Minerals Engineering 22 (2009) 10071019

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Minerals Engineering
journal homepage: www.elsevier.com/locate/mineng

Phytomining: A review
V. Sheoran a, A.S. Sheoran b,*, P. Poonia a
a
Department of Zoology, Faculty of Science, Jai Narain Vyas University, Jodhpur, Rajasthan 342 011, India
b
Department of Mining Engineering, Faculty of Engineering, Jai Narain Vyas University, Jodhpur, Rajasthan 342 011, India

a r t i c l e i n f o a b s t r a c t

Article history: Bioharvesting of metals from high biomass crops grown in soil substrates particularly those associated
Received 21 June 2008 with sub-economic mineralization is termed phytomining. It is a recent more advanced technology of
Accepted 4 April 2009 phytoremediation to produce low volume, sulphide-free bio-ore, which can either be safely disposed
Available online 6 May 2009
of or, if the target metal is of sufcient economic value, smelted, and recovered. This technology has
potential application in the mineral industry to return an economic prot by commercial production
Keywords: of metals via cropping. Numerous sites across the globe are enriched with metals that could potentially
Mining
be phytomined. In recent years major scientic progress has been made in understanding the potential
Pollution
Reclamation
for application of this herbage-based technique in the mining industry to develop a good relationship
Wasteprocessing between the industry and community. This paper reviews various aspects of phytomining along with
Precious metal ores the advantages, limitations, and future feasibility of the technology.
2009 Published by Elsevier Ltd.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
2. Factors influencing the phytomining . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
2.1. Plant associated factors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
2.1.1. Hyperaccumulating plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
2.2. Soil associated factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009
2.2.1. Soil pH. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009
2.2.2. Fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009
2.2.3. Chelates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1010
3. Mechanism of metal hyperaccumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
3.1. Solubilization of metal from the soil matrix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
3.1.1. Acidification of the rhizosphere. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
3.1.2. Secretion of ligands by rhizosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
3.1.3. Rhizosphere associated with microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
3.2. Root absorption and transport to shoot . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
3.3. Distribution, detoxification, and sequestration of metal ion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
4. Phytomining of various metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1012
4.1. Nickel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1012
4.2. Thallium. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1012
4.3. Cobalt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1013
4.4. Gold and silver . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1013
5. Economics of phytomining . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1014
6. Advantages of phytomining. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1014
7. Limitations of phytomining . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1015
8. Future scope . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1016
9. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1017
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1017

* Corresponding author. Tel.: +91 291 2611512.

E-mail addresses: as_sheoran@yahoo.com, sheoran@sancharnet.in (A.S. Sheoran).

0892-6875/$ - see front matter 2009 Published by Elsevier Ltd.

