequisite, but is not suffi-
cient, for metal tolerance [18, 129].
The sulfhydryl-rich phytochelatins (PC) have high affinity
for binding Cd, Hg, Cu or even As. Arabidopsis cad1 mu-
tants, deficient in PC synthase, are very sensitive to Cd [66].
Nonetheless, treatment of Cd-exposed plants with BSO, an
inhibitor of PC synthesis, increased Cd sensitivity only in
plants that lacked Cd hypertolerance. These results indicate
that Cd hypertolerance is not based on PC-mediated se-
questration. In contrast, PC-based sequestration may be es-
sential in both constitutive As tolerance and As hypertoler-
ance [124].
A metal can be bound by a number of ligands within dis-
tinct plant organs and compartments. In this regard, in 1975,
Mathys [96] and Ernst [51] proposed the malate shuttle hy-
pothesis. According to this hypothesis, in Zn-resistant plants
excess Zn is bound to malate in the cytoplasm and, after
transport to the vacuole, a ligand exchange occurs. Zn
forms more stable complexes with citrate, oxalate or other
ligands, while malate returns to the cytoplasm. Recent re-
search shows that ligand exchange can also play a critical
role in hyperaccumulators. Studies with the Al hyperaccu-
mulator Fagopyrum esculentum revealed the importance of
ligand exchange (oxalate-citrate-oxalate) during Al trans-
port from the rhizosphere through roots to the leaves [88].
Furthermore, in the Ni hyperaccumulator Thlaspi goesin-
gense, Ni is bound by several ligands. Cytoplastic Ni seems
to be detoxified by binding to histidine, while vacuolar stor-
age of Ni is probably in the form of citrate [74].
Data indicate that metal hyperaccumulation is not based
on the capacity of a plant to produce a high concentration of
a particular chelator, but that it involves the coordinated ac-
tion of a number of ligands and differential distribution of di-
verse metal transport systems. Current research is begin-
ning to identify the components that interact in metal
hyperaccumulation. However, the regulatory processes re-
sponsible for this particularly altered metal homeostasis in
hyperaccumulators remains to be elucidated. Progress in
this field of basic research is essential to identify or produce
effective plants for phytoextraction technologies.
Conventional breeding and genetic engineering
for efficient phytoextraction
As stated at the beginning of this review, the development of
commercial phytoextraction technologies requires plants
that produce high biomass and that accumulate high metal
concentrations in organs that can be easily harvested, i.e. in
shoots. There are two main approaches to this problem:
(1) Domestication and breeding of improved hyperaccu-
mulator species [33] and
(2) Application of genetic engineering to develop fast-
growing high biomass plants with improved metal uptake,
translocation and tolerance [69, 73]. Some examples are
shown in Table 2.
The first approach, mainly developed in the USA by the
group headed by Chaney, involves several crucial steps: se-
lection of hyperaccumulator plants that are likely to be do-
mesticated, collection of seeds from wild plants and bioas-
say of their phytoextraction utility, breeding for improved
cultivars and development of adequate soil and crop man-
agement practices [33]. The usefulness of this system has
been shown for Co and Ni and has obtained a utility patent
[35]. However, the authors recognize that in situations where
available hyperaccumulator species are too small to afford
economic cleanup procedures, biotechnology may be re-
quired to combine hyperaccumulation and high biomass
The V Framework Research Program of the European
Community includes two projects [68] on the production of
genetically modified plants for phytoremediation, PHYTAC
and METALLOPHYTES. The former (
vaha/PHYTAChome.htm) aims to transfer genes from the hy-
peraccumulator Thlaspi caerulescens to the high biomass–
producing Brassica or tobacco. While the METALLO-
PHYTES project is devoted to engineering Festuca for im-
proved metal tolerance and or accumulation
To date, the most successful approach has been the
transformation of plants using modified bacterial merA gene
(mer A9) for detoxifying Hg (II). The merA gene codifies for a
mercuric ion reductase that removes Hg from stable thiol
salts by reducing it to volatile metallic Hg. When grown in a 5
Phytoremediation: principles and perspectives 339
µM Hg(II) solution, transformed Arabidopsis plants express-
ing the merA9 gene volatilized 10 ng of metallic Hg per
minute and mg plant tissue. Hg reductase has also been
successfully transferred to Brassica, tobacco and yellow
poplar trees [101].
