Metal Hyperaccumulation in Plants: A Review Focusing on Phytoremediation Technology
Metal hyperaccumulation is a characteristic present in over 500 plant species and approximately in 0.2% of all angiosperms. Hyperaccumulators are model plants for phytoremediation as they are tolerant to heavy metals. Metals hyperaccumulation and tolerance are genetically inherited traits. Plants possess a range of potential cellular mechanisms that may be involved in the detoxification of heavy metals and thus tolerance to metal stress. Recent discovery have given first insights into the molecular basis of metal hyperaccumulation and metal hypertolerance in some plants. However, the ecological and biological significance of hyperaccumulation is not clear yet. The recent progress of molecular techniques has helped to improve the performance of phytoremediation technology as well as plant adaptation to extreme metallic environments. The knowledge of metal hyperaccumulation physiology has recently developed as a result of the advancement of molecular biology. Molecular technique help to understand the gene regulations system and plant metal homeostasis. This study reviews the recent advances of phytoremediation technology using hyperaccumulator plants addressing both potential and limitations, physiological and molecular aspects and provides a broad overview of most important genes which have been correlated to metals hyperaccumulation and tolerance, evidence of the effect of heavy metal on biomass productions, plant biochemical, antioxidant defence system and discusses the prospects of transgenic plants in phytoremediation of heavy metals.
Received: April 06, 2010;
Accepted: May 23, 2010;
Published: August 21, 2010
In recent years, public concerns relating to ecological threats caused by heavy
metal (HM) have led to intensive research of new economical plants based remediation
technologies. Conventional methods used for reclamation of contaminated soils,
namely chemical, physical and microbiological methods, are costly to install
and operate (Danh et al., 2009). The rapid increase
in population coupled with fast industrialization growth causes serious environmental
problems, including the production and release of considerable amounts of toxic
waste materials into environment (Zhuang et al.,
2007). Over recent decades, the annual worldwide release of heavy metals
reached 22,000 t (metric ton) for cadmium, 939,000 t for copper, 783,000 t for
lead and 1,350,000 t for zinc (Singh et al., 2003).
Vanadium released from fertilizer effluents usually ranges between 16.58-18.44
mg L-1 (Sarma, 2008). However, the combustion
of coal and petroleum-based products is considered as the primary source of
vanadium in the environment (Adriano, 1986). According
to an estimate, in US approximately 2125 ton of elemental vanadium has escaped
in to the environment annkually (Kaplan et al., 1990).
In an ecological research, any metal or metalloid that causes environmental
problem which cannot be biologically degraded should be considered as a heavy
metal. Heavy metals are natural components of the Earth's crust, but in many
ecosystems the concentration of several HMs has reached toxic levels due to
consequence of anthropogenic activities. Fifty three elements fall into the
category of heavy metal till date and defined as the group of elements whose
densities are higher than 5 g cm-3 and recognized as ubiquitous environmental
contaminants in industrialized societies (Padmavathiamma
and Loretta, 2007). The adaptative responses of plants to HM contaminated
environments are efficient processes that include many physiological, molecular,
genetic and ecological traits. These traits give certain species the ability
to survive or hyperaccumulate the toxic metals. Soil pollution caused by metals
is some what different from air or water pollution, because heavy metals persist
in soil much longer periods of time than in other compartments of the biosphere
(Lasat, 2002). Out of the 92 known elements present
on earth crust, only 17 are known to be essential to all living plants for normal
growth and 12 are potentially beneficial required only in trace amounts includes
silver (Ag), cerium (Ce), chromium(Cr), fluoride (F), iodine(I), lanthanum (La),
rubidium (Rb), tin (Sn), serium (Sr), titanium (Ti), vanadium (V) and tungsten
(W) ( Pilon-Smits et al., 2009).
Mechanisms of carcinogenicity has been discussed for metals and classified
arsenic, antimony, beryllium, cadmium, chromium, cobalt, lead, nickel and vanadium
are some metals and metalloids that are carcinogenic to humans or considered
to be carcinogenic to humans by International Agency for Research on Cancer
(Beyersmann and Hartwig, 2008). Toxic heavy metals cause
DNA damage and their carcinogenic effects in animals and humans are probably
caused by their mutagenic ability (Knasmuller et al.,
1998; Baudouin et al., 2002). Exposure to
high levels of these metals has been linked to adverse effects on human health
The hyperaccumulation of heavy metals in some plants has been recorded by many
researchers during last few decades (Barman et al.,
2000) and this has emphasized the importance of further advanced research
in molecular basis of phytoremediation technology. The hyperaccumulation of
heavy metals is depends on the plant species, soil condition (pH, organic matter
content, cation exchange capacity etc.) and types of heavy metal (Barman
et al., 2001; Spinoza-Quinones et al.,
2005; Xian and Shokohifard, 1989; Otte
et al., 1993). In metal biology, it is experimentally proved that
even some metals that are essential for the normal plants growth (such as iron
and copper) may become toxic, depending on the oxidation state, complex form,
dose and mode of exposure (Beyersmann and Hartwig, 2008).