doi:10.1016/j.mineng.2009.04.001
1008 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
1. Introduction
Commercial mining of metals is usually performed from ores
that have a high concentration of target metals (above the cut-off
grade) and requires huge capital investment. Ore bodies of this
nature occur only in small localized areas and are being exhausted
due to expanding economics, burgeoning populations and disar-
rayed industrialization. Sub- or low-grade ore occupies much lar-
ger area and percentage of metal is well below the metal content
required to be economically extracted and smelted by conven-
tional techniques.
Most of sub- or low-grade ore bodies are associated with ultra-
mac deposits. Ultramac deposits are formed from magma rich in
olivine and pyroxene minerals. Weathering of ultramac rocks has
produced the ultramac or serpentine soils, characterized by a pH
of 68, low ratio of Ca/Mg in the exchangeable cations and soil
solution, low level of organic matter, nitrogen, phosphorous, potas-
sium, and contains relatively large amounts of nickel, chromium,
manganese, cobalt, titanium, iron, magnesium, and other metals
(Li et al., 2003b; Berazain et al., 2007a; Chaney et al., 2008). These
deposits are scattered throughout the world and usually support a
characteristic ora called endemic ora (Brooks, 1987; Robinson
et al., 1999). These oras on their native metalliferous soils have
constitutive (present in most phenotypes) and adaptive (present
only in tolerant phenotypes) mechanism for accumulation or toler-
ating high metal concentration (Khan et al., 2000). There is a great-
er need to exploit such areas in the future to generate revenue by
extracting saleable metals.
The link between mineralization and plants has been recog-
nized since medieval time, but it was not until the 20th century
that it became possible to analyze plant tissues for these metal
concentrations (Memon et al., 2001). A focal point of soil plant
interactions is the micro ecosystem surrounding the plant roots,
the rhizosphere, characterized by different physical, chemical,
and biological conditions created by the plant roots and its sur-
rounding soil environment. It is well documented that soil solution
is drawn from the roots to the above ground portions of their bio-
mass by plant water uptake, which depends upon the root absorp-
tion factor, a dimensionless parameter describing the xylem/soil
solution metal concentration quotient (Marschner, 1995; Robinson
et al., 2003). Increased understanding of the role of metal extract-
ing plants in circulation of minerals in biosphere has made them
important biotechnological tools in mining process from low-grade
ores.
Plants have shown several response patterns to the presence of
high metal concentrations in the soils. Most are sensitive to
high metal concentration and others have developed resistance,
tolerance, and accumulate them in roots and above ground tissues
such as shoot, ower, stem, and leaves (Barcelo et al., 1994). The
phenomenon of plants accumulating inordinate concentrations of
Potential of phytomining of
areas unable to be exploited
by conventional methods.
Metalliferous soils
Low grade ores
Mill tailings
Reclaimed soil product
Fig. 1. Integrated process for bioharvesting of metals by phytomining.
heavy metals was termed hyperaccumulation. The current crite-
rion to dene a hyperaccumulator is, a plant that can accumulate
metal to a concentration that is 100 times greater than normal
plants growing in the same environment (Brooks et al., 1977; Baker
and Brooks, 1989; Anderson et al., 2003).
Hyperaccumulators efciently extract metals from the metallif-
erous soils and then translocate them to above ground tissues.
After sufcient growth, plant is harvested and left for drying. Dried
plant material is reduced to an ash with or without energy recov-
ery, which is further treated by roasting, sintering, or smelting
methods, which allow the metals in an ash or ore to be recovered
according to conventional metal rening methods such as acid dis-
solution and electrowinning (Fig. 1) (Robinson et al., 1999). Thus
phytomining is the in situ removal of metals from sub-economic
ore bodies or from contaminated mine sites with the additional
aim of recovery of economic amount of metals from the plants
(Chaney et al., 1998; Anderson et al., 1999a).
2. Factors inuencing the phytomining
A successful phytomining process depends on adequate bio-
mass yield and high metal contents in the harvestable parts of
the plants. Many metals are largely immobile and their bioavail-
ability to plant root is restricted. The bioavailability of metals for
plant uptake and biomass can be increased by bringing modulation
in both internal (plant associated) and external (soil associated)
factors.
2.1. Plant associated factors
2.1.1. Hyperaccumulating plants
The term hyperaccumulator was rst applied by Jaffre and his
co-workers when they observed the accumulation of nickel in
Sebertia accuminata (Jaffre et al., 1976), but the present connotation
concerning the concentration of more than 1000 mg/kg (0.1%) of
metal in plant tissues was introduced by Brooks and his co-work-
ers in the year 1977, when they examined the Ni concentration in
Homalium and Hybanthus from different sites throughout the
world. For most elements the threshold concentration is
1000 mg/kg (0.1%) dry mass, except for zinc (10,000 mg/kg), gold
(1 mg/kg), and cadmium (100 mg/kg) (Brooks et al., 1977,
1998). Hyperaccumulating plants are taxonomically widespread
throughout the plant kingdom. Approximately 400 plant species
from at least 45 plant families have been reported to hyperaccu-
mulate metals, most of which are nickel hyperaccumulators occur-
ring in ultramac areas all over the world (Table 1).
Baumann (1885) was the rst to report the small herbaceous
biennial Thlaspi calaminare and Viola calaminaria, found near Aa-
chen, Germany, with a foliar zinc concentration of around 1%
Bioextraction / phytoextraction of
metals for commercial gain.
Cropping
Harvesting
Drying
Ashing
Small volume of bio-ore
Smelt metal
 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
Table 1
Lower limit for hyperaccumulation of various metals and, number of known hyperaccumulators with their families (Baker et al., 2000; Reeves and Baker, 2000; Reeves, 2003,
2006).
Element Lower limit for hyperaccumulation (mg/kg)
Arsenic 1000
Cadmium 100
Cobalt 1000
Copper 1000
Golda 1 Brassicaceae
Leada 1000
Manganese 10,000
Nickel 1000
Selenium 100
Silvera 1 Brassicaceae
Thallium 100
Uraniuma 1000
Zinc 10,000
a
For induced hyperaccumulation.
(10,000 mg/kg) on a dry weight basis. This concentration was
about two orders of magnitude higher than the mean concentra-
tion of zinc in other plants. Two Italian scientists Minguzzi and
Vergnano (1948) reported a small herb named Alyssum bertolonii
growing on ultramac soils in Tuscany Italy, had a tissue nickel
concentration of 0.79% (7900 mg/kg dry wt). This plant was grow-
ing on soil with a nickel concentration of 0.42% (4200 mg/kg),
hence the plant showed an ability to accumulate metal to a con-
centration greater than that in the soil substrate (Robinson et al.,
1997b).
Natural metal accumulating plants release metal chelating
compounds (phytochelators/phytosiderophores) to the rhizo-
sphere which increases the bioavailability of metals that are tightly
bound to the soil and helps to carry them into plant tissues (Eapen
and DSouza, 2005). Phytochelators are usually low molecular
weight organic compounds such as malic, malonic, oxalic acids,
acetic acid, succinic acid, sugars, oxalic acids, amino acids and
phenolics that can change the metal speciation and thus metal bio-
availability (Cieslinski et al., 1998; Ma et al., 2001; Nascimento
et al., 2006). Some of the metal chelating compounds such as
mugenic acid and avenic acids are released in response to nutrient
metal deciency which increases the bioavailability of metals as in
case of iron (Ma and Nomoto, 1996), aluminium (Pellet et al.,
1995), and zinc (Cakmak et al., 1996) and helps to carry them into
plant tissues. Metal chelate complexes may also be transported
across the plasma-membrane as reported for ironphytosidero-
phore in cereals (Romheld, 1991).
The rhizosphere provides a complex and dynamic microenvi-
ronment where microorganisms such as free living as well as sym-
biotic rhizobacteria and mycorrhizal fungi, in association with
roots form unique communities that have considerable potential
for detoxication of hazardous waste compounds. Their interaction
can improve metal bioavailability in rhizosphere through the
secretion of proton, organic acids, phytochelatins (PCs), amino
acids, and enzymes (Idris et al., 2004; Yang et al., 2005). Fungal
symbiotic associations have the potential to enhance root absorp-
tion area and stimulate the acquisition of plant nutrients including
metal ions (Khan et al., 2000). Abou-Shanab and his co-workers re-
ported that concentration of extractable Ni increased from 2.2 to
2.6 mg/kg when the soil was inoculated with M. arabinogalactano-
lyticum AY509224 (Abou-Shanab et al., 2006).
2.2. Soil associated factors
2.2.1. Soil pH
Soil pH affects the solubility of trace elements, and hence is a
major factor inuencing the bioavailability of elements in the soil
1009
No. of hyperaccumulators Families of hyperaccumulators
5 Pteridaceae
2 Brassicaceae, Asteraceae, Chenopodiaceae
30 Lamiaceae, Scrophulariaceae
34 Cyperaceae, Lamiaceae, Brassicaceae, Poacea, Scrophulariaceae
14 Compositae, Brassicaceae
11 Apocynaceae, Cunoniaceae, Proteaceae
320 Brassicaceae, Cunoniaceae, Flacortiaceae, Violaceae, Euphorbiaceae
20 Fabaceae, Brassicaceae
1 Brassicaceae
Brassicaceae
16 Brassicaceae, Crassulaceae, Leguminosae
for plant uptake. It depends not only on the plant species able to
grow in serpentine or calamine soils but also, on the edaphic con-
ditions at the time which may have considerable variation. Horn-
burg and Brummer (1993) reported that as pH decreased below
6.5 and 5.3, the proportions of soluble content of Cd and Zn in-
creased. Similarly when pH decreased below 4.5 and 3.5 the solu-
bility of Cu and Pb also increased. However the mobility of arsenic
decreases with decreasing pH (Irgolic, 1994). pH of rhizosphere of
some plants is often up to 2 pH units below the surrounding soils
which indicates the role of pH in metal solubility. The amount of
metal extracted is proportional to the concentration and pH of
the extractant.
Possible amendments for lowering the pH include ammonia
containing fertilizers, organic and inorganic acids, and elemental
sulphur (S). There are limits to the degree to which pH can be low-
ered. Most of the plant species can survive in a relatively narrow
pH range, pH 4.5 being the lower limit (Salisbury and Ross,
1978). Robinson et al. (1999) observed effect of MgCO3, CaCO3,
and sulphur on nickel and cobalt uptake by Berkheya coddii and
found that MgCO3 increased soil pH from 6.9 to 8.7, caused a sig-
nicant (P < 0.05) decrease in plant uptake of both Ni and Co. The
addition of S caused decrease in soil pH from 6.9 to 5.5, hence in-
creased the plant uptake of both the metals. Thus acid extractants
have the advantage of extracting more metal.
pH of the rhizosphere is species and probably age-dependent, it
is impossible to state a single value for all plants (metallophytes).
From a given extraction value at pH 7, the amount of extractable
metal at lower pHs can be calculated by
M m k1 mk2  P2
where m is the [M] (lg/g) extracted at pH 7; P is the pH of the
extractant solution, k1 and k2 are constants.
2.2.2. Fertilizers
The agronomy of producing high yields of phytoextraction crops
is central to success of phytomining technology. For this one must
characterize fertilization besides pH optima. Addition of fertilizers
such as nitrogen, phosphorus, potash to soil, decreases the soil pH
hence increases the metal bioavailability and also supports the
growth of plants. Robinson et al. (1997b) reported that with the
addition of fertilizers, the maximum annual biomass of Alyssum
bertolonii was about 300% above control values. The highest
individual increase reported was 130% with N alone and highest
combined increase of 308% was with N + P + K. Similar observa-
tions were reported for B. coddii where addition of N increased Ni
1010 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019

Table 2
Some specic plant hyperaccumulators with their metal concentration and denite biomass (kg/ha).