There are, however, ecological, social, and legal objec-
tions to the practical application of genetically modified or-
ganisms in the field. The potential of transgenic plants to effi-
ciently cleanup contaminated sites may help to change
adverse public opinion. Nonetheless, future research should
address not only the “know-how” of producing efficient
plants for phytoremediation and their integration into sus-
tainable cropping and management systems, but should
also clarify the potential impact of transgenic plants on the
target habitat and the fate of the introduced genes in the sur-
rounding environment.
Concluding remarks
Phytoremediation is a new, attractive technique that has
emerged over recent years. This technique offers excellent
perspectives for the development of plants with the potential
for cleaning metal-contaminated soils, at least under certain,
favorable conditions and for using adequate crop manage-
ment systems. Advances in molecular biology and genetic
engineering of plants have been indispensable for this
progress. However, this spectacular development would not
have been possible without the invaluable contribution of a
small group of researchers. More than thirty years ago they
showed extraordinary scientific insight by recognizing the
enormous potential of plants that can colonize metal-conta-
minated soils and they dedicated many years of conscien-
tious research to the geobotany and ecophysiology of metal-
lophytes. Exploratory studies of this kind are still necessary
and should be supported in order to preserve the immense
natural genetic resources of metallipherous habitats and to
increase our basic knowledge about the natural adaptation
mechanisms of hyperaccumulators.
In this regard, we dedicate this review to Prof. W.H.O
Ernst, an eminent pioneer in research into metallophytes.
Part of the authors work cited in this paper was supported by
the Generalitat de Catalunya (Autonomous Government of
Catalonia) (2001 SGR-00200), the European Union (ICA4-
CT-2000-30017), and the Spanish Government (DGICYT,
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344 Joan Barceló and Charlotte Poschenrieder
About the authors
Joan Barceló was born in Palma de
Mallorca in 1938. He graduated in
Pharmacy from the University of
Barcelona in 1964 and obtained Ph.D.
in 1970 with his work on the effect of
UV radiation on plants. In 1973 he be-
came an associate lecturer at the Fac-
ulty of Pharmacy of the same university
and in 1976 he was appointed Full Pro-
fessor of Plant Physiology at the Com-
plutense University of Madrid. From
1980 to 1982 he held the post of Pro-
fessor of Plant Physiology at the Uni-
versity of the Balearic Islands, where
he was also the Dean of the Science
Faculty. Since 1982 Joan Barceló has
been a Professor and Head of the
Plant Physiology Laboratory at the Sci-
ence Faculty of the Autonomous Uni-
versity of Barcelona. He is full member
of the Royal Academy of Pharmacy of
Charlotte Poschenrieder was born in
1954 in Munich (Germany). She ob-
tained her degree in Pharmacy and her
Ph.D. from the Complutense University
of Madrid in 1978 and 1980, respec-
tively. From 1980 to 1982 she held the
post of assistant lecturer at the Science
Faculty of the University of the Balearic
Islands. Since 1982, she has been
teaching and carrying out research in
the Plant Physiology Laboratory at the
Autonomous University of Barcelona;
at present she holds the post of
tenured lecturer.
The authors research mainly focus-
es on stress physiology in plants, and
is reflected in more than 250 publica-
tions, many in peer-reviewed interna-
tional journals. The team headed by
Joan Barceló and Charlotte Poschen-
rieder is involved in several national
and international, research projects.
The mechanisms of heavy metal stress
and tolerance and the adaptation of
maize to acid soil conditions in the
tropics are the main subjects of their
current research.
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... Unlike phytoextraction, in the phytostabilization mechanism plants must have a dense root system, in order to produce a large amount of biomass at the root level, and possess the ability to immobilize the contaminant and retain it in this part of the plant [386] through root adsorption or the precipitation/complexation/reduction of metals [387]. ...
... Unlike phytoextraction, in the phytostabilization mechanism plants must have a dense root system, in order to produce a large amount of biomass at the root level, and possess the ability to immobilize the contaminant and retain it in this part of the plant [386] through root adsorption or the precipitation/complexation/reduction of metals [387]. ...