The removal and recovery of heavy metals from contaminated media are of great
importance in terms of protection of the environment as well as abatement of
heavy metal toxicity (Kim et al., 2004). Metals
and their compounds are accumulating up to harmful levels, unlike organic waste
by some living plants. The level of toxic metals (Pb, Cr, Hg etc.) can be reduced
from contaminated media by a number of aquatic plants taken up by the roots
system and transported to the stems and leaves without showing toxicity syndrome
has confirmed by many studies (Rai et al., 1995;
Cardwell et al., 2002). This uptake of metals
largely depends on the type and chemical speciation of metal and habitat characteristics
of plants, i.e., terrestrial, aquatic etc. Hence, plant selection is important
for remediation of contaminated site.
Remediation of metal-contaminated soils became a goal for many research laboratories
in the world. The use of plants in designing low cost treatment system is still
a challenge in environmental managements. Phytoremediation, a new green technology
has been inventoried, in which some metal hyperaccumulator plants were utilized
to decontaminate soil, water and ambient environment (Prasad,
2003) and it is growing without symptoms of toxicity (Reeves
and Brooks,1983; Baker and Brooks,1989; Baker
et al., 1991).
Hyperaccumulator plants represent a resource for remediation of metal polluted
site, as they are able to extract wide range of metals and to concentrate them
in their upper parts with the character of metal tolerance. In some plant species,
the concentrations accumulated in aboveground biomass of metals or metalloids
are more than one and up to four, orders of magnitude higher than in other adjacent
plants (Baker and Brooks, 1989; Reeves
and Baker, 2000). This unique extent of accumulation of heavy metals, have
been reported in a total of approximately 500 plant species to date (Kramer,
2010). The first field trial on Zn and Cd phytoextraction was conducted
by Baker et al. (1991) and now a days, this technology
is receiving considerable attention for clean up of soil contaminated with heavy
metals (USEPA, 2000). Several comprehensive reviews have
been published, summarizing many important aspects of this novel green technology
(Padmavathiamma and Loretta, 2007; Kramer,
2010). The present reviews give general guidance of research trends in last
few decades, focusing the physiological and molecular basis of phytoremediation.
For this review potential publications were searched using Biological Abstracts
(BIOSIS), Biological Sciences (CSA), Biosis Previews (BIOSIS), CAB Abstracts
(CAB International), Plant Science (CSA) and Web of Science (ISI) data bases;
the last round of the search was conducted in June 2010. We used key words that
referred to phytoremediation for searching (different combinations of keywords:
metals *, plants, hyperaccumulator*, physiology*, Phytochelatins biochemical*).
These keywords produced a reasonable output that was then sorted manually; However,
the list is not exclusive. In addition, we checked the reference sections of
all discovered publications for references to other potentially suitable studies
as a cross reference. This review specially focused update information so far
available and provides a critical overview of the present state of the art.
Definitions: The term phytoremediation (phyto meaning plant and the
Latin suffix remedium meaning to clean or restore) refers to a diverse collection
of plant-based technologies that use either naturally occurring, or genetically
engineered, plants to clean contaminated environments (Flathman
and Lanza, 1998). Phytoremediation is clean, simple, cost effective, non-environmentally
disruptive (Wei et al., 2004) green technology
and most importantly, its by-products can find a range of other uses (Truong,
Phytoremediation is an eco friendly approach for remediation of contaminated
soil and water using plants comprised of two components, one by the root colonizing
microbes and the other by plants themselves, which accumulates the toxic compounds
to further non toxic metabolites. Various compounds viz., organic synthetic
compounds, xenobiotics, pesticides, hydrocarbon and heavy metals, are among
the contaminants that can be effectively remediated by plants (Suresh
and Ravishankar, 2004).