Elements Plant species Concentration mg/kg dry Biomass kg/ References

matter ha
1 Cadmium Thlaspi caerulescens 3000 (1) 4000 Reeves et al. (1995, 2001), Brooks (1997)
2 Cobalt Haumaniastrum robertii 10,200 (1) 4000 Brooks (1977), Brooks (1997)
Berkheya coddii Robinson et al. (1999), Keeling et al.
(2003)
3 Copper Haumaniastrum 8356 (1) 5000 Brooks (1977), Brooks (1997)
Katangense Baker and Walker (1990)
Ipomea alpine
4 Gold (induced-hyper- Brassica juncea, Berkheya coddii 10 (.001) 20,000 Anderson et al. (1999a,b)
accumulation) Chicory Lamb et al. (2001)
C. linearis Msuya et al. (2000)
Gardea-Torresdey et al. (2005)
5 Lead Thlaspi rotundifolium 8200 (5) 4000 Reeves and Brooks (1983)
6 Manganese Macadamia neurophylla 55,000 (400) 30,000 Jaffre (1980), Brooks (1997)
7 Nickel Alyssum bertolonii 13,400 (2) 9000 Minguzzi and Vergnano (1948)
Berkheya coddii 17,000 (2) 18,000 Morrey et al. (1992)
Streptanthus polygaloides Brooks (1997)
Nicks and Chambers (1995, 1998)
8 Silver B. juncea Harris and Bali (2008)
Medicago sativa
9 Thallium Iberis intermedia 4055 (1) 8000 Brooks (1997), Leblanc et al. (1999)
Biscutella laevigata Anderson et al. (1999b)
10 Uranium Atriplex confertifolia 100 (0.5) 10,000 Cannon (1964)
11 Zinc Thlaspi calaminare 10,000 (100) 4000 Baumann (1885), Brooks (1997)

NB: values in parentheses are mean concentrations usually found in non-accumulator plants.