Full-text available
Nowadays, there are a multitude of sources of heavy metal pollution which have unwanted effects on this super organism, the soil, which is capable of self-regulation, but limited. Living a healthy life through the consumption of fruits and vegetables, mushrooms, edible products and by-products of animal origin, honey and bee products can sometimes turn out to be just a myth due to the contamination of the soil with heavy metals whose values, even if they are below accepted limits, are taken up by plants, reach the food chain and in the long term unbalance the homeostasis of the human organism. Plants, these miracles of nature, some with the natural ability to grow on polluted soils, others needing a little help by adding chelators or amendments, can participate in the soil detoxification of heavy metals through phytoextraction and phytostabilization. The success of soil decontamination must take into account the collaboration of earth sciences, pedology, pedochemistry, plant physiology, climatology, the characteristics of heavy metals and how they are absorbed in plants, and in addition how to avoid the contamination of other systems, water or air. The present work materialized after extensive bibliographic study in which the results obtained by the cited authors were compiled.
... Material And MethodsPlant material and growing conditionsSeeds of a monoecious hemp bre cultivar (Cannabis sativa cv.Santhica 27) were sown in loam substrate in greenhouse conditions. After one week, the obtained seedlings were transferred to nutrient Mo7 O 24 and 14.5 Fe-EDDHA) in 5 L tanks: for each tank, the seedling was adapted to plugged hole in a polystyrene plate oating at the top of the solution. Tanks were placed in a phytotron under fully controlled environmental conditions (constant temperature of 24 ± 1°C with a mean light intensity of 230 µmoles m − 2 s − 1 provided by Phillips lamps (Philips Lighting S.A., Brussels, Belgium) (HPI-T 400 W), a photoperiod of 16h under a relative humidity of 65%). ...
Full-text available
Hemp ( Cannabis sativa L.) is a promising crop for non-food agricultural production on soils contaminated by moderate doses of heavy metals, while silicon, as a beneficial element, is frequently reported to improve stressed plants behavior. Using a hydroponic system, plants of Cannabis sativa (cv. Santhica 27) were exposed for one week to 100 µM Zn in the presence or absence of 2 mM Si. Zinc accumulated in all plants organs but was mainly sequestered in the roots. Additional Si reduced Zn absorption but had no impact on Zn translocation. Zn accumulation had a negative impact on biomass and chlorophyll content but additional Si did not mitigate these symptoms. Exogenous Si reduced the Zn-induced membrane lipid peroxidation (assessed by malondialdehyde quantification) and increased the total antioxidant activities estimated by the FRAP index. In the absence of Si, leaf phytochelatin and total glutathione were the highest in Zn-treated plants and Si significantly decreased their concentrations. Additional approaches using omics strategies and histological localization of element will provide interesting information regarding the interaction of Zn and Si in hemp.
... Previous and current practices of transition metal "clean-ups" have involved various physical, chemical, or biological processes such as incineration, soil washing, vitrification, chemical oxidation, solidification/stabilization, electrokinetic treatment, and excavation and offsite treatment (Poschenrieder and Coll 2003;Montpetit and Lachapelle 2017). In addition to being costly, some of these traditional methods of remediation could be very invasive and environmentally destructive (EPA 2008). ...
Full-text available
The use of plants to extract metal contaminants from soils has been proposed as a cost-effective means of remediation, and utilizing energy crops for this phytoextraction process is a useful way of attaining added value from the process. To simultaneously attain both these objectives successfully, selection of an appropriate plant species is crucial to satisfy a number of imporTant criteria including translocation index, metal and drought tolerance, fast growth rate, high lignocellulosic content, good biomass production, adequate calorific value, second generation attribute, and a good rooting system. In this study, we proposed a multi-criteria decision analysis (MCDA) to aid decision-making on plant species based on information generated from a systematic review survey. Eight species Helianthus annuus (sunflower), Brassica juncea (Indian mustard), Glycine max (soybean), Salix spp. (willow), Populus spp. (poplar), Panicum virgatum (switchgrass), Typha latifolia (cattails), and Miscanthus sinensis (silvergrass) were examined based on the amount of hits on a number of scientific search databases. The data was normalized by estimating their min–max values and their suitability. These criteria/indicators were weighted based on stipulated research objectives/priorities to form the basis of a final overall utility scoring. Using the MCDA, sunflower and silvergrass emerged as the top two candidates for both phytoremediation and bioenergy production. The multi-criteria matrix scores assist the process of making decisions because they compile plant species options quantitatively for all relevant criteria and key performance indicators (KPIs) and its weighing process helps incorporate stakeholder priorities to the selection process.