TYPES OF PHYTOREMEDIATION TECHNOLOGY
The four different plant-based technologies of phytoremediation, each having
a different mechanism of action for remediating metal-polluted soil, sediment
||Phytoextraction: Plants absorb metals from soil through
the root system and translocate them to harvestable shoots where they accumulate.
Hyperaccumulators mostly used this process to extract metals from the contaminated
site. The recoveries of the extracted metals are also possible through harvesting
the plants appropriately
|| Cost of different remediation technologies (Glass,
||Phytovolatilization: Plants used to extract certain
metals from soil and then release them into the atmosphere by volatilization
||Phytostabilization: In this process, the plant roots and microbial
interactions can immobilized organic and some inorganic contaminants by
binding them to soil particles and as a result reduce migration of contaminants
to grown water
||Phytofiltration: Phytofiltration is the use of plants roots (rhizofiltration)
or seedlings (blastofiltration) to absorb or adsorb pollutants, mainly metals,
from water and aqueous waste Streams (Prasad and Freitas,
Limitations: The application of phytoremediation for pollution control
has several limitations that require further intensive research on plants and
site-specific soil conditions (Danh et al., 2009).
It is generally slower than most other treatment viz., chemical, physical and
microbiological plants with low biomass yields and reduced root systems do not
support efficient phytoremediation and most likely do not prevent the leaching
of contaminants into aquatic system. Environmental conditions also determine
the efficiency of phytoremediation as the survival and growth of plants are
adversely affected by extreme environmental conditions, toxicity and the general
conditions of soil in contaminated lands (Danh et al.,
2009). In phytoremediation technology, multiple metals contaminated soil
and water requires specific metal hyperaccumulator species and therefore requires
a wide range of research prior to the applications. Though the phytoremediation
is cost effective (Table 1), environment friendly, ability
to reclaim heavy metals contaminated site, several limitations also create trouble
in implementing the strategy, e.g., metal must be in bio-available form to plants;
if metals is tightly bound to the organic portions of the soil, some time it
may not be available to plants. Furthermore, if the metals are water soluble,
in nature it will pass by the root system without accumulation.
The phytoremediation of mixed heavy metals contaminated soil have conformant
with some problem e.g., The cadmium/zinc model hyperaccumulator Thlaspi caerulescens
is sensitive toward copper (Cu) toxicity, which is a problem in remediation
of Cd/Zn from soils in the presence of Cu by application of this species. In
T. caerulescens Cu induced inhibition of photosynthesis followed the
sun reaction type of damage, with inhibition of the photosystem II reaction
center charge separation and the water-splitting complex (Mijovilovich
et al., 2009). Despite some limitations, present day phytoremediation
technology are using worldwide and various research laboratories are at present
engaged to overcome the limitations.
PLANTS SELECTIONS CRITERIA FOR PHYTOREMEDIATION
Plant species selection is a critical management decision for phytoremediation.
Grasses are thought to be excellent candidates, because their fibrous rooting
systems can stabilize soil and provide a large surface area for root-soil contact
(Kulakow et al., 2000). The selection of plants
is possibly the single most important factor for fruitful phytoremediation strategy.
The application of indigenous plant species for phytoremediation is often favoured
as it requires less management and acclimatizes successfully in native climate
conditions and seasonal cycle. However, some exotic plant species may perform
better in remediation of specific metals and can be safely used where the possibility
of invasive behavior has been eliminated (USEPA, 2000).
Some important criteria in selecting plant species for phytoremediation are:
||The levels of tolerance with respect to metal known to exist
at the site
||The level of adequate accumulation, translocation and uptake potential
||High growth rate and biomass yield
||Tolerance to water logging and extreme drought conditions
||Availability, habitat preference e.g., terrestrial, aquatic, semi-aquatic
||Tolerance to high pH and salinity
||Root characteristic and depth of the root zone
METAL HYPERACCUMULATORS PLANTS/FAMILIES
Over 500 plant species comprising of 101 families have been reported, including
members of the Asteraceae, Brassicaceae, Caryophyllaceae, Cyperaceae, Cunouniaceae,
Fabaceae, Flacourtiaceae, Lamiaceae, Poaceae, Violaceae and Euphobiaceae. Metal
hyperaccumulation occurs in approximately 0.2% of all angiosperms and is particularly
well represented in the Brassicaceae (Kramer, 2010).