content from 2500 mg/kg to 4200 mg/kg in leaves (Robinson et al.,
1997a). LHuiller et al. (1996) supplied over 1000 kg P/ha to ser-
pentine soil to obtain a full yield of maize (Zea mays L.) where as
Li et al. (2003a) found that 100 kg P/ha to serpentine soils gave a
full yield of Alyssum murale. Higher N fertilization increased Ni,
Cd, and Zn accumulation along with the yield (Keller et al., 2003,
2005; Keller and Hammer, 2004; Chaney et al., 2008).
Serpentine soils are low in Ca and high in Mg, hence repeated
harvest and removal of the biomass in phytomining would require
Ca fertilization. Bennett et al. (1998) studied the effect of fertiliza-
tion on three hyperaccumulator species, A. bertolonii, Streptanthus
polygaloides, and Thlaspi caerulescens. The use of fertilizers is not
at the expense of lowered metal concentrations. They found that
fertilization with nitrogen, phosphorus, and potassium doubled an-
nual biomass production without reducing shoot Ni concentration.
Schremmer et al. (1999) reported the effect of ammonium sulfate
fertilization (equal to 100 mg N/kg) on the accumulation of Cd
and Zn by willow from non-calcareous moderately contaminated
soil (1.92.4 mg Cd/kg). The Cd and Zn concentrations in willow in-
creased up to 22-fold (up to 4.5 and 400 mg/kg, respectively).
Schmidt (2003) also reported the application of ammonium sulfate
(equal to 500 kg N/ha) to a soil contaminated with 20 mg Cd/kg,
planted with perennial ryegrass and found that the Cd concentra-
tion of crop increased 1.5-fold. Similarly ammonium sulfate fertil-
izers when added to soil with very low Zn and Ni concentrations
(38 and 56 mg/kg), doubled their crop concentration to 204 mg/
kg and 100 mg/kg, respectively without affecting plant yield. Li
et al. (2003b) suggests soil fertility management an important fac-
tor for commercial phytomining.
2.2.3. Chelates
Plants with both a high biomass production and high metal up-
take capacity are needed to phytomine the metals from the metal-
liferous soils (Romkens et al., 2002). Metal uptake from soil is
accomplished by roots that take up metals from soil solution. To
enhance metal solubility, natural hyperaccumulators are believed
to excrete organic acids or lower the soil pH in the rhizosphere.
A general characteristic of these species is their slow growth and
limited biomass production. As total metal extraction is the prod-
uct of biomass and metal concentration in tissue, so the speed of
metal extraction is accordingly limited (Ebbs et al., 1997). The abil-
ity to cultivate a high biomass plant with improved uptake speed
of metal extraction capacities, the addition of chelates has been
proposed.
Chelates are high molecular weight compounds (aminopoly-
carboxylic acid) extract a wide variety of metals such as Cu, Cd,
Zn, Pb, Ni, Au, Ag, etc. (Barona et al., 2001). Chelating agents have
a capacity to form water soluble metal organic complexes (Mar-
tell and Calvin, 1958). The formation of metal chelate complexes
bring metals into solution through desorption of sorbed species
and allowing further dissolution of Fe and Mn oxides. The disso-
lution of precipitated compounds continues until equilibrium is
reached between the complexed metal, free metal, and insoluble
metal fraction (Prasad and Frietas, 2003). This approach makes
use of high biomass crops and, even nonhyperaccumulators such
as Z. mays, Brassica juncea, V. zizanoides, and Helianthus annus are
induced to take up large amounts of metals by enhancing the
metal solubility and, bringing the immobile metal in the mobile
form by chelate treatments. Various reported chelates are
EDTA (ethylenediaminetetraacetic acid), HEIDA (hydroxyethyli-
minodiacetic acid), NTA (nitrolenetriaceticacid), CA (citric acid),
DTPA (diethylenetriaminepentaacetic acid), EDDS (ethylene-
diaminedisuccinicacid), and thiocyanates (Kayser et al., 2000;
Chiu et al., 2005; Luo et al., 2005; Nowack et al., 2006; Evangelou
et al., 2007).
Citric acid (CA) has been reported to be the most effective che-
lating agent in increasing many fold uranium (U) concentrations in
the shoots of selected plant species. Huang et al. (1997) added
20 mmol/kg CA in the soil to increase uranium uptake in various
plant species viz. Indian mustard (B. juncea), Chinese cabbage
 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
(B. chinesis), Chinese mustard (B. narinosa), Cow pea (P. sativum),
Bush bean (P. vulgaris), and Corn (Z. mays). Indian mustard and Chi-
nese cabbage showed best results of metal uptake (100-fold and
900-fold, respectively). Ebbs et al. (1998) added 10.5 mg CA/kg to
a soil that contained 310 mg U/kg which enhanced U solubility to
73-fold, this strong mobilization of U by CA was due to the forma-
tion of citrate- uranyl complexes. Similar observations were ob-
served for U in Indian mustard by Chang et al. (2005).
Robinson et al. (1997a) while working on B. coddii for phytomin-
ing of nickel after adding EDTA and CA to the substrates, reported
decrease in shoot nickel concentration despite an increase in the
concentration of soluble nickel in the rhizosphere. This loss was
attributed to the competition with plants own nickel binding
agents, thereby diffusing nickel downwards to the plants root sys-
tem. Robinson et al., 1999 also reported similar observations by
NTA and DTPA for nickel but cobalt uptake was unaffected. Meers
et al. (2005) however reported increase in Ni uptake while working
on sunower (H. annus) from 1.8- to 2.8-fold by adding 1.6 mmol/
kg EDTA and EDDS, NTA application also increased Ni uptake by
2.5-fold. Induced hyperaccumulation of gold has also been re-
ported in various plant species viz. B. juncea, Z. mays, Daucus carota,
B. coddii, Chicory (Chichorium spp.) by adding thiosolutions (thiocy-
anate, thiosulphate, and thiourea) and sodium cyanide (Anderson
et al., 1999b, 2005; Msuya et al., 2000; Lamb et al., 2001; Gar-
dea-Torresdey et al., 2005). Application of appropriate chelating
agent for a particular metal is required to enhance phytoextraction
of metal.
3. Mechanism of metal hyperaccumulation
Metal hyperaccumulation is a complex and rare phenomenon
that occurs in plant species with high metal uptake capacity. This
process involves several steps (Fig. 2).
Fig. 2. Mechanism of major processes involved in metal hyperaccumulation by
plants.
1011
3.1. Solubilization of metal from the soil matrix
Out of the total metal concentration in soil matrix, metals are
present in three forms: available form, potentially available form,
and unavailable form. In available form metals are available to
organisms at any time. In potentially available form metal is avail-
able once the available fraction has been removed. Metals in
unavailable form have extremely low solubility and are chemically
bound to an organic or silicate matrix (Robinson et al., 1999, 2003).
Plants use various methods to desorb metals from the soil matrix.
3.1.1. Acidication of the rhizosphere
Acidication of the rhizosphere and exudation of carboxylate
are considered potential targets for enhancing metal accumulation.
Secretion of H+ by roots could acidify the rhizosphere and increase
the metal dissolution. The proton extrusion of the roots is operated
by plasma-membrane H+ ATPase and H+ pumps (Ghosh and Singh,
2005).
3.1.2. Secretion of ligands by rhizosphere
Plant roots secrete various ligands such as organic acids (malon-
ic and oxalic acids), metal chelating compounds (phytosidero-
phores), and enzymes (reductase). These act as chelating agents
and enhance metal desorption from soil thus increasing the bio-
availability of metals in the soil solution and a greater accumula-
tion in plants (Ma et al., 2001; Callahan et al., 2006).
3.1.3. Rhizosphere associated with microorganisms
Rhizosphere is populated by large concentrations of microor-
ganisms which mainly consist of bacteria and mycorrhizal fungi.
These root-colonizing bacteria and mycorrhizae have been shown
to catalyze redox transformations leading to increase in soil metal
bioavailability (Idris et al., 2004; Chen et al., 2005).
3.2. Root absorption and transport to shoot
Soluble metals can enter into the root symplast by crossing the
plasma-membrane of the root endodermal cells or they can enter
the root apoplast through the space between cells. While it is pos-
sible for solutes to travel up through the plant by apoplastic ow,
the more efcient method of moving up the plant is through the
vasculature of the plant, called xylem. To enter the xylem, solutes
must cross the casparian strip, a waxy coating, which is imperme-
able to solutes, unless they pass through the cells of the endoder-
mis. Therefore, to enter the xylem, metals must cross a membrane,
probably through the action of membrane pump or channel. This
type of transport of metals which takes place in xylem after they
cross the casparian strip is called symplast transport. It is more
regulated due to the selectively permeable plasma-membrane of
the cells that control access to the symplast by specic or generic
metal ion carriers or channels (Gaymard, 1998; Hall, 2002).
Once loaded into the xylem, the ow of xylem sap will transport
the metals to the shoots. Several classes of proteins have been
implicated in heavy metal transport in plants. These include the
heavy metal or CPx-type ATPase, the natural resistance- associated
macrophage protein (Nramp) family of proteins, the cation diffu-
sion facilitator (CDF) family proteins, zinciron permease (ZIP)
family proteins, etc. Xylem loading is operating through cation
proton antiport, cation-ATPases or ion channel (Williams et al.,
2000; Yang et al., 2005).
3.3. Distribution, detoxication, and sequestration of metal ion
At any point along the pathway, metal could be converted to a
less toxic form through chemical conversion or by complexation
with organic acid such as malate, citrate, and nicotianamine (Mari
1012 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
et al., 2006; Gendre et al., 2007). Various oxidation states of heavy
metals have very different uptake, transport, and detoxication
characteristics in plants. Once the metals are translocated to shoot
cells, they are stored in cellular locations such as trichone (apoplast
tissue), epidermis, mesophyll, cell wall, etc., where the metal will
not damage the vital cellular processes (Shah and Nongkynrih,
2007). The nal step for accumulation of most of the metals is
the sequestration of the metal away from any cellular processes
it might disrupt. Sequestration usually occurs in the plant vacuole,
where the metal/metal-ligand must be transported across vacuolar
membrane. Metal binding proteins such as metallothioneins (MTs)
and phytochelatins (PCs) in plants play important role in seques-
tration and also enhance metal tolerance and accumulation. Metal
such as Ag (I), Cu (II), and Ni (II) are sequestered by bonding with
organic sulphur (R-SH) on the cysteine residues of these peptides.
MTs and PCs complex the metal ions to inactivate and, transport
them into vacuoles for long-term sequestration (Eapen and
DSouza, 2005).
4. Phytomining of various metals
4.1. Nickel
Ultramac or serpentine soils contains potentially good amount
of Ni at various global locations. In these soils, Ni is usually present
at concentrations between 1000 and 7000 mg/kg, well below the
minimum Ni concentration required for modern mining technolo-
gies (<30,000 mg/kg), but adequate to supply to Ni hyperaccumu-
lators. Thus, there is an opportunity to commercially phytomine
such soils to produce biomass ash much richer in Ni than common
Ni ores (Chaney et al., 1998; Brooks et al., 1998). Severne and
Brooks (1972) reported 1600 mg/kg Ni in dried leaves of Hybanthus
oribundus, a hyperaccumulator of Ni, growing in associated soil of
Australian elds with only 700 mg/kg Ni. In a survey of gold elds
of Western Australia, Cole (1973) reported excess of one percent
nickel concentration in H. oribundus.
Chaney (1983) and Baker and Brooks (1989) reported the
hyperaccumulator plants for metal mining from sub-economic
ore bodies but it was not until the mid 1990s that eld trial
was carried out. The rst eld trial for phytomining was reported
by then US Bureau of the Mines, Reno, Nevada (Nicks and
Chamber, 1995, 1998; Chaney et al., 1998) on a naturally occur-
ring strain of S. polygaloides which is a species known to hyperac-
cumulate nickel. The serpentine soil at the site contained normal
range of about 3500 mg/kg Ni. The total dry biomass obtained
was 10,000 kg/ha, containing Ni 10,000 mg/kg. It was reported
that a net return of $513/ha to the grower could be achieved
assuming a nickel price of $US 7.65/kg, and also a quarter of
the energy of combustion of biomass could be turned into
electricity for a yield of $US 131/ha and, nally the return to
the grower would be half of the gross yield of $US 765 for metal
plus the energy yield of $US 131. Brooks and Robinson (1998)
however pointed out limitations on the use of an incinerator to
produce steam for power generation from the hyperaccumulating
crops. As harvesting would occur over a fairly short space of time
and therefore the power plant should be situated in the area
where other waste might be used as a feed stock to keep the plant
going the rest of the year.
Second eld trial for phytomining of nickel was carried out by
Robinson et al. (1997a) on hyperaccumulator A. bertolonii. In the
eld trial plants were fertilized with N + P + K combinations over
a period of 2 years. They reported biomass yield of 9000 kg/ha of
8000 mg/kg Ni content in dry matter (in ash 110,000 mg/kg) gave
a conservative value of 72 kg Ni/ha of worth $US 539 of that time
world price of Ni. B. coddii was also used for another eld trial for
phytomining of nickel. They obtained a biomass yield of 22,000 kg/
ha containing about 5500 mg/kg (0.55%) nickel. This would have
provided 121 kg/ha of nickel, together with potential energy yield
of $US 288, total earnings of worth $US 871. The value 22,000 kg/
ha/yr is among the highest reported for any natural hyperaccumu-
lator species, and more than twice the biomass production of A.
bertolonii. Brooks et al. (1999) reported B. coddii to be one of the
best candidates for phytomining of nickel as it has a high biomass,
easy to grow from seed; perennial and tolerant of severe climatic
conditions such as frost and cool weather. Anderson et al.
(1999b) proposed that a yield of 100 kg/ha of Ni could be achiev-
able with B. coddii at many sites world wide with applied fertilizers
and adequate moisture. At current world price (May 2008), it will
be worth of $2268 (Table 3).
Li et al. (2003b) reported shoot Ni concentration as high as
22,000 mg/kg and biomass as high as 20,000 kg/ha in selected
parental lines of A. murale and Alyssum corsicum in their breeding
program. They further reported Ni metal recovery from the ash
of Alyssum biomass by placing 500 kg of ash in a revert bag added
to an electric arc furnace, at the Inco Ltd., smelter complex
(Sudbury, Ontario, Canada). Ni was very readily recovered from
the ash. Ljung and Nordin (1997) reported that for processing of
biomass to phytoextract Cd and Zn, greater volatility requires
stronger emission controls to separate these metals from the
remaining biomass ash components by fractional distillation.
Koppolu and Clements (2003) and Boominathan et al. (2004)
suggested pyrolysis as a technique for separating heavy metals
from bio-ores/hyperaccumulators.
The mining company Anglo-American Platinum Corporation
(Amplats) at Rustenberg, S. Africa at the site of rening operations
carried out recovery process for Ni, Pt and several other metals. The
land near the rening operations was contaminated with nickel
from a number of sources. In 1996 Amplats commissioned a pro-
ject to investigate the feasibility of using B. coddii to phytoremedi-
ate this area. The biomass of B. coddii was collected and incinerated
to produce a bio-ore and smelted. The crude metal was then re-
ned and cast into small ingots containing predominantly nickel.
In carrying out this process, the Amplats team was the rst in
the world to show that metal from a hyperaccumulator crop could
effectively be recovered in a relatively pure form. Amplats feed the
dry biomass directly in metal smelter. In this way the resulting bio-
ore was incorporated into bulk metal ore and contaminating metal
from outside the renery turned into a valuable product (Anderson
et al., 1999b).
4.2. Thallium
The growing demand of thallium coupled with the relative
unavailability of this metal in nature, makes it the fourth most-pre-
cious metal on the earth from economic point of view after gold,
platinum, and palladium. It is extremely toxic metal with a crustal
abundance of about 07 mg/kg (ppm). Elevated concentration of
thallium however remains in the environment from both natural
and man-made sources. A signicant property of thallium is that
it is readily taken up and accumulated by some plant species,
hence can be used for recovery of the metal (Anderson et al.,
1999b; LaCoste et al., 2001).
Leblanc et al. (1999) discovered unusually high hyperaccumula-
tion of thallium by the brassicaceous Iberis intermedia (candyduft)
and Biscutella laevigata growing over lead/zinc mine tailings at Les
Malines (Les Avinieres) near Montpellier, France. Tailings typically
contained Zn 15,000 mg/kg, Pb 5000 mg/kg, and locally up to
40 mg/kg (mean 10 mg/kg) Tl. It was found that Iberis contained
up to 4000 mg/kg Tl in the whole plant dry matter with a biomass
of 10,000 kg/ha and the Biscutella over 14,000 mg/kg with a bio-
mass 4000 kg/ha. Similar results were also reported in eld trials
 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019 1013