... Todas las plantas absorben metales del suelo donde se encuentran pero en distinto grado, dependiendo de la especie vegetal, y de las características y contenido en metales del suelo. Las plantas pueden adoptar distintas estrategias frente a la presencia de metales en su entorno (Baker, 1981;Barceló et al., 2003). Unas basan su resistencia a los metales con la estrategia de una eficiente exclusión del metal, restringiendo su transporte a la parte aérea. ...
... The rejection mechanism of plants to heavy metals usually includes two aspects: to reduce the absorption of heavy metals in roots, and to restrict the transfer of heavy metals to shoot using compartmentalization and preservation in roots [45]. The most important feature of the exclusion plants is that the heavy metal content of the plant body, especially the shoots, is low. ...
Full-text available
Miscanthus floridulus is a plant with a high biomass and heavy metal tolerance, which is a good candidate for phytoremediation. Pot experiments were conducted to compare the growth response, Pb enrichment ability, and the effect on Pb speciation of two ecotypes of M. floridulus from the Dabaoshan Mining Area and the non-mining area of Boluo County, Huizhou, in soils with different Pb contents. The results showed that two ecotypes of M. floridulus had different growth responses to Pb concentrations in soil. Under a low concentration of Pb (100 mg·kg−1) treatment, the aboveground biomass of the non-mining area plant ecotype was significantly affected, while the plants with the mining area ecotype were not significantly affected. When the concentration of Pb increased, the aboveground biomass of the non-mining ecotype was 30.2–41.1% of the control, while that of the mining ecotype was 57.8–65.0% of the control. The root biomass of the non-mining ecotype decreased with the increase of treatment concentration, accounting for 57.8–64.2% of the control, while that of the mining ecotype increased significantly, accounting for 119.5–138.6% of the control. The Pb content in the shoots and roots of the mining ecotype M. floridulus increased rapidly with the increase of the Pb treatment concentration in the soil, and the increase in speed was obviously faster than that of the non-mining ecotype. The total amount of Pb accumulated in the roots of the ecotype from the mining area was much greater than that of the ecotype from the non-mining area, and increased significantly with the increase of Pb concentration in the soil (p < 0.05). With the aggravation of Pb stress, the transfer coefficient and tolerance index of the two ecotypes decreased by different degrees. The transfer coefficient and tolerance index of the mining ecotype were significantly higher than those of the non-mining ecotype. Pearson correlation analysis showed that root biomass was positively correlated with shoot biomass, and shoot biomass was negatively correlated with Pb content in both root and shoot, indicating that Pb accumulation in root and shoot was toxic to plants and inhibited the growth of M. floridulus. The mining ecotypes showed stronger tolerance to and enrichment of Pb.
... The physicochemical methodologies (landfill, thermal, leaching, electro-reclamation and removal) have long been embraced for remediation of HMs (Sheoran et al. 2011;Barcelo and Poschenrieder 2003). Physico-chemical methodologies are quick however insufficient, expensive and occasionally may cause unfavorable consequences for soil inherent characteristics, and make secondary contamination (Glick 2010;Doble and Kumar 2005;Ali et al. 2013). ...
Soil is a dynamic life-supporting component of this Planet Earth but its contamination with toxic heavy metalsHeavy metals (HMs) is omnipresent throughout the planet. Abundances of these HMs in soil have augmented considerably in last 2–3 decades due to rapid industrialization, agricultural practices (fertilizers and pesticides application), and other anthropogenic activities, which causing environmental, ecological and health risks. Consequently, their remediation approaches from the environmental components are critical. Among the several procedures for metals remediation, organic residues with the plant-microbes (phyto-remediation) can simultaneously increase the fertility of soil along with the bio-remediation, which in turn is thought as one of the lucrative and cost-effective approaches of HM’s remediation from soil. Efficacy of phyto-remediation can be improved by simultaneous participations of plant-growth-promoting bacteria which can convert HMs into soluble and bio-available forms by the activities of siderophores, redox processes, biosurfactants, organic acids, and biomethylation. This work highlights the recent applications and advancements made hitherto to understand the molecular and biochemical mechanisms of metal-microbe-plant interactions with organic residues along with their functions in major processes belong to the phyto-remediation, for instance heavy metalHeavy metals detoxification, transformation, mobilization, distribution, and immobilization.