Recently Environment Canada has released a database Phytorem which compiled
a worldwide inventory of more than 750 terrestrial and aquatic plants with potential
value for phytoremediation. The study of Co accumulations in 670 species of
terrestrial plants showed that leaf Co concentration was in general less than
0.2 ppm, with the exception of Ericales, Euasterids and Asparagales, where 0.3-0.5
ppm of Co was measured (Watanabe et al., 2007).
A list of 26 Co hyperaccumulators species belonging to the families of Lamiaceae,
Scrophulariaceae, Asteraceae and Fabaceae has been reported (Baker
et al., 2000). Zn hyperaccumulation was first discovered in 1865
in Noccaea caerulescens (syn. Thlaspi caerulescens) of Brassicaceae
(Reeves and Baker, 2000) and Ni hyperaccumulation, which
was first reported in 1948 in Alyssum bertolonii of Brassicaceae (Kramer,
2010). A member of Crassulaceae Sedum alfredii is the only known
Cd hyperaccumulator outside the Brassicaceae (Deng et
al., 2007). The hyperaccumulation of arsenic (As) has been discovered
in only two species of the Brassicaceae (Karimi et al.,
2009) apart from a number of pteridophytes (Ma et
METAL HYPERACCUMULATOR MODEL PLANTS
Mixed pollution with heavy metals is characteristic for many spill areas and
industrial effluents dumping sites. The danger for the environment and human
health from such sites is large and sustainable remediation strategies are urgently
needed. Phytoremediation seems to be cheap and environmentally sound option
for reclaim the hazardous toxic metals and metalloids. The most important challenge
is how to improve the efficiency of phytoremediation by increasing the accumulation
of metals in plants, or by improving key plant biological traits that should
enhance metal uptake (Wu and Tang, 2009). The heavy
metals accumulation on several plants species have been focused viz., Thlaspi
sp. (Baker et al., 1994), Brassica sp.
(Blaylock et al., 1997; Huang
et al., 1997) and Alyssum (Kramer et al.,
1996). Heavy metal accumulators is increasing steadily (currently more than
500 plant species) and some are presented in Table 2.
|| Examples of some plants and metals they can remediate
Some species are highly metal specific, have a small biomass, slow growth habit
and require careful management for multiplications (Gleba
et al., 1999) which are not suitable for commercial applications.
Thus identification of novel plant species with high biomass yield coupled with
ability to tolerate and accumulate multiple metals has become an important aspect
of phytoremediation research. A multiple metal hyperaccumulator scented geranium
(Pelargonium sp.) has been recently discovered. This plant has an ability
to tolerate and accumulate multiple metals (Cd, Ni and Pb) and maintain normal
metabolic processes (Dan et al., 2000; KrishnaRaj
et al., 2000). Another potential Pb hyperaccumulator perennial shrub
Sesbania drummondii with high biomass yield has been discovered from
southern coastal areas of the United State (Sahi et al.,
2002) was given as evidence for model plants.
In the last few decades many scientists in different parts of the worlds has worked out the metals bioaccumulation potential of various species and some are presented in Table 3 derived through meta-analysis.
Works on physiological aspects of Vetiveria zizanioides has provided
an extensive research foundation which makes this plant a good candidate for
a wide range of phytoremediation purposes (Danh et al.,
|| Examples of some metal hyperaccumulator and their bioaccumulation
|| Concentrations of heavy metals accumulated in Vetiveria
zizanioides roots and shoots (Truong, 1999)
This plant has an ability to accumulate multiple heavy metals in roots and
shoots (Table 4) which has been experimentally determined.
The multiple metal accumulation and metal transfer factors from soil (TFS)
of three wild macrophyte species viz., Ipomea sp., Eclipta sp.
and Marsilea sp. have been studied by Gupta et
al. (2008) and recorded that Ipomea sp. shows transfer factor
(TFS) for Cd, Cu, Mn and Zn, while Eclipta sp. and Marsilea sp.
shows TFS ≥1 for Fe, Cu and Cd. The ratio of metals between soil and plant
parts (TFS) is an important criterion for the selection of model plant species
for phytoremediation and the ratio >1 means higher accumulation of metals
in plant parts than soil (Barman et al., 2000).
Among aquatic plants, Elodea densa showed a high accumulation of mercury
in leaves, stems and roots from the natural sediment enriched with CH3HgCI
(Ochiai, 1987) which make this plant potentials for Hg
PHYSIOLOGY OF METAL HYPERACCUMULATION
Metals influenced the physiology of plants by promote or inhibit the growth.