Table 3
Concentration of trace metals that would be needed in plant to provide a crop with a gross value of $1000 per hectare.

Metals Price of metals May 2008 ($/kg) Metal content (mg/kg) in biomass yield (kg/ha) Price of metals January 2009 ($/kg)
1000 10,000 15,000 20,000 30,000
Platinum 73,555 13.6 1.4 0.9 0.7 0.5 34,686
Gold 31,753 31.5 3.2 2.1 1.6 1.0 32,445
Palladium 15,414 65 6.5 4.3 3.3 2.2 6918
Thallium 4650 215.1 21.5 14.4 10.8 7.2 4850
Silver 614 1628 162.8 108.5 81.4 54.3 441
Uranium 132 7560 756 504 378 252 104
Cobalt 108 9257 925.7 617.1 462.8 308.5 38
Tin 23.9 41,928 4192.8 2795.2 2096.4 1387.6 12
Nickel 22.7 44,091 4409.1 2939.4 2204.5 1469.7 11.6
Cadmium 8.3 120,918 12091.8 8061.2 6045.9 4030.6 2.2
Copper 8.2 122,249 12224.9 8149.9 6112.5 4074.9 3.3
Manganese 3.1 323,624 32362.4 21574.9 16181.2 10787.5 1.4
Zinc 2.1 480,770 48077.0 32051.3 24038.5 16025.6 1.3
Lead 2.0 502,512 50251.2 33500.8 25125.6 16750.4 1.2

Sources: gold and silver prices provided by KITCO Bullion dealers (http://www.kitco.com).
Platinum group metals prices provided by Johnson Mattey (http://www.platinum.mattey.com).
Base metal (Cd, Pb, Ni, Sn, and Zn) prices provided by London metal exchange.
Co, Cd, U, and Mn metal prices provided by http://www.metalprices.com.
Thallium metal price provided by US Ecological survey, Mineral Commodities, January 2008 and January 2009.

