Ecotoxicology and Environmental Safety 119 (2015) 186–197

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Ecotoxicology and Environmental Safety

journal homepage: www.elsevier.com/locate/ecoenv

Review

Mechanisms of silicon-mediated alleviation of heavy metal toxicity

in plants: A review
Muhammad Adrees a, Shafaqat Ali a, Muhammad Rizwan a,n, Muhammad Zia-ur-Rehman b,
Muhammad Ibrahim a, Farhat Abbas a, Mujahid Farid a, Muhammad Farooq Qayyum c,
Muhammad Kashif Irshad a
a
Department of Environmental Sciences and Engineering, Government College University, Allama Iqbal Road, 38000 Faisalabad, Pakistan
b
Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad 38040, Pakistan
c
Department of Soil Sciences, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan

art ic l e i nf o a b s t r a c t

Article history: In present era, heavy metal pollution is rapidly increasing which present many environmental problems.
Received 18 January 2015 These heavy metals are mainly accumulated in soil and are transferred to food chain through plants
Received in revised form grown on these soils. Silicon (Si) is the second most abundant element in the soil. It has been widely
13 April 2015
reported that Si can stimulate plant growth and alleviate various biotic and abiotic stresses, including
Accepted 9 May 2015
heavy metal stress. Research to date has explored a number of mechanisms through which Si can alle-
viate heavy metal toxicity in plants at both plant and soil levels. Here we reviewed the mechanisms
Keywords: through which Si can alleviate heavy metal toxicity in plants. The key mechanisms evoked include re-
Abiotic stress ducing active heavy metal ions in growth media, reduced metal uptake and root-to-shoot translocation,
Genotypes
chelation and stimulation of antioxidant systems in plants, complexation and co-precipitation of toxic
Heavy metal
metals with Si in different plant parts, compartmentation and structural alterations in plants and reg-
Plant
Silicon ulation of the expression of metal transport genes. However, these mechanisms might be associated with
Tolerance plant species, genotypes, metal elements, growth conditions, duration of the stress imposed and so on.
Further research orientation is also discussed.
& 2015 Elsevier Inc. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Silicon in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. Silicon uptake and accumulation in plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
4. Protective role of silicon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
5. Silicon-mediated alleviation of metal toxicity in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
5.1. Decrease in metal uptake by plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
5.2. Enhancement in gas exchange attributes and photosynthetic pigments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
5.3. Changes in mineral nutrients uptake and plant growth and biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
6. Mechanisms of Si-mediated metal detoxification in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
6.1. Immobilization of toxic metal in the growth media . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
6.2. Enhancement in antioxidant defense system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
6.3. Compartmentation within plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
6.4. Co-precipitation of silicon with metals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6.5. Chelation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
6.6. Modification of gene expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
6.7. Structural alterations in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
6.8. Other . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
7. Conclusions and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

n
Corresponding author. Fax: þ92 41 9200671.
E-mail address: mrazi1532@yahoo.com (M. Rizwan).

http://dx.doi.org/10.1016/j.ecoenv.2015.05.011
0147-6513/& 2015 Elsevier Inc. All rights reserved.
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
1. Introduction
Soil contamination is indeed considered one of the main
threats to agricultural soil as identified in the European Union soil
communication (CEC, 2002). This contamination originates from
natural sources by means of mineral dissociation, weathering of
parent material and atmospheric deposition as well as anthro-
pogenic sources related to mining, industrial emissions, disposal
or leakage of industrial wastes, application of sewage sludge to
agricultural soils, fertilizer and pesticide use (Nagajyoti et al.,
2010). Heavy metals like cadmium (Cd), lead (Pb), chromium (Cr),
copper (Cu), manganese (Mn) and zinc (Zn) contribute the major
share of soil contamination. Due to the potential toxicity and high
persistence of heavy metals, soils polluted with such elements
create an environmental problem that threats the plant, animal
and human health (do Nascimento and Xing, 2006; Adrees et al.,
2015).
Among heavy metals, some metals such as Cd, Pb and Cr have
no known biological role while others such as Cu, Zn and Mn are
required in small amount for normal plant growth and develop-
ments but are extremely toxic to plants and animals slightly larger
than the required concentrations (Kabata-Pendias and Pendias,
2001). It has been widely reported that accumulation of heavy
metals in plants may cause many biochemical, structural and
physiological changes (Nagajyoti et al., 2010; Afshan et al., 2015).
Heavy metals negatively affected plant growth, biomass and
photosynthesis (Wuana and Okieimen, 2011; Adrees et al., 2015;
Ali et al., 2015a, 2015b). In an excess, heavy metals also affect the
accumulation and translocation of essential elements by plants
(Wagner, 1993; Wuana and Okieimen, 2011; Zia-ur-Rehman et al.,
2015). Consequently, there is growing concern related to heavy
metal pollution issues worldwide in order to reduce toxic metal
bioavailability and plant uptake for increasing plant growth and
yield and ultimately safe food production.
Silicon is a very important part of the earth's crust and it
consists about 28% of the earth's crust (Sommer et al., 2006).