Some metals that required in high concentration suggest a structural or osmotic
role, while effects at low concentration may indicate a role as cofactor for
specific enzymes. The summary of the beneficial effects of Al, Co, Na, Se and
Si on plants under represented (Fig. 1) adopted from Pilon-Smits
et al. (2009).
Many plants developed Al tolerance characteristics via either apoplastic or
symplastic detoxification mechanisms (Ma et al.,
2001; Pilon-Smits et al., 2009).
In higher plants, Co has been reported to strongly bind to roots and to be
mainly absorbed from the soil solution through passive transport. Co is chemically
similar with nickel (Ni) and these two elements enter inside the cells through
plasma membrane carriers and may be transported by IRT1 (Pilon-Smits
et al., 2009). A strong adsorption of Cd on root apoplast might act
as a driving force to extract the metal from the soil, compete with the symplastic
absorption and contribute to the amount of metals taken up by the hyperaccumulator,
at least in its roots (Redjala et al., 2009).
Se hyperaccumulators namely Stanleya sp. and Astragalus sp. can
accumulate 1000-15000 ppm (0.1-1.5% Se), even from low external concentrations
and this has been enhanced by some specialized transporter. Hyperaccumulators
such as Astragalus bisulcatus, Brassica oleracea have a specific
selenocysteine methyl transferase, lead to accumulation of Se (Tamaoki
et al., 2008)
Toxic metal ions Hg preferentially binds with sulphur and nitrogen rich ligands
(amino acids) and entered inside the cells. Hg effect damage include blocking
functional groups of enzymes, polynucleotides, or transport systems for
nutrient ions, denaturing and inactivating enzymes and disrupting cell and organelle
membrane integrity (Ochiai, 1987). The possible causal
mechanisms of Hg toxicity are changes in the permeability of the cell membrane,
reactions of sulphydryl (-SH) groups with cations, affinity for reacting with
phosphate groups and active groups of ADP or ATP and replacement of major cations
(Kabata-Pendias and Pendias, 1989).
||The mechanisms responsible for the growth promoting effects
of the five beneficial elements Al, Co, Na, Se and Si (Pilon-Smits
et al., 2009)
Heavy metals like copper (Cu) and iron (Fe) can be toxic in excess amount because
of their participation in redox cycles producing hydroxyl radicals which are
extremely toxic to living cells (Stohs and Bagchi, 1995).
Unlike Cu and Fe, Cd is a non-redox metal that is strongly phytotoxic and caused
growth inhibition and plant death. Cd induced changes in lipid profile (Ouariti
et al., 1997) and by affecting the enzymatic activities associated with
membranes, such as the H+- ATPase (Fodor et
al., 1995). Cd is also reported to damage the photosynthetic apparatus
(Siedlecka and Baszynsky, 1993), decrease chlorophyll
content and inhibit the stomatal regulations (Barcelo and
Poschenrieder, 1990). The major storage site for Zn and Cd in plants is
cell wall of roots, vacuoles of epidermis and bundle sheath of leaves (Hu
et al., 2009). The Cd influx and efflux in leaf mesophyll layer depends
on the expression of plasma membrane and tonoplast transporters. Root metal
uptake rates are increased, generally through an increase in VMAX,
without major changes in KM, of root metal uptake rates (Lasat
et al., 1996; Lombi et al., 2001).
Works on Alyssum lesbiacum has given a base of Nickel uptake into vacuoles
from leaf tissue and this was enhanced by the presence of Mg/ATP, presumably
via energisation of the vacuolar H+-ATPase (Ingle
and Fricker, 2008). The model hyperaccumulator Thlaspi caerulescens
is capable to tolerat Zn, Cd and Ni and it has been shown that part of the Ni
is translocated as a stable Ni-NA complex in the xylem sap (Mari
et al., 2006).
The discussion of the effect of heavy metal on biomass productions of metal hyperaccumulation is restricted here to Cd, Pb, Zn, V and Cr.
In metal hyperaccumulators the biomass production level depends on the concentration
of the metals and duration of exposures e.g., The biomass is negatively correlate
with Cd concentration in B. napus, cultured in the nutrient solution and the
reduction in dry weight was significantly higher for the root than the shoot.
Considering the high aboveground biomass production and Cd accumulation in the
shoot, B. napus can be a potential candidate for the phytoextraction
of Cd (Selvam and Wong, 2008).