in New Zealand by Anderson et al. (1999b)with a biomass of
10,000 kg/ha Iberis. The hyperacumulator plant produced about
700 kg/ha of bio-ore containing 8 kg of Tl worth $US 2400 at that
time world price of $US 300/kg. To be economic at that time world
price, phytomining should be able to produce $US 500/ha irrespec-
tive of additional revenue from incineration of the biomass to gen-
erate electricity. For such purpose, a crop with biomass of
10,000 kg/ha would have to contain at least 170 mg/kg Tl in dry
matter, a level attainable with I. intermedia. Whereas in B. laevigata,
at 4000 kg/ha, less than half of the biomass of Iberis but three times
more Tl concentration, to achieve $US 500/ha, Biscutella needs on
an average of about 425 mg/kg Tl and it was reported that about
39% of the plants exceeded this threshold concentration. The po-
tential yield of saleable power by incineration of biomass could
add $US 131/ha to that of Iberis crop and $US 53/ha to that of Biscu-
tella using assumptions of Nicks and Chambers (1998).
4.3. Cobalt
Robinson et al. (1999) while phytomining cobalt and nickel re-
ported that addition of sulphur at the rate of 5000 mg/kg in the
substrate increased cobalt concentration to 290 mg/kg in the dry
mass of plant B. coddii, representing ve-fold increase relative to
the controls (56 mg/kg), whereas for nickel the increase was
three-fold. Addition of elemental sulphur has the potential to en-
hance metal crops when the plants are grown on soils with a sol-
uble metal fraction less than that required for maximum plant
uptake sulphur addition would be of relatively low cost than EDTA.
Keeling et al. (2003) investigated the Ni hyperaccumulator B.
coddii to phytoextract Co and Ni from articial metalliferous med-
ia. They observed that cobalt was readily taken up with and with-
out the presence of Ni, but Ni uptake was inhibited by the presence
of an equal concentration of cobalt. The bioaccumulation coef-
cients of Ni and Co for single element substrates (total metal con-
centration of 1000 mg/kg) were 100 and 50, respectively. Elevated
Co concentrations signicantly decreased the biomass production
of B. coddii (due to phytotoxicity) without affecting the bioaccumu-
lation coefcients. The mixed NiCo substrate produced bioaccu-
mulation coefcient of 22 for both Ni and Co. When grown in the
presence of both Ni and Co (mixed substrate), the bioaccumulation
coefcient of each metal were reduced as compared to single ele-
ment substrate. The crop yields for single element substrates were
approximately 14.5 kg Ni/ha and 12.6 kg Co/ha. By comparison, the
extrapolated metal yields for the mixed NiCo substrate were
0.9 kg Ni/ha and 3.1 kg Co/ha, reduction in Ni and Co bioaccumula-
tion coefcients by 95% and 75%, respectively. It was nally con-
cluded and suggested that due to interference relationship
between Ni and Co, there is limitation to phytomining where both
metals are present.
4.4. Gold and silver
Gold has been suggested as a likely candidate for phytomining.
Tailing areas usually contains residual gold in very low concentra-
tions, whereas relatively high concentration has been observed in
spent heap leach pads and waste dumps. Plants do not normally
accumulate gold; the metal must be made soluble before uptake
can occur. The residual gold could be extracted using induced
hyperaccumulation if the substrates were amenable to plant
growth. The concentration of gold that can be induced into a plant
is dependant upon the gold concentration in the soil on which the
plant is growing. Anderson and his co-workers showed that
approximately 2 mg of gold per kg of soil is needed by considering
a soil prole of 20 cm depth to achieve 100 mg/kg of plant dry
mass (Anderson et al., 2003). Various researches have shown that
uptake of gold can be induced using lixiviants such as sodium cya-
nide, thiocyanate, thiosulphates. In an induced hyperaccumulation
operation of gold, the geochemistry of the substrate (pH, Eh, and
chemical form of gold) will dictate the choice of the solubilizing
agent necessary to affect the uptake of the precious metal. For
low-pH sulphide tailings, gold is made soluble by thiocyanate
and for high-pH unoxidised sulphide tailings gold is soluble with
thiosulphate (Anderson et al., 1999b).
Since the turn of 20th century, there have been many reports of
gold accumulation by plants, in particular trees. Work conducted
over 30 years in Canada by Warren and Delavault (1950) from
the University of British Columbia showed that common conifers
could accumulate up to 0.02 mg/kg gold over gold mineralization.
Dunn (1995) reported a background level of gold in plants of
0.0002 mg/kg dry weight, although this author stated that values
up to 0.1 mg/kg could be found. Hyperaccumulation of gold was
dened in 1998 as accumulation greater than 1 mg/kg, this limit
being based upon a normal gold concentration in plants of only
0.01 mg/kg (Anderson et al., 1998a,b).
Anderson et al. (1998b) induced Indian mustard ( B. juncea)
with ammonium thiocyanate at the rate of 0, 80, 160, 320, and
1014 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
640 mg/kg dry substrate weight in pots containing an articial
5 mg/kg nely disseminated gold rich material, analogous to a nat-
ural, oxidized, non sulphidic ores. Hyperaccumulation of Au was
achieved above a thiocyanate treatment level of 160 mg/kg and
yield up to 57 mg/kg Au. A similar experiment with B. juncea grown
in a medium containing 5 mg/kg Au prepared from nely pow-
dered native Au (44 lm) and treated with ammonium thiocyanate
at an application rate of 250 mg/kg also conrmed the results
(Anderson et al., 1999b). Anderson et al. (2003) also predicted that
a harvested crop of 10,000 kg/ha biomass (dry) with gold concen-
tration of 100 mg/kg, which would yield 1 kg of gold/hectare could
be economically viable. Anderson and his colleagues experimented
with B. juncea (Indian mustard) and Z. mays (corn) induced with
sodium cyanide and thiocyanate grown on oxidized ore pile con-
taining 0.6 mg/kg gold. They reported that B. juncea showed the
best ability to concentrate gold giving an average of 39 mg/kg
after sodium cyanide treatment. The highest individual gold con-
centration determined through analysis of selected biomass was
63 mg/kg (NaCN treatment of B. juncea) (Anderson et al., 2005,
Minerals Engineering).
Gold phytomining has also been reported by Msuya et al. (2000)
with ve root crops (carrot, red beet, onion and two cultivars of
radish) grown in articial substrate consisting of 3.8 mg/kg gold
and concluded that carrot roots yield 0.779 Au kg/ha, worth $US
840; by adding chelaters ammonium thiocyanate and thiosulphate
carrot roots yield 1.45 Au kg/ha of nal worth $US 7550. Lamb et al.
(2001) induced plant species B. juncea, B. coddii, and Chicory with
thiocyanate and cyanide solutions to determine gold concentration
in different parts of plants. The ashed plant material was dissolved
in 2 M HCl, followed by solvent extraction of the gold into solvent
methyl isobutyl ketone (MIBK). Addition of the reducing agent so-
dium borohydride to the organic layer caused a formation of black
precipitate at the boundary between the two layers and heating
this precipitate to 800 C caused formation of metallic gold. Gold
concentrations ranged from negligible in the leaves of B. coddii in-
duced with thiocyanate, to 326 mg/kg Au dried biomass in the
leaves of B. juncea induced with cyanide. The chemical additives
KI, KBr, NaS2O3, and NaSCN were also used with the B. juncea
and Chicory. The results showed varying degrees of hyperaccumu-
lation with all chemical treatments. Cyanide again gave the best re-
sults with 164 mg/kg Au dried biomass measured in the Chicory
plant. NaS2O3, KI, and NaSCN gave maximum results of 51, 41,
and 31 mg/kg Au dried biomass, respectively. Gardea-Torresdey
et al. (2005) have reported that C. linearis (desert willow a com-
mon inhabitant of Mexican Chihuahuan Desert) is a potential plant
for gold phytomining. Desert willow seedlings grew very well in
the presence of NH4SCN concentration lower than 1  104 mol/
L. It has been reported that shoot elongation was also not affected
by either the Au or NH4SCN concentrations. In addition when using
NH4SCN at a concentration of 104 mol/L with 5 mg Au/L, Au up-
take was enhanced by approximately 595, 396, and 467 percent-
ages in roots, stems, and leaves, respectively, compared with gold
uptake by plants grown in only 5 mg Au/L. Their studies also
showed that this plant produced Au (0) nanoparticles with an
approximate radius of 0.55 nm.
Mohan (2005) recommended phytomining to be a novel cost-
effective technology to extract gold from larger residual dumps
(mounds of tailings) and from low-grade ores at KGF (Kolar Gold
Fields) in Karnataka. Continuous conventional mining has depleted
the level of gold up to 3 mg/kg, hence union government closed the
mine. Committees worked over closed mine, proposed a scheme to
recover gold from larger residual dumps (mounds of tailings) that
had accumulated over the years. Studies have shown that there are
about 33 million tonnes of dumps accumulated over the years with
a concentration of gold 0.70.8 mg/kg, which may be a source of
24,000 kg of gold.
Silver uptake levels in the above ground shoots of terrestrial
plants are reported to be around 1 mg/kg (Sagiroglu et al., 2006)
or 126 mg/kg during induced accumulation in lupinus species (Blue
lupin) (Anderson et al., 2003). Further more, there have been no re-
ports in the literature on the hyperaccumulation of silver. The con-
cept of recovery of silver nanoparticles by any plant species was
proposed by Harris and Bali (2008). They investigated the uptake
of metallic silver by two common metallophytes B. juncea and
Medicago sativa and assessed the form and distribution of the metal
once sequestered by the plants. B. juncea accumulated up to
12.4 wt.% silver when exposed to an aqueous substrate containing
1000 ppm AgNO3 for 72 h, and silver uptake was largely indepen-
dent of exposure time and substrate silver concentration. M. sativa
accumulated up to 13.6 wt.% silver when exposed to an aque-
ous substrate containing 10,000 ppm AgNO3 for 24 h. However
M. sativa showed an increase in metal uptake with a corresponding
increase in the substrate metal concentration and exposure time.
In both the cases silver was stored as discrete nanoparticles, with
a mean size of approximately 50 nm. The addition of chelating
agent EDTA resulted in no discernable improvement in the ability
of either of the plant to extract and sequester silver, rather
impacted negatively upon the health of plants and the level of up-
take reduced accordingly. It has been recommended that synthesis
of large quantities of metallic nanoparticles is feasible with the
help of plants. Further experiments are needed in order to eluci-
date the optimum parameters and on the optimum technique for
complete recovery of nanoparticles.
Details of some specic plant hyperaccumulators with their me-
tal concentration (mg/kg) in denite biomass (kg/ha) of various
metals are given in Table 2.
5. Economics of phytomining
The economics of the operation depends upon number of fac-
tors, such as the metal content of the soil and plant, its biomass
production per annum and whether or not the energy of combus-
tion of the biomass can be recovered and sold. The most important
factor, however, is the revenue generation, world price of metal
being phytomined (Brooks et al., 1998). Metal value ranges from
about $73,555/kg for platinum to about $2.0/kg for lead (May
2008 Table 3). The best candidates for phytomining are gold, thal-
lium, cobalt and nickel due to their high cost, high metal concen-
tration in hyperaccumulator biomass (Table 4). Although metal
prices of uranium are comparatively high, but its reported metal
concentration (100 mg/kg) in biomass (10,000 kg/ha) is low, which
makes it uneconomical for phytomining (plant species Atriplex).
Manganese metal price is low ($3.1/kg) but metal concentration re-
ported in Macadamia is high, which makes it viable for phytomin-
ing. Metal prices are subjected to cyclical variation, and a low
current value for a given metal should not preclude consideration
of its extraction by phytomining. The biomass could be combusted
immediately for its economic value and the plant ash stored until
the world price improved (Brooks et al., 1998, 2001; Brooks and
Robinson, 1998). Various plant species reported for phytoextrac-
tion of valuable metals (platinum, thallium, cobalt, nickel, and
manganese) may be used for phytomining purpose after examining
their performance in the elds (Table 5). The recent metal prices
has also been incorporated in Table 3 (January 2009).
6. Advantages of phytomining
Phytomining offers the possibility of exploiting metals from
low-grade ores, overburdens, mill tailings, or mineralized soil that
is uneconomic by conventional mining methods (Nedelkoska and
 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019 1015