... 4. Chromium can cause rapid hair fall (Salem et al., 2000). 5. Higher levels of Cu have been reported to cause brain and kidney damage, severe anemia and intestinal irritation (Salem et al., 2000). 6. Arsenic in arsenate form being analogous to phosphate interferes with cellular processes such as oxidative phosphorylation and ATP synthesis (Tripathi et al., 2007). ...
Conference Paper
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Heavy metals are among the contaminants in the environment. Beside the natural activities, almost all human activities also have potential contribution to produce heavy metals as side effects. Migration of these contaminants into no contaminated areas as dust or leachates through the soil and spreading of heavy metals containing sewage sludge are a few examples of events contributing towards contamination of the ecosystems. Several methods are already being used to clean up the environment from these kinds of contaminants, but most of them are costly and far away from their optimum performance. The chemical technologies generate large volumetric sludge and increase the costs chemical and thermal methods are both technically difficult and expensive that all of these methods can also degrade the valuable component of soils. Conventionally, remediation of heavy-metal contaminated soils involves either onsite management or excavation and subsequent disposal to a landfill site. This method of disposal solely shifts the contamination problem elsewhere along with the hazards associated with transportation of contaminated soil and migration of contaminants from landfill into an adjacent environment. Soil washing for removing contaminated soil is an alternative way to excavation and disposal to landfill. This method is very costly and produces a residue rich in heavy metals, which will require further treatment. Moreover, these physic-chemical technologies used for soil remediation render the land usage as a medium for plant growth, as they remove all biological activities. Recent concerns regarding the environmental contamination have initiated the development of appropriate technologies to assess the presence and mobility of metals in soil, water, and wastewater. Presently, phytoremediation has become an effective and affordable technological solution used to extract or remove inactive metals and metal pollutants from contaminated soil. Phytoremediation is the use of plants to clean up a contamination from soils, sediments, and water. This technology is environmental friendly and potentially cost effective. In this study, application of phytoremediation technology as a management option for soils contaminated with heavy metal ions it was discussed.
Different forms of pollutions as resulted from the anthropogenic activities and the consequent eco-degradations of various landscapes and ecosystems in different parts of the world, including the wetland ecosystem have emerged as a burning environmental issue across the globe. This has necessitated to undertake proper eco-rehabilitation, eco-reclamation and eco-restoration efforts with an eye to achieve the goals of sustainable eco-management of perturbed and degraded ecosystems so that continued supply of ecosystem services can be ensured. The eco-dynamism of wetland ecosystem endowed with embedded complexity requires to have an in-depth analysis in order to adopt transparent, flexible and effective ecological planning and environmental management strategies accommodating and integrating a diversity of knowledge bases and ethical values of human perception. Both of the recently emerged eco-management components, the bio-monitoring (an important part of eco-monitoring) and bio-remediation (an integral step towards any eco-restoration effort), help in reaching the goal of sustainability of the wetland ecosystem. This chapter has dealt with the different emergent issues pertaining to the bio-monitoring and bio-remediation and scopes of their applicability in the management of environment in general and wetland ecosystem in particular. Case studies pertaining to the applicability of several biotic indices [Water Quality Index (WQI), Biotic Community Indices, Pollution Load Index (PLI), Bio-Concentration Factor (BCF), etc.] calculated and deducted based on the occurrences, distribution, abundances and diversity of some aquatic living organisms, such as fungi, zooplankton and molluscs in relation to major ecological variables from both the freshwater lotic and lentic water bodies, have been discussed. Besides, how does the quantification of the variabilities of different biotic components caused by the changes in the ecological variables of the wetland, including the seasonal population dynamics and binary distribution patterns of zooplankton, help in formulating and deducting similarity indices, and some other biotic indices like Species Pollution Value (SPV) and Community Pollution Value (CPV) contribute for more effective assessment of the degree of pollution of the concerned wetlands have been discussed with case studies.