Biomass production were extensively studied in split pots filled with soil
spiked at 0, 3, 6, 12, 25 and 50 mg Cd kg-1 soil by Selvam
and Wong (2009) and revealed decline in biomass production which established
that cadmium is toxic for biomass production.
Suitable levels of Pb, Zn and Cd could stimulate the biomass production in
A. paniculata and thus, it provides a new plant material for understanding
the mechanisms of stimulatory effect and co-hyperaccumulation of multiple heavy
metal (Tang et al., 2009). However, biomass production
is inhibited in Glycine max and Phaseolus vulgaris in treated
with VOSO4 (Kaplan et al., 1990).
Similarly in E. fluctuans, biomass production was not affected up to
concentration of 2.5 mg L-1 V2O5 when exposed
for 7 days (Fig. 2). However, V2O5 concentration
>2.5 mg L-1 significantly reduced the biomass and increased in
treatment duration enhanced the V2O5 toxicity (Sarma
et al., 2009). The author recorded that after 21 days exposure of
10.0 mg L-1 V2O5 to E. fluctuans approximately
42.47% biomass was decreased (Fig. 2). Similarly in Vallisneria
spiralis L., an increased in treatment duration enhanced the chromium toxicity
and 0.1 μg mL-1 Cr caused 7% decrease in biomass after 48 h
and 64% loss of biomass was recorded after 72 h exposure of 10 μg mL-1
Cr (Vajpayee et al., 2001). The results addressed
that heavy metals toxicity to biomass were concentration and durations
||Biomass production of vanadium treated E. fluctuant
was negatively correlated with concentration of vanadium in nutrient medium
with increased in duration
However, modern transgenic research approach at present going on for introduction
of novel traits into high biomass plants for development of effective phytoremediation
technologies. A number of transgenic high biomass yield plants have been successfully
generated in an attempt to modify the tolerance, uptake or homeostasis of trace
elements (Kramer and Chardonnens, 2001).
Several heavy metals such as Fe, Cu, Co, Mn, Mo and Ni are essential elements
to plant metabolism. In higher concentrations, many heavy metals inhibit plants
biochemical production and this has been extensively studied and reviewed (Fernandes
and Henriques, 1991; Sarma and Sarma, 2007; Sarma
et al., 2009). Photosynthetic pigments of plants belonging to different
groups exhibit differential tolerance to metals (Vajpayee
et al., 2001). Heavy metal substituted chlorophylls and related porphyrins
have been known in vitro for a long time (Kupper et al.,
2000). Many researchers examined the effect of heavy metals on photosynthesis
and observed a decrease in fluorescence (Atal et al.,
1991; El-Sheekh, 1992). Cd induced reduction of
photosynthetic pigment were recorded in two species viz., M. heterophyllum
and P. crispus (Fig. 3a, b and 4a,
b). The highest decrease in chlorophyll a was recorded in
7.34 mg g-1 in M. heterophyllum and 8.09 mg g-1
in P. crispus (at 64 mg L-1 and 96 h) have given as evidence
for the Cd toxicity to chlorophyll.
Cadmium hyperaccumulator Atriplex halimus subsp. schweinfurthii
was sensitive to high Cd results reduction of chlorophyll pigments, stomatal
transpiration and root hydraulic conductivity (Nedjimi and
Daoud, 2009). The Cr uptake by many aquatic plants influenced in biochemical
process results alteration of pigments and amino acids. It has been reported
that Cr (VI) causes toxicity to δ-amionolevulinic acid dehydratase (an
enzyme involved in Chlorophyll biosynthesis) by impairing δ-amiono levulinic
acid (ALA) utilizations (Vajpayee et al., 2000).
Further, Vajpayee et al. (2000) suggested that
Cr (VI) could exchange the Mg from active site of enzyme resulting into phaeophytin
and thus depleted chlorophyll contents in Cr treated plants. Chromium also inhibits
chlorophyll biosynthesis by creating nutrient imbalance (Barcelo
et al., 1986). It has been reported that chromium induced degradation
of carotenoid in some plants while in contrast Vajpayee
et al. (2001) reported that carotenoid contents was increased in
Cr treated V. spiralis. Thus, the effects of heavy metals on carotenoid
contents were plants and metal specific.