Table 4
Current metal prices for reported metal concentrations and biomass of metal hyperaccumulators (from Table 2).

Metals Biomass Metal concentration Metal concentration Current metal price in $ per hectare Current metal price in $ per hectare
(kg/ha) (mg/kg) (kg/ha) (May 2008) (January 2009)
Thallium 8000 4055 32.5 151,125 157,625
Gold 20,000 10 0.2 6351 6489
Manganese 30,000 55,000 1650 5115 2310
Cobalt 4000 10,200 40.8 4406 1550
Nickel 18,000 17,000 306 6946 3550
9000 13,400 120 2724 1392
Copper 5000 8356 41.8 343 138
Uranium 10,000 100 1 132 104
Cadmium 4000 3000 12 100 26
Zinc 4000 10,000 40 84 52
Lead 4000 8200 33 66 40

Table 5
Plant species of some valuable metals can be used for phytomining.

Metals Plant species References

Cobalt Haumaniastrum katangense, Crepidorhopalon perennis, Acalypha cupricola, Anisopapus chinesis Faucon et al. (2007)
Manganese Macadamia neurophylla, Phytolacca acinosa Brooks (1997), Xue et al. (2004)
Nickel Thlaspi goesingense Reeves and Baker (1984)
Psyshotria douarrei Davis et al. (2001)
Sebertia acuminate Perrier et al. (2004)
Alyssum narkgrai Vinterhalter and Vinterhalter (2005)
Alyssum murale Li et al. (2003b), Bani et al. (2007), Chaney et al. (2008)
Phyllanthus species, Euphorbia helenae, Leucocroton avicans, L. linearifolius Berazain et al. (2007a,b)
Platinum Sinapis alba, Lolium perenne Alt et al. (1998), Babula et al. (2007), Kologziej et al. (2007)
Silver Amanita strobiliformis Borovicka et al. (2007)
Thallium Lolium perenne, B. napus, Phaseolus vulgaris Makridis et al. (1996)
Zea mays, B. napus Tremel et al. (1997)
B. oleracea acephala, Iberis intermedia Al-Nazar et al. (2005)
Hirschfeldia incana, Diplotaxis catholica Madejon et al. (2007)