However, Si is only 0.03% of the biosphere (Fauteux et al., 2005). In
fact, Si is accumulated in many plants up to 10% by weight (Hod-
son et al., 2005) that is greater than some macronutrients (Epstein,
1994). Silicon has been shown to alleviate the deleterious effects of
heavy metals in plants grown on contaminated soils (Chen et al.,
2000). Experiments have demonstrated that certain crops benefit
significantly from Si application (Takahashi et al., 1990). Various
beneficial effects of Si have been identified in plants (Epstein, 1994,
1999). Various studies describe the ameliorative effect of Si ap-
plication on plants under heavy metals or dangerous toxic ele-
ments, like Al, Cd, Pb, Cr or Cu (da Cunha and do Nascimento,
2009; Ali et al., 2013; Li et al., 2013; Shen et al., 2014; Keller et al.,
2015). Thus, use of Si to enhance plant growth and alleviate heavy
metals toxicity is predicted to become an emerging trend in the
agriculture in near future. This review article summarizes the re-
cent progress in understanding the mechanisms of Si-mediated
heavy metal tolerance in plants.
2. Silicon in soil
Silicon is the second most abundant element in the soil ranging
from 50 to 400 gSi kg  1 of soil (Kovda, 1973). Silicon compounds
187
in the soil are usually present as SiO2 and in various alumino-si-
licate forms. Silicon dioxide comprises about 50–70% of the soil
mass (Ma and Yamaji, 2006). External sources of Si include calcium
and magnesium silicates, silicate slag, dolomite, rock phosphate
and diatomite (Savant et al., 1997; Guntzer et al., 2012; Rizwan
et al., 2012). Silicon compounds exist both in the liquid and in solid
phase in the soil. In the solid phase, Si compounds can be divided
into amorphous, poorly crystalline and crystalline forms. Amor-
phous silica (ASi) is comprised of both ASi from plants including
phytoliths and other inorganic forms of ASi (Sauer et al., 2006) and
it is considered to be the first pool of available Si for plants
(Alexandre et al., 1997). The amount of biogenic silica (phytoliths)
in soils ranges from 0.03 to 0.06 wt% (Desplanques et al., 2006).
Grassland soils contain phytoliths up to only 1–3% of total Si pool
(Blecker et al., 2006). The phytoliths are mainly composed of about
92 wt% silica and 6 wt% water with small amounts of carbon and
traces of Al and Fe (Meunier et al., 1999). In liquid phase, Si is
present as mono- and poly-silicic acids, complexed with organic
and inorganic compounds (Cornelis et al., 2011). In natural soil
solution, Si is mainly present in the form of uncharged orthosilicic
acid, H4SiO4 ranging from 0.1 to 0.6 mM (Epstein, 1994; Sommer
et al., 2006) and it is thought to be the only form which is taken up
by plants (Epstein, 1994, 1999; Ding et al., 2005).
3. Silicon uptake and accumulation in plants
All plants grown in soil contain some Si in their tissues varying
from 0.1% to 10% by weight of plants (Epstein, 1994, 1999; Ma and
Yamaji, 2008). Silicon uptake by plants varies greatly between
species and cultivars, i.e., gramineous vs leguminous plants, and
plants are classified as high-, intermediate-, and non-Si-accumu-
lators (Takahashi et al., 1990; Ma et al., 2001). However, Si con-
centration in plant tissues depends upon the characteristics of Si
uptake and transport, variability between species and genotypes
within a species (Epstein, 1994; Ma and Yamaji, 2008). Plant roots
take up Si in the form of un-dissociated H4SiO4 (Casey et al., 2003;
Ding et al. 2008) and Si uptake mechanisms differ between plant
species (Ma and Yamaji, 2006). The mechanisms of Si absorption
by roots are still controversial. However, there are three possible
mechanisms of Si uptake by higher plants namely passive, active
and rejective (Ma et al., 2004; Mitani and Ma, 2005). Passive up-
take of Si takes place along the transpiration stream and it is
shown that most dicotyledonous plants absorb Si passively (Ma
et al., 2001). Active Si uptake is dominant in many plant species
such as rice, maize, sugarcane and wheat (Casey et al., 2003; Rains
et al., 2006). Transporters responsible for Si uptake by roots have
been identified in different plant species such as rice, barley,
maize, wheat and cucumber (Ma et al., 2007, 2011; Chiba et al.,
2009; Mitani et al., 2009).
Once absorbed by roots, Si moves to the shoots by transpira-
tional water flow via the xylem (Ma et al., 2006). In many plants,
more than 90% of Si taken up by the roots is translocated to the
shoots (Ma and Takahashi, 2002). In the xylem sap, Si is mostly
present in the form of monosilicic acid and some as disilicic acid
(Casey et al., 2003; Mitani and Ma, 2005). Recently, Si transporters
responsible for xylem unloading in leaves (Lsi6) and inter-vascular
transport have been identified (Yamaji et al., 2008, 2012). After
translocation to shoots, Si is ultimately deposited as amorphous
188 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
silica, SiO2  nH2O, mainly at transpiration sites (Ma and Takahashi,
2002). Once deposited in this form, Si is immobile and not redis-
tributed (Hodson and Sangster, 1990). Deposition of Si takes place
in different parts of plant such as epidermis of shoots but can also
occur in cell walls of root endodermis (Lux et al., 2003; Keller et al.,
2015). However, phytoliths varies greatly between individual plant
families with respect to type, composition and localization, which
depends upon plant species, and environmental conditions
(Guntzer et al., 2012; Li et al., 2014).
4. Protective role of silicon
Although Si is not considered as an essential element for plants,
it has been proved to be beneficial for the growth and develop-
ment of many plant species (Epstein, 1994). Experiments showed
that plants supplied with Si resist lodging by increasing mechan-
ical strength of plants enabling them to achieve and maintain an
erect habit. This might be due to association of Si with cell walls
which increased the rigidity of plant cell walls (Raven, 1983).
Epidermal tissue deposition of Si also protects plants against ex-
cessive loss of water by transpiration (Emadian and Newton, 1989).
Beneficial effects of Si are studied in many plant species such as
wheat, rice, cucumber, maize and bamboo, in particular, under
stressful conditions (Rogalla and Romheld, 2002; Ma and Taka-
hashi, 2002; Shi et al. 2005a; Zhang et al., 2008; Vaculik et al.,
2009; Feng et al., 2010; Collin et al., 2014). Silicon protects the
plants from a number of biotic stresses such as diseases i.e., blast
and powdery mildew and pest i.e., stem borer and plant hopper
(Ma and Yamaji, 2006). Silicon also protects plants from a number
of abiotic stresses such as heavy metals, radiation, heat and
drought stresses (Bélanger et al., 2003; Côté -Beaulieu et al., 2009;
Epstein, 2009).
5. Silicon-mediated alleviation of metal toxicity in plants
Heavy metal toxicity negatively affects biomass production and
grain yield in almost all major field grown crops (Nagajyoti et al.,
2010; Adrees et al., 2015). Several studies reported the
Fig. 1. Hypothetical mechanisms for Si-mediated alleviation of heavy metal toxicity in plants (for details see the text).
ameliorative effect of Si on the toxicity of certain metals such as
Zn, Mn, Al, Cu and Cd in many plant species. Here, we reviewed
the recent progress on the effects of Si on metal uptake, photo-
synthetic pigments, mineral nutrients uptake and plant growth
and biomass (also see Fig. 1).
5.1. Decrease in metal uptake by plants
One of the major effects of Si on the reduction of metal toxicity
is reducing the metal uptake and transport in plants. It was re-
ported by many researchers that Si application would enhance
tolerance to toxic metals in many plant species by reducing the
uptake and translocation of metals. Silicon application decreased
Cd concentration in many plant species such as maize (Liang et al.,
2005; Dresler et al., 2015), rice (Shi et al., 2005b; Li et al., 2008),
wheat (Rizwan et al., 2012; Naeem et al., 2014; Hussain et al.,
2015), cotton (Farooq et al., 2013), peanut (Shi et al., 2010) and in
chinese cabbage (Brassica chinensis L.) (Song et al., 2009). It has
been reported that Si not only reduced Cd uptake by the plants but
also reduced shoot to grain translocation of Cd (Naeem et al., 2014;
Hussain et al., 2015). Si-mediated decrease in Cu uptake and
translocation was observed in wheat (Nowakowski and Now-
akowska, 1997; Keller et al., 2015). Silicon application decreased Al
in roots, stem and leaves of peanut and rice seedlings (Singh et al.,
2011; Shen et al., 2014). Furthermore, Si decreased Cr concentra-
tion in shoots and roots of rice, barley and wheat (Zeng et al., 2011;
Ali et al., 2013; Tripathi et al., 2015). Application of Si significantly
suppressed Zn accumulation in various plant parts, i.e., roots, and
leaves of cotton, maize (Kaya et al., 2009; Anwaar et al., 2014;
Bokor et al., 2014a, 2014b). In addition, it was shown that a sig-
nificant negative correlation exist between external Si supply and
arsenate and/or arsenite uptake and concentration in rice seed-
lings under hydroponic and soil culture conditions (Guo et al.,
2005, 2006, 2007, 2009; Tripathi et al., 2013; Hu et al., 2013;
Sanglard et al., 2014). Similarly, soil application of Si (silica gel,
10 g kg  1 of soil) reduced the As concentration in straw, flag leaf,
husk and grains of rice plants (Fleck et al., 2013). This is because
both Si and As share the same influx transporter (Low silicon rice 1,
Lsi1) in rice as suggested by Guo et al. (2009). However, Si effect on
metal uptake and translocation varies with plant species and
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
genotypes (Liu et al., 2013b; Marmiroli et al., 2014; Hussain et al.,
2015).
This decrease in metal uptake in the presence of Si can be ex-
plained in many ways such as Si can enhance the uptake of cal-
cium ions and reduced Al uptake by plants (Hammond et al.,
1995). Silicon may stimulate production of root exudates which
can chelate metals and reduce their uptake by roots (Kidd et al.,
2001). In addition, this reduction in metal uptake can also be ex-
plained by the fact that Si reduced the apoplasmic transport of
metals by decreasing free metal concentration in the apoplasm
(Iwasaki et al., 2002; Rogalla and Romheld, 2002). Moreover, the
physical barrier formed by the deposition of Si in the vicinity of
the endoderm may reduce the cell wall porosity of inner root
tissues, thus reducing the metal concentration in the xylem (Shi
et al. 2005a; da Cunha and do Nascimento, 2009; Keller et al.,
2015). Similarly, Si decreased apoplasmic transport of Cd through
the enhanced adsorption of Cd on the cell walls (Ye et al., 2012).
Silicon accumulation in the roots endodermis may reduce the
mobility of heavy metals such as Al (Wang et al., 2004) and Cu
(Keller et al., 2015). Additionally, it has been reported that in Si
treatments the Si-accumulating ( þSi) cells significantly inhibited
the net Cd2 þ influx, compared with that in Si-limiting (  Si) cells
(Liu et al., 2013a). Decrease in metal uptake by the plants at least
partially related to development of apoplasmic barriers and ma-
turation of vascular tissues root (Greger et al., 2011; Vaculik et al.,
2012).
It has been widely reported that increasing Si treatments in
hydroponics or in soil increased Si uptake in shoots and roots of
many plant species while increasing metal concentrations in the
growth medium reduced Si uptake by the plants (Shi et al., 2005b;
Li et al., 2008; Guo et al., 2009; Naeem et al., 2014; Keller et al.,
2015). Therefore, it could be concluded that Si reduced the heavy
metal toxicity in plants by decreasing metal uptake and blocking
metal transfer in plants. It has also been reported that Si appli-
cation increased metal accumulation by plants. For example, Si
application in soil in the form calcium silicate (CaSiO3) increased
Cd and Zn accumulation in maize plants (da Cunha and do Nas-
cimento, 2009). Liang et al. (2005) reported that total Cd was
significantly higher in the shoots and roots of maize plants in the
Si-amended Cd treatments than in the non-Si-amended Cd treat-
ments. Similarly, Vaculik et al. (2009, 2012) showed that Si did not
reduce the total Cd uptake in maize plant. In Chinese Kale, po-
tassium silicate application in soil increased the Si contents in
shoots while increased Cd concentration in roots without affecting
Cd concentration in leaves as compared to control (Lu et al., 2014).
Additionally, Cocker et al. (1998) reported that total Al in-
creased in wheat plants in the presence of Si, suggesting a Si-
mediated mechanism in plants. Furthermore, Collin et al. (2013)
reported that in bamboo plants Cu concentration was higher in
roots followed by stem and leaves and Si did not alter the ab-
sorption of Cu by plants grown in hydroponics. Similarly, Si did not
affect the Mn concentration in roots and leaves of cucumber plants
(Dragišić Maksimović et al., 2007). This showed that Si-mediated
alleviation of metal phytotoxicity is not only due to the decreased
metal uptake by plants but there might be Si-mediated mechan-
isms of metal detoxification in plant. Decrease in metal uptake by
plants might be due to immobilization of metals in the growth
media and/or modulation of influx transporters which reduced
metal transport from root surface to root xylem. Decrease in metal
translocation from roots to shoot and grains might be due to
structural alterations in shoots and roots and/or co-precipitation,
chelation and compartmentation of metals in plants. These Si-
mediated metal tolerance mechanisms in plants are described
latter in the text (mechanisms of Si-mediated metal detoxification
in plants).
189
5.2. Enhancement in gas exchange attributes and photosynthetic
pigments
Positive effects of Si on chlorophyll biosynthesis and photo-
synthetic machinery under metal toxicity have been widely re-
ported. For example, Siþ Cd application increased chlorophyll a,
chlorophyll b and carotenoid contents in leaves as compared to
Cd-only treatments in maize (Malčovská et al., 2014), wheat
(Rizwan et al., 2012; Hussain et al., 2015), cucumber (Feng et al.,
2010) and rice (Nwugo and Huerta, 2008). Silicon application in-
creased chlorophyll contents under Al, Cr and As toxicity in rice,
mongbean, wheat and barley (Yang et al., 1999; Singh et al., 2011;
Ali et al., 2013; Sanglard et al., 2014; Tripathi et al., 2015). Si ap-
plication in hydroponics enhanced the activity of gas exchange
characteristics (net photosynthetic rate, stomatal conductance,
transpiration rate, water use efficiency), chlorophyll, and car-
otenoids contents under Cd stress in cotton, rice and cucumber
(Nwugo and Huerta, 2008; Feng et al., 2010; Farooq et al., 2013).
Similarly, Si enhanced gas exchange characteristics under Al and
Cr stress in peanut and barley (Ali et al., 2013; Shen et al., 2014), in
cotton under Pb stress (Bharwana et al., 2013) and in rice under Zn
stress (Song et al., 2014).
Similarly, Hu et al. (2013) reported that Si supply increased net
photosynthetic rate and reduced stomatal limitation in rice under
arsenic (As) stress. Furthermore, Sanglard et al. (2014) studied
detailed gas exchange measurements with chlorophyll fluores-
cence analysis to examine the effects of Si nutrition on photo-
synthetic performance in rice plants under As (arsenite) toxicity.
Authors reported that Si considerably reverted As-mediated im-
pairment in carbon fixation and leaf conductance at the stomata
and mesophyll levels and the response was time and genotype-
dependent manner. Furthermore, Si increased photosynthetic ac-
tivity, chlorophyll fluorescence, in many plant species under metal
stress such as in barley and wheat under Cr stress (Ali et al., 2013;
Tripathi et al., 2015). Moreover, Nwugo and Huerta (2010) reported
that in rice leaves Si enhanced the Cd tolerance by increasing in-
stantaneous water-use-efficiency, carboxylation efficiency of ri-
bulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO), and
light-use efficiency.
In general, positive effect of Si on photosynthetic machinery
might be due to lower uptake of metal by the plants (as reported
in Section 5.1) which reduced the damage to photosynthetic ma-
chinery and/or due to activation of plant defense system and
morphological, anatomical and ultrastructual alterations in pho-
tosynthetic apparatus (see the details later in the text).
5.3. Changes in mineral nutrients uptake and plant growth and
biomass
Mineral nutrients are the major constituents of the plant
structural component and provide mechanical, biochemical, and
physical strengths to the plants. Mineral nutrients also play a
major role in the growth and development of plants and heavy
metals may interfere with essential nutrient uptake and transport,
thereby disturbing the mineral nutrition composition. Therefore,
informations, qualitative and quantitative, about the mineral up-
take and transport with Si application under metal stress may
provide a deeper insight of the mechanisms by which Si reduce
metal toxicity in plants. Silicon plays an important role in the
absorption of nutrients by the plants under metal stress. Si ap-
plication in hydroponic solution increased the content and accu-
mulation of micro-, Zn and Mn, and macro-nutrients, Ca, Mg, P and
K, by wheat plants under Cr, Cd and Cu (Rizwan et al., 2012; Keller
et al., 2015; Tripathi et al., 2015). Similarly, Wang et al. (2014)
reported that foliar application with nano-Si increased Mg, Fe, and
Zn nutrition in rice seedlings under Cd stress. Silicon application
190 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
under Al stress increased Mg and Zn concentrations in shoots and
roots of rice as compared to Al treatment alone while Si did not
affect the Mn concentration in both parts (Singh et al., 2011).
Moreover, Si influenced mineral nutrient concentrations, either as
a main effect or as an interactive effect, in zinnia (Zinnia elegans)
and Erica andevalensis plants under Cu stress (Frantz et al., 2011;
Oliva et al., 2011). Under Zn toxicity, Si þZn application increased
K, P and Fe in maize ad rice seedling as compared to Zn stress
alone (Kaya et al., 2009; Mehrabanjoubani et al., 2014).
Although Si application increased mineral nutrient under dif-
ferent metal stress but recently Bokor et al. (2014b) reported that in
maize plants Si application decreased mineral elements Mn, Fe, Ca,
P, Mg, Ni, Co, and K in shoots and roots in Siþ Zn treatment as
compared to the corresponding Zn treatment without Si. This
showed that homeostatic network of mineral elements was dis-
rupted and caused negative alterations in mineral nutrition. Taken
together, Si could reduce metal toxicity in plants by the interaction
with other elements but there is still need to explore the me-
chanisms of mineral nutrient absorption in the presence of Si in
multi-metal contaminated and texturally different soils. Moreover,
it remains for future studies why this positive or negative correla-
tion occurred between Si and mineral nutrients under different
metal toxicity and study expression level of other transporter genes.
Role of Si in the growth and biomass of plants has been widely
accepted. Si supply may increase the biomass of plants under
metal stress and may decrease the metal toxicity by dilution effect
(the same uptake but larger biomass). However, this mechanism is
not well understood and is still controversial. Several authors have
observed beneficial effects of Si on plants biomass under heavy
metal stress in soil or in nutrient solution. Si supply increased the
dry weight of both shoots and roots of many plant species under
Cd stress including maize (Liang et al., 2005; da Cunha and do
Nascimento, 2009; Vaculik et al., 2009), wheat (Rizwan et al.,
2012; Naeem et al., 2014), strawberry (Treder and Cieslinski, 2005)
and rice (Nwugo and Huerta, 2008; Zhang et al., 2008; Gu et al.,
2011; Tripathi et al., 2012a, 2012b; Srivastava et al., in press). In
addition, Si supply increased the shoot and root dry weights under
Al stress in maize (Corrales et al., 1997), rice (Hara et al., 1999;
Singh et al., 2011), mongbean (Yang et al., 1999) and barley
(Morikawa and Saigusa, 2002). Similarly, Si supply increased plant
biomass under Cr stress in barley (Ali et al., 2013), pakchoi (B.
chinensis L.) (Zhang et al., 2013a, 2013b), wheat (Tripathi et al.,
2015) and rice (Zeng et al., 2011). Recently it has been shown that
Si supply also increased plant biomass of wheat, Arabidopsis
thaliana and E. andevalensis under Cu stress grown in hydroponics
(Khandekar and Leisner, 2011; Oliva et al., 2011; Keller et al., 2015).
Silicon application also positively affected the biomass of maize
and rice under Zn stress (Kaya et al., 2009; Song et al., 2011, 2014;
Gu et al., 2012; Mehrabanjoubani et al.. 2014). Contrary, it was
reported that 5 mM Si þ150 mM Zn in hydroponic reduced shoot
and roots biomass of sorghum as compared to corresponding Zn
treatment during 20 days (Masarovic et al., 2012). Similarly, 5 mM
Si þ800 mM Zn addition decreased shoot and root biomass of
maize plants, grown in hydroponics for 10 days, as compared to
same Zn treatment without Si (Bokor et al., 2014a, 2014b).
In general, increase in plant growth and biomass might be due
to decrease in toxic metal uptake by plants and/or increase in
nutrient uptake by plants and increase in photosynthetic pigments
and maintenance in the structure of photosynthetic machinery.
Overall, Si is beneficial to plants under metal toxicity and in-
creased plant biomass under metal stress.
6. Mechanisms of Si-mediated metal detoxification in plants
In the above section, we reported that Si application reduced
the metal uptake by plants and enhanced the plant growth by
enhancing photosynthesis and uptake of mineral elements. These
positive effects of Si might be due to different mechanisms un-
derlying at the soil and plant levels. A good understanding of the
mechanisms of Si-mediated metal detoxification in plants is very
important for the targeted application of Si. Silicon-mediated
metal detoxification mechanisms have been extensively studied in
many plant species. At soil level, these mechanisms may include
immobilization of metals in the soil. At plant levels, these me-
chanisms include reduction in oxidative stress by enhancing the
activities of antioxidant enzymes, structural alterations in different
parts of plants, compartmentation of metals into metabolically
inactive parts, co-precipitation of metals with Si, chelation and
modification of gene expression. The following sections, we dis-
cussed these mechanisms in detail in the light of recent reports.
6.1. Immobilization of toxic metal in the growth media
Silicon-mediated alleviation of metal toxicity to plants might
be due to an external plant effect by decreasing availability of
phytotoxic metals in the culture media (Liang et al., 2005; da
Cunha et al., 2008; Naeem et al., 2014). It has been shown that Si
application in the soil affects the soil properties which in turn
control heavy metals availability to plants (Liang et al., 2007;
Rizwan et al., 2012). Among soil factors, pH and organic matter are
two of the most important factors that control metal availability
and it has been shown that Si decreased metal bioavailability by
increasing soil pH (Chen et al., 2000; Morikawa and Saigusa, 2002;
Liang et al., 2005; Treder and Cieslinski, 2005; Gu et al., 2011). Li
et al. (2012) reported that addition of sodium metasilicate
(800 mg kg  1 Si) in Pb contaminated soil significantly increased
soil pH and decreased the proportion of exchangeable Pb in soil,
thus reducing Pb bioavailability but the affect was not clear at
lower (100 mg kg  1) amendments. Additionally, Rizwan et al.
(2012) reported that ASi application in the soil slightly increased
soil pH and reduced bioavailable Cd in the soil. Silicon application
increased Si and decreased pH and Cd in the soil solution. How-
ever, Naeem et al. (2014) reported that calcium silicate,
150 mg kg  1, decreased plant available soil Cd without affecting
soil pH. Similarly, da Cunha et al. (2008) reported no change in soil
pH associated with decrease in bioavailable Cd concentration in
soil. More recently, it was reported that sodium silicate amend-
ment in the soil significantly increased soil pH and decreased Cd
and Cr bioavailability compared to control (Zhang et al., 2013b; Lu
et al., 2014).
Silicon can also change the speciation of metals in soil solution
by the formation of silicate complexes (Ma et al., 1997; Liang et al.,
2007; Putwattana et al., 2010). It has been reported that the higher
Si concentration due to added furnace slag reduced bioavailable
Cd. In addition, more Cd was found in the form of oxides or ad-
sorbed Fe–Mn oxides bound and organic matter fractions in the Si-
amended soil (Chen et al., 2000; Liang et al., 2005). Hara et al.
(1999) reported that Si changed the chemical forms of Al in the
solution and Hodson and Evans (1995) hypothesized that Al
formed hydroxyaluminosilicate (HAS) species in solutions or
growth media by the addition of Si which seems to contribute Si-
mediated detoxification of Al in plants. However, Cocker et al.
(1998) did not observed significant formation of HAS in the growth
media. Zhang et al. (2013b) reported that addition of Si markedly
decreased the proportion of exchangeable Cr in Cr-contaminated
soil by increasing the proportion of precipitation-bound, organic
matter bound Cr fraction, thus reducing Cr availability in the soil.
Silicon application in the form of calcium silicate also altered
the Cd and Zn distribution in the soil and both metals were found
in more stable fractions such as complexed with organic matter
and crystalline iron oxides (da Cunha et al., 2008). Gu et al. (2011)
reported that Si rich amendments immobilized Cu, Cd and Zn in
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
multi-metal contaminated acidic soils by increasing soil pH. They
also showed that metals were mainly deposited as their silicates,
phosphates and hydroxides in amended treatments. Recently,
Shim et al. (2014) reported that corn cob silica application in
contaminated soil reduced metal mobility in the soil and x-ray
diffraction data indicated the formation of insoluble lead silicate in
soil. The above studies suggest an external interaction between Si
and heavy metals. Taken together, Si application can immobilize
toxic metals in the soil by increasing soil pH and changing metal
speciation in soil. The above studies showed that the metal spe-
ciation and pH was observed in the bulk soil, soil which is not part
of the rhizosphere, after crop harvest. However, pH and metal
speciation in rhizosphere, the narrow region of soil that is directly
influenced by root secretions and associated soil microorganisms,
and in the soil solution needs to be explored to better understand
Si-mediated metal immobilization in the growth media and up-
take by plants. Moreover, there is still a need to evaluate the effect
of more Si amendments/sources on the metal speciation in the
soil.
6.2. Enhancement in antioxidant defense system
Oxidative stress may occur in plants when they are exposed to
various environmental stresses, both biotic and abiotic, including
heavy metal stress (Adrees et al., 2015; Ali et al., 2015a, 2015b;
Habiba et al., 2015; Noman et al., 2015). However, Si application
may reduce oxidative stress in plants by reducing the production
of reactive oxygen species (ROS) and by enhancing the activities of
antioxidant enzymes. For example, it was reported that Si de-
creased the contents of malondialdehyde (MDA), hydrogen per-
oxide (H2O2) and electrolytic leakage (EL) in shoots and roots of
cotton plants under Cd, Zn and Pb stress (Bharwana et al., 2013;
Farooq et al., 2013; Anwaar et al., 2014). Silicon decreased MDA
concentration in Nigella sativa, peanut, pakchoi and rice under Cd
stress (Song et al. 2009; Shi et al., 2010; Kim et al., 2014; Rad et al.,
2014; Wang et al., 2014) and in peanut under Al stress (Shen et al.,
2014). Similarly, Liu et al. (2013b) reported that Si application re-
duced the H2O2 and EL in S. nigrum seedlings under Cd stress.
Silicon application decreased H2O2, superoxide anion (O2∙−), and
TBARS (thiobarbituric acid reactive substances) contents in leaves
and roots of maize and rice plants under Cd stress (Malčovská
et al., 2014; Srivastava et al., in press). Similarly, Si application
decreased H2O2 and MDA contents in spinach, rice and wheat
shoots and roots under Cd, Zn, Fe, B, As and Mn toxicity (Gunes
et al., 2007a, 2007b; Song et al., 2011; Li et al., 2012; Tripathi et al.,
2012a, 2012b, 2013; Chalmardi et al., 2014). Furthermore, Si re-
duced the TBARS contents in leaves and roots of rice under Cr
stress (Zeng et al., 2011).
Plants have developed a complex antioxidative defense system
including both enzymatic and non-enzymatic antioxidants (Suzuki
et al., 2011; Gill et al., 2015). Stimulation of antioxidants under
metal stress appears a mechanism that accounts for increased
metal tolerance in plants. However, antioxidant enzymes activities
decreased under higher metal stress (Ehsan et al. 2014; Adrees
et al., 2015). Silicon supply may enhance the activity of antioxidant
(e.g. superoxide dismutase (SOD), peroxidases (POD), catalase
(CAT), ascorbate peroxidase (APX) under metal stress to help
plants to cope with metal stress.
This Si stimulation effect on antioxidants has been observed
under Cd stress in maize (Lukacova et al., 2013), wheat (Hussain
et al., 2015), cotton (Farooq et al., 2013), pakchoi (Song et al.,
2009), rice (Tripathi et al., 2012a, 2012b; Srivastava et al., in press)
and peanut (Shi et al., 2010). Khodarahmi et al. (2012) reported
that in cucumber cultivars Si application increased CAT activity in
Negin cultivar under Cd stress but did not affect in Super Dominus
cultivar which showed cultivar dependent response of Si under
191
metal stress. Si also stimulated the antioxidant enzymes under Mn
toxicity in cucumber (Shi et al., 2005b) and Mn-tolerant (Zhu-
liangyou 99) cultivar of rice but decreased in Mn-sensitive (Xin-
xiangyou 640) cultivar of rice (Li et al., 2012), under Zn toxicity in
rice roots (Song et al., 2011) and under Cu toxicity in A. thaliana
(Khandekar and Leisner, 2011). Similarly, the application of Si
significantly enhanced the activities of POD, SOD and CAT of pak-
choi and rice under excess Cr (Zeng et al., 2011; Zhang et al.,
2013b) and of cotton and banana under Pb stress (Li et al., 2012;
Bharwana et al., 2013). Under Zn and Fe toxicity, Si application
increased antioxidant enzymes activities in rice and cotton
(Chalmardi et al., 2014; Anwaar et al., 2014). Silicon application
enhanced the activities of non-enzymatic antioxidants (glu-
tathione (GSH), non-protein thiols (NPT) and ascorbic acid (AsA))
in rice cucumber and pakchoi under Mn and Cd stress (Shi et al.,
2005b; Song et al., 2009; Li et al., 2012; Wang et al., 2014).
On the other hand, several studies reported that Si reduced the
antioxidant enzymes activities in the presence of heavy metals. For
examples, the activities of SOD, CAT, POD and APX significantly
decreased in functional leaves of Solanum nigrum L. in the pre-
sence of Si under Cd stress as compared to Cd treatments alone
(Liu et al., 2013b). Similarly, foliar application with 2.5 mM nano-
silicon decreased POD and CAT activities in rice roots and shoots
respectively while POD and CAT activities increased in shoots and
roots respectively under Cd stress as compared to Cd treatment
alone (Wang et al., 2014). Furthermore, it was reported that Si
application significantly decreased CAT, SOD and POD activities in
roots of peanut and maize under Al and Zn stress as compared to
the same metal treatments without Si supply (Bokor et al., 2014a;
Shen et al., 2014). The root application of Si decreased POD ac-
tivities in both roots and leaves of cucumber plants under Mn
stress (Dragišić Maksimović et al., 2007). The activity of SOD and
POD was also negatively affected by the combination of Si and Zn
or As (Masarovic et al., 2012; Hu et al., 2013).
These changes in activities of antioxidant enzymes might be
due to difference in plant species, age, duration of treatment and
experimental conditions (Sharma and Dietz, 2009; Shi et al., 2010;
Hussain et al. 2015; Tang et al., 2015). Above literature showed that
Si application could notably increase plant defense system by re-
ducing oxidative damage and by altering the activities of anti-
oxidant enzymes up to a certain level of metal stress. However,
under higher metal stress this mechanism seems ineffective in
many plant species as the activities of antioxidant enzymes de-
creased under higher metal stress. Thus, it could be concluded that
Si-mediated enhancement in the activities of antioxidants works
only under mild metal stress and under higher metal stress; other
mechanisms might be actively involved in metal detoxification
than this one.
6.3. Compartmentation within plants
Several studies have observed the compartmentation of metals
in shoots and roots of plants to understand Si detoxification me-
chanisms in plants. For the first time in 1957, Williams and Vlamis
(1957) showed that Si application did not affect Mn concentration
in barley leaves but Mn was evenly distributed in leaves instead of
discrete necrotic spots, so in this way Si reduced the effect of Mn
toxicity. It has been widely reported that Si increased metal con-
centrations in plants roots as compared to shoots (Lukacova Ku-
likova and Lux, 2010; Rizwan et al., 2012; Srivastava et al., in press;
Keller et al., 2015). Gu et al. (2011) observed higher metal con-
centrations in roots followed by stem and leaves of rice plants
grown on multimetal contaminated soils. More recently, Naeem
et al. (2014) reported that in wheat plants Si application increased
Cd in roots and decreased translocation to shoots and grains. Jú-
nior et al. (2010) reported that Si enhanced the Mn percentage in
192 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
roots and decreased in shoots of rice plants as compared to Mn
only treated plants. Similarly, Shi et al. (2005b) showed that in rice
plant, Si application decreased the translocation of Cd from roots
to shoots by 33%. They showed that Cd was mainly deposited in
the vicinity of the endodermis and epidermis and Si was more
deposited in the vicinity of the endodermis than in the epidermis.
Deposition of Si in endodermis may play a role in the decrease of
Cd translocation. Similar results were also reported in wheat
plants under Cu stress (Keller et al., 2015).
Sequestration of heavy metals in metabolically less active cell
compartments, such as the cell walls, might be an important
mechanism for Si-mediated heavy metal tolerance in plants. Zhang
et al. (2008) observed that Si decreased Cd accumulation in rice
shoots by compartmentalization of Cd in the root cell walls. Liu
et al. (2009) reported that Si foliar application increased Cd con-
centration and percentage bound to cell wall of shoots but did not
affect the Cd distribution in cell wall of roots. Similarly, Vaculik
et al. (2012) reported that Si application considerably decreased
symplasmic and increased apoplasmic concentration of Cd in
maize shoots but did not affect the distribution in roots. It was
found that in the presence of Si, Mn fraction increased in the cell
wall of shoots of cucumber plants (Rogalla and Romheld, 2002;
Maksimović et al., 2012). Similar results were also reported by
Iwasaki et al. (2002) in cowpea under Mn stress. Doncheva et al.
(2009) suggested that excess Cu might be sequestrated in non-
photosynthetically active leaf epidermal cells could be a Mn tol-
erance mechanism in maize. Effect of Si on metal distribution
varies not only among plant species but also among genotypes. For
example, Shi et al. (2010) reported that in leaves of peanut culti-
vars, Si pretreatment significantly decreased Cd content in cell
organelle fractions in Luhua 11, while remain unaffected in Luzi
101 cultivar. By contrast, in Luzi 101, the reduction of Cd content by
Si pretreatment was pronounced in cell wall fractions and re-
mained unaffected in Luhua 11. Li et al. (2009) reported that Si
application in soil decreased the inorganic As concentration in
grain by 59% while increasing the concentration of dimethylarsinic
acid (DMA) by 33% but the response varies between two rice
genotypes. More recently, scanning electron microscopy (SEM)
analysis showed that As was more concentrated in tomato shoots
external tissues, epidermis and parenchyma while Si was ubiqui-
tously distributed throughout the root and shoots in Si þAs
treatments but localization varied from cultivar to cultivar (Mar-
miroli et al., 2014).
Ye et al. (2012) reported that in Kandelia obovata plant Si en-
hanced binding of Cd to the cell walls and restricted the apo-
plasmic transport of Cd in root tips. Additionally, Zhang et al.
(2014) reported that in Avicennia marina plants Si increased Cd in
the apoplasm and decreased in the symplasm of root tips but did
not affect the distribution in leaf apoplasm and symplasm. This
showed that Si-mediated changes in the distribution of Cd in the
root tips might also be an important mechanism for Si-induced Cd
tolerance. Luo et al. (2013) reported that Si application might
modify the Cd binding properties of S. nigrum root cell walls and
resultantly increased the relative proportion of ethanol-ex-
tractable, water-extractable and NaCl-extractable Cd in roots by
adding Si. Keller et al. (2015) studied the localization of Cu in
wheat roots with and without Si application. In the presence of Si,
root adsorbed Cu concentration increased especially with highest
Cu (30 mM) concentration. In the absence of Si, Cu was mainly
localized in the central cylinder of root while in the presence of Si,
Cu was mainly localized in the vicinity of root epidermis while Si
was localized mainly in the endodermis irrespective Cu treatment.
In rice plant, Gu et al. (2012) reported that Zn and Si was co-lo-
calized in the cell wall of metabolically less active tissues, espe-
cially in sclerenchyma of root and Si supply increased about 10%
the cell wall bound fraction of zinc. Thus, Si localization in the root
endodermis might serve as a barrier to block heavy metal entrance
into cells. Taken together, effects of Si on metal compartmentation
in the leaves and roots might be the crucial mechanism in metal
uptake and detoxification in plants. However, this mechanism
differ with plant species, genotypes and metal stress imposed.
Therefore, a detailed understanding of the Si effects on metal lo-
calization and transformation is