||Chlorophyll a, b and carotenoid contents of (mg g-1
FW) M. heterophyllum exposed to various Cd concentrations for (a)
24 and (b) 96 h (Sivaci et al., 2008)
||Chlorophyll a, b and carotenoid contents of (mg g-1
FW) P. crispus exposed to various Cd concentrations for (a) 24 and
(b) 96 h (Sivaci et al., 2008)
Mercuric cations have a high affinity for sulphydryi (-SH). In almost all proteins
contain sulphydryl groups or disulphide bridges, Hg could disturb the normal
functions of proteins in binding in two sites of a protein molecule without
deforming the chain, lead to protein precipitation. (Clarkson,
Mercury affects both light and dark reactions in photosynthesis and caused
inhibitions of electron transport activity, oxygen evolution and quenching of
chlorophyll fluorescence in photosystem II (PS II). Substitution of the central
atom of chlorophyll, magnesium, by mercury in vivo is an important damage mechanism,
because it prevents photosynthetic light harvesting in the affected chlorophyll
molecules and results in the breakdown of photosynthesis (Krupa
and Baszynski, 1995).
GENETIC AND MOLECULAR BASIS OF METAL HYPERACCUMULATION
Metal hyperaccumulation is a fascinating phenomenon, which has interested scientists
for over a century. Hyperaccumulators constitute a group of exceptional plant
species and they possesses genetically inherited traits of metals hyperaccumulation
and tolerance. The understanding of metal hyperaccumulation physiology has recently
improved as a result of the development of molecular tools (Verbruggen
et al., 2009). Transgenic approaches successfully employed to promote
phytoextraction of metals (Cd, Pb and Cu) and metalloids (As, Se) from contaminated
soil by their accumulation in the aboveground biomass involved mainly implementation
of metal transporters, improved production of enzymes of sulphur metabolism
and production of metal-detoxifying chelators metallothioneins and phytochelatins
(Kotrba and Najmanova, 2009).
Recent research revealed that Arabidopsis thaliana has eight genes encoding
members of the type 1 B heavy metal transporting subfamily of the P-type ATPases.
Three of these transporters, HMA2, HMA3 and HMA4, are closely related to each
other and are most similar in sequence to the divalent heavy metal cation transporters
of prokaryotes (Hussain et al., 2004).
Quantitative mRNA in situ hybridization (QISH) in Thlaspi caerulescens
shows that transporter gene expression changes during cadmium (Cd)/zinc
(Zn) hyperaccumulations. Members of the ZIP gene family, a novel metal transporter
family first time identified in plants are capable of transporting a variety
of cations including Cd, Fe, Mn and Zn. The different cellular expression patterns
for ZNT1 and ZNT5 were recorded by Kupper and Kochian (2010)
both belonging to the ZIP family of transition metal transporters. ZNT1 may
function in micronutrient nutrition while ZNT5 may be involved in metal storage
associated with hyperaccumulation. Cadmium induced changes in cellular expression
for ZNT1, ZNT5 and MTP1 could also be part of plants acclimatization to Cd toxicity.
The integral membrane protein Thlaspi goesingense metal tolerance protein
1 (TgMTP1) has been suggested to play an important role in Zn hyperaccumulation.
High levels of TgMTP1 at the vacuolar membrane in shoot tissue of the Zn hyperaccumulator
T. goesingense has been played an important role in both Zn tolerance
and enhanced Zn uptake and accumulation, via the activation of a systemic Zn
deficiency response (Gustin et al., 2009).
An antiporter is an integral membrane protein which is involved in secondary
active transport of two or more ions across a phospolipid membrane in opposite
directions. A recent genomic analysis provides a breakthrough in acquisition
of zinc hypertolerance and hyperaccumulation characters via involvement of Zn2+/H+
antiporter. Metal Tolerance Protein 1 (MTP1) is one of genes present in A.
halleri which encodes a Zn2+/H+ antiporter involved
in cytoplasmic zinc detoxification and developed a zinc tolerance characteristic
(Shahzad et al., 2010).
Plant tissue cultures such as callus, cell suspensions and hairy roots are
extensively used in phytoremediation research as model plant systems. Many studies
have demonstrated that plant tissue cultures are an extremely valuable tool
in phytoremediation research. The results derived from tissue cultures can be
used to predict the responses of plants to environmental contaminants and to
improve the design and thus reduce the cost of subsequent conventional whole
plant experiments (Doran, 2009).
ANTIOXIDANTS DEFENSE SYSTEM IN METAL HYPERTOLERANCE
Phytochelatins are oligomers of glutathione, produced by the enzyme phytochelatin
synthase. They are found in plants, fungi, nematodes and all groups of algae
including cyanobacteria. Phytochelatins act as chelators and are important for
heavy metal detoxification (Ha et al., 1999).