Doran, 2000). Its effect on the environment is minimal because of
the stabilizing action of the plants when compared with the ero-
sion caused by opencast mining operation (Salt et al., 1995; Robin-
son et al., 2003). In case of low-grade ores/mill tailings of sulphide
minerals, the bio-ores from phytomining are virtually sulphur free
and their smelting requires less energy than sulphide ores. The me-
tal content of a bio-ore is usually much greater than that of a con-
ventional ore and requires less storage space, despite the lower
density of a bio-ore (Brooks et al., 1998; Anderson et al., 1999a).
Phytomining can also be used for remedial purpose of high con-
centration of toxic metals (nickel and thallium) from mine tailings
and other metal contaminated areas. Hyperaccumulators accumu-
late large amount of these metals in their shoots, and hence pro-
vides a potential route for soil remediation and recovery and
reuse of the metal (Anderson et al., 1999b).
Phytomining not only produce just gold ingots but more impor-
tant are gold nanoparticles with in plant cells (crystallite or pri-
mary particles measuring less than 100 nm in size), which has
great importance for rapidly expanding nanoparticle market (Re-
eves and Baker, 2000; Gardea-Torresdey et al., 2005; Harris and
Bali, 2008). Another potential source of income from phytomining
is from the sale of carbon dioxide credits. Serpentine soils are nat-
urally infertile, support little plant biomass and, in some areas,
have low levels of soil or organic matter. Long term cultivation of
Alyssum with use of fertilizers may result in a permanent increase
in soil organic matter levels and sequestration at atmospheric car-
bon dioxide (Li et al., 2003b).
Natural revegetation may take decades or hundreds of years
because it is dependent on animal and windborne seedlings.
Phytomining restores mined degraded land by planting hyperaccu-
mulator species. A plant cover effectively prevents metal spread by
minimizing wind erosion and surface run off, as well as by reduc-
ing percolation to the ground water (Karenlampi et al., 2000). The
area to be mined may be ready to be vegetated and can be reused
for agriculture, horticulture, and forestry. In large scale applica-
tions of phytomining the potential energy stored can be utilized
to generate thermal energy. Restoration of vegetation cover can
fulll the objectives of stabilization and accelerate ecological suc-
cession (Wong, 2003). Phytomining involves plants that are cheap
and renewable resources. Also, source of energy is mostly solar.
Hence this is environment friendly, aesthetically pleasing; visual
unobstructive, non-invasive, non-destructive technology that has
high probability of public acceptance and has approaches in
mining elds.
7. Limitations of phytomining
Phytomining is climate and season dependent, limited by bio-
geochemical factors viz. rhizobiological activity, root exudates,
temperature, moisture, pH and concentration of competing ions
affecting the growth rate of plants, and the solubility and availabil-
ity of the metals in the soil (Ghosh and Singh, 2005). Plant requires
the metal to be in contact with root zone of the plant. Either the
plants must be able to extend roots to metals, or the metal must
be mobile to be in range of the plant roots. The use of chelators
(solubilizing agents) to increase metal mobility may also create
problem if the amount of chemical applied is above the level of me-
tal in soil solution that could be effectively taken by plants. Metals
1016 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
that are mobilized by chelators can migrate offsite of the rhizo-
sphere zone affecting plant metal uptake, may also affect soil
ecosystem stability, its function and may also increase extraction
cost (Greman et al., 2001; Gramss et al., 2004; Bouwman et al.,
2005).
Thiosulphates used for induced hyperaccumulation of gold are
extremely unstable in the environment, particularly at lower pH
values and their half life in the environment has been assessed
about six months. Ammonium thiocyanate can be biodegraded to
ammonia, bicarbonate, and sulphate (Huang and Pavlostathis,
1997). Thiocyanates have low toxicity over cyanides. The toxicity
of thiosulphate is even lower and is about equal to that of common
salt (Anderson et al., 1998b). Use of thiocyanate would have to be
strictly controlled to prevent leaching into ground and surface
waters if these chemicals and its associated metals are not taken
up by plants. It might also be possible to use transgenic plants
expressing a bacterial thiocyanate degrading system in order to ex-
tract Au from auriferous substrates. Such an approach would solve
the problem of thiocyanate toxicity to plants and perhaps allow
them to extract more Au, but not non target metals (Anderson
et al., 1999a).
Most natural metal hyperaccumulators are generally slow
growing with a small biomass and shallow root system, as a result
induced hyperaccumulators are recommended for phytomining.
The plants used for induced hyperaccumulation do not have to
be exotic species. A native plant that best suits the requisite fea-
tures of high and rapid biomass production would be the ideal
choice. Historic evidences shows that introduced exotic plants fre-
quently thrive and colonize areas of new land at the expense of
indigenous species. In situation where successful regrowth of na-
tive plant species is initially inhibited by a combination of high lev-
els of phytotoxic soil metals and low nutrient status, a
phytoextraction operation would result in the indigenous ora
competitively superseding the exotic species once soil metal levels
began to diminish. This could effectively restore the environment
to that which existed before soil metal levels became articially
elevated. As the metal concentration in the substrate diminishes
over time, the environment would become suitable for an increas-
ingly greater and diverse range of species (Anderson et al., 1999a).
For the phytomining to be economic, large mineralized areas
are required to get large biomass production of the desired plant
species to recover more target metal. The large biomass would also
be able to maintain a central incineration plant. This would provide
economic capital return from the metal sale and energy produc-
tion. This technology requires expert project designers with plenty
of eld experience that carefully choose the proper species and
cultivars for particular metals (and combinations of them) and re-
gions, and manage the entire system to maximize the biorecovery
of metals. Proper storage of harvested biomass will be necessary
for phytomining to prevent potential risk pathways such as intro-
duction to the food chain. Metal collected in leaves can be released
again to the environment during litter fall (Macek et al., 2000; Ne-
vel et al., 2007). Scheduling of harvest has to be based on avoiding
defoliation during owering and seed lling, because most of metal
is in leaves, it is important to harvest the shoots before much defo-
liation. This has the additional benet of limiting viable seed dis-
persal (Chaney et al., 2007).
8. Future scope
Phytomining has the possibility to be improved by discovery of
fast growing plants with high biomass and ability to accumulate
high concentration of metals in harvestable parts. Many genes
are involved in metal accumulation, translocation and sequestra-
tion and, transfer of any of these genes into candidate plant is a
Fig. 3. Strategies for improvement of hyperaccumulators using genetic engineering
(PCs-phytochelatin, MTs-metallothioneins).
possible strategy for genetic engineering of plants for improved
phytoextraction traits (Chaney et al., 2000, 2007). Selection of indi-
viduals with genetic coding for high metal content, high biomass
production and superior tolerance to soil heavy metal content will
not only augment metal crops, but may also provide genetic mate-
rial capable of being introduced into other species. The isolation of
these genetic materials may allow the genetic manipulation of high
biomass plants such as Z. mays, to produce a plant that will extract
large quantities of metals. Alternatively, the biomass production of
an existing hyperaccumulator T. caerulescens (with small biomass)
may be improved to enhance hyperccumulation of Ni, Zn, and Cd.
The ecological impacts by genetic engineering can be prevented by
proper management; by using sterile clones, harvesting plants
prior to owering, and selecting species that will not outcompete
native plants (Pion-Smits and Pilon, 2000). Genetic engineering is
currently being used to improve metal hyperaccumulation in
plants by changing oxidation state of metals, enhancing metal
transporters and chelators, encoding metal sequestration proteins
(MTs and PCs), and encoding transport proteins such as ZIP family
proteins (zinciron permease), ZAT (Zn transporter). Further iden-
tication of plant genes encoding metal-ion/metal complex trans-
porters and their molecular components could be of immense use
for phytomining studies (Fig. 3) (Eapen and DSouza, 2005; Shah
and Nongkynrih, 2007). Environment friendly and biodegradable
chelators should be developed (Hauser et al., 2005). Further work
needs to be carried out to elucidate the forms of metal complexes
with in the plants. If phytomining proceeds beyond the theoretical
and pilot plant stages there are two possible scenarios that might
be envisaged: rst scenario presupposes a commercial project on
a very large scale involving a few square kilometers of low-grade
metalliferous soil, the second, perhaps the more likely, could in-
volve phytomining being farmed out to small-scale land holders
through out the region in which a peasant farmer might grow a
few hectares of the plant material. It can be harvested, and pro-
cessed close to a large city where industrial waste could also be
used as a feedstock for the incineration plant. This in turn could
supply steam for producing local supplies of electricity (Brooks
et al., 2001). The locations with sub-economic metal mineraliza-
tion and ultramac soils might be an obvious site for the small-
scale farmers scenario.
 V. Sheoran et al. / Minerals Engineering 22 (2009) 10071019
9. Conclusion
Extraction of metals from conventional mining is limited to the
proved category of reserves which are fastly depleting. The phyto-
mining technology-based on the ability of plants to accumulate
large concentration of metals has potential for valuable metals.
The economics of phytomining basically depends on the metal con-
tent in the soil, metal uptake by the plant, plant biomass and most
importantly the metal price. Metal prices are subjected to cyclical
variation, and a low current value for a given metal should not pre-
clude consideration of its extraction by phytomining. Recently the
mining industry like other industries has entered into a recession
tsunami (Table 3 metal prices in May 2008 and January 2009)
and the metal prices has dropped considerably except gold and
thallium. The authors are of the opinion that before implementing
phytomining reassessment of the economics should be carried out
by considering the present metal prices.
Majority of the research has been conducted on laboratory scale
and in relatively controlled conditions for a short period of time;
the true potential of the phytomining is yet to be established. More
extensive research under eld conditions on commercial scale for
longer durations is required, particularly, in the eld of increasing
metal uptake by plants and measures to prevent leaching of metals
during induced phytomining. Further integrated multidisciplinary
research efforts that combine plant biology, genetic engineering,
soil chemistry, and soil microbiology, as well as agricultural and
environmental engineering is required. It is only then that we will
know whether phytomining is just a temporary aberration in the
long history of scientic progress, or a new idea whose time has
come. Most of the studies have been carried out in developed
countries and the knowledge of suitable plants is particularly lim-
ited in developing country like India where phytomining is in its
infancy. It is difcult in the enthusiasm of describing a new tech-
nique not to be accused of overstating the case, rather it is pointing
the way to future research into the use of hyperaccumulators in or-
der to phytomine the worlds vast reserves of sub-economic depos-
its of different valuable metals.
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