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The present study was based on a hypothesis that excess copper (Cu) in the soil reduces the growth and seed yield of chicory plants and chicory plants have the potential to clean up the Cu-contaminated soil. A pot experiment was conducted to investigate the abovementioned hypothesis in which chicory plants were grown in the garden soil contaminated with three doses of copper (150, 450 and 750 mg Cu kg⁻¹ soil) except control and the results were recorded to evaluate the effect of copper-induced toxicity on the vegetative and reproductive growth parameters of Cichorium intybus L. and its soil remediation potential. Results revealed that all Cu treatments decreased the vegetative and reproductive growth parameters of Cichorium intybus. Chlorophyll content (a, b and total) decreased significantly (P ≤ 0.05) while proline content in the fresh leaves and Cu accumulation in different plant organs increased significantly (P ≤ 0.05) on increasing Cu concentration in the soil. The pattern of Cu accumulation in different plant organs was shoot > root > seeds. Cu levels in the seeds obtained from 450 and 750 mg Cu kg⁻¹ soil-treated plants exceeded the permissible limits of the world health organization (WHO). Biological concentration factor (BCF), biological accumulation coefficient (BAC) and translocation factor (TF) values showed that Cichorium intybus absorbed and accumulated a considerable amount of Cu and accumulation of Cu was found to be greater in the shoots than in the roots. Hence Cichorium intybus L. can be used for phytoextraction and is considered a potential candidate to clean up the Cu-contaminated soil.
Full-text available
Aluminium (Al) toxicity is widely considered to be the most important growth‐limiting factor for plants in strongly acid soils (pH<5.0). The inhibition of root elongation in three varieties of maize ( Zea mays L. vars Clavito, HS701b and Sikuani) was followed over the first 48 h of Al treatment, and during the initial 10 h elongation was determined on an hourly basis. The silicon (Si)‐induced amelioration of Al toxicity was investigated by pre‐treating seedlings for 72 h in nutrient solutions with 1000 μM Si before transfer into solutions with 0, 20 or 50 μM Al (without Si). Plants were either grown in complete low ionic strength nutrient solutions (CNS) or in low salt solutions of 0.4 mM CaCl 2 (LSS). In addition, the role of root exudation of organic compounds as a mechanism of Si‐induced alleviation of Al toxicity was investigated. Aluminium‐induced inhibition of root elongation in the maize var. HS701b was observed within 1 h of Al exposure. After a lag time of at least 8 h, Si‐induced alleviation of Al toxicity was observed in this variety when grown in LSS. In the Al‐resistant var. Sikuani, Al‐resistance was only observed after exposure to 50 μM Al, and not after exposure to 20 μM Al, suggesting that there exists a threshold Al concentration before the mechanisms of Al resistance are activated. Aluminium stimulated root exudation of oxalic acid in all three varieties, but exudate concentrations did not increase with either Al resistance or with Si pretreatment. Aluminium and Si triggered release of catechol and of the flavonoid‐type phenolics: catechin, and quercetin. In the Al‐resistant variety, Sikuani, Al‐exposed plants pretreated with Si exuded up to 15 times more phenolics than those plants not pretreated with Si. The flavonoid‐type phenolics, to date unconsidered, appear to play a role in the mechanism(s) of Si‐induced amelioration of Al toxicity.
Trace metals occur as natural constituents of the earth's crust, and are ever present constituents of soils, natural waters and living matter. The biological significance of this disparate assemblage of elements has gradually been uncovered during the twentieth century; the resultant picture is one of ever-increasing complexity. Several of these elements have been demonstrated to be essential to the functions of living organisms, others appear to only interact with living matter in a toxic manner, whilst an ever-decreasing number do not fall conveniently into either category. When the interactions between trace metals and plants are considered, one must take full account of the known chemical properties of each element. Consideration must be given to differences in chemical reactivity, solubility and to interactions with other inorganic and organic molecules. A clear understanding of the basic chemical properties of an element of interest is an essential pre-requisite to any subsequent consideration of its biological significance. Due consideration to basic chemical considerations is a theme which runs through the collection of chapters in both volumes.