They are abbreviated PC2 through PC11. Plants possess several antioxidative
defense systems to scavenge toxic free radicals in order to protect themselves
from the oxidant stress including that caused by heavy metals. The antioxidative
defense system falls into two general classes: (1) low molecular weight antioxidants,
which consist of lipid-soluble membrane-associated antioxidants (e.g., α-tocopherol
and β-carotene) and water-soluble reductants (e.g., glutathione and ascorbate)
and (2) antioxidative enzymes: Superoxide Dismutase (SOD) Ascorbate Peroxidase
(APX), Catalase (CAT) and Glutathione Reductase (GR).
Glutathione (GSH), a sulfur containing tripeptide, is considered to be the
most important cellular antioxidant involved in cellular defense against toxicants
(Scott et al., 1993) and function directly as
a free radical scavenger. This antioxidant is also the precursor for the phytochelatins
that act as heavy metal binding peptides in plants (Rosen,
2002). GSH levels in plants are known to change under metal stress (Koricheva
et al., 1997).
The Cd treatments significantly enhanced the synthesis of phytochelatins (PCS)
in plants. However, Sun et al. (2010) reported
that the variation in phytochelatins productions in root and shoots in two Cd
treated species viz., R. globosa and R. islandica may be used
as a biomarker of Cd hyperaccumulation and the synthesis of PCS may be related
to an increase in the uptake of Cd ions into the cytoplasm, not the primary
mechanism for Cd tolerance. Similarly the accumulation of Cd has influenced
on the synthesis of phytochelatins in Brassica napus and in the shoot,
the concentration of PC3 and PC4 was higher than the PC2 irrespective of the
quantity of Cd uptake (Selvam and Wong, 2008). This
result gives an evidences that the detoxification of Cd involves higher molecular
weight thiol complexes in the shoot. In Arabis paniculata after Cd exposure
induced formation of PCS and three unknown thiols in the roots, but none were
detected in the shoots (Zeng et al., 2009). Sesbania
sp. responded to Hg induced oxidative stress by modulating non-enzymatic antioxidants
viz., Glutathione (GSH) and Non-Protein Thiols (NPSH) and enzymatic antioxidants:
Superoxide Dismutase (SOD), ascorbate peroxidase (APX) and Glutathione Reductase
(GR). The Sesbania plants were able to tolerate Hg induced stress using effective
antioxidative defense mechanisms (Israr et al., 2006;
Israr and Sahi, 2006). It has been suggested that phytochelatins
play a constitutive role in plant metal tolerance (Zenk,
1996). However, evidence provided by Zenk (1996)
for this role is not conclusive and could just as easily indicate a stress response
(e.g., production of phytochelatins upon exposure to metals).
Phytoremediation is initiated all over the globe and this has considered one of the low-cost novel green technologies. The physiological and molecular basis of metal hyperaccumulation in plants are still in research and development phase. This review has focused on recent evidence that identifies potential molecular mechanism that may be involved in the resistance, tolerance as well as hyperaccumulation of heavy metals. The findings suggest that in some plants ZIP family genes contribute to metal hyperaccumulation and transport, but their individual functions yet to be identified and further intensive research is needed in this concern. The identifications of individual functions of metal transporters will help to develop the knowledge of plants metal homeostasis. Results already obtained have been indicated that the physiological and biochemical responses were plants and metal specific. Identification of novel genes with high biomass yield characteristics and the subsequent development of transgenic plants with superior remediation capacities will be encouraging further research. In depth research study is warranted to find out which plant is maximum resistant and best adapted in particular metallic environment or region. In situ toxicity text could be beneficial for initial identification of particular species.
I am thankful to all colleagues, in particular to current and previous members of my research team, for their supports. I thank to all my Lab mates of Ecosystem Research Laboratory, North-Eastern Hill University. I am grateful to Ms. Idaiarilin Lyndogh Synrem for reading the fist draft of the manuscripts and Mr. Souravjyoti Borah for technical assistant. Funding by a Dr. D.S. Kothari Post Doctoral Fellowship from the University Grants Commission, New Delhi (F. 4-2/2006 (BSR)/13-177/2008 (BSR) is gratefully acknowledged. Finally, I apologize to all colleagues for those parts of their work that were not cited in the manuscripts because of restrictions in space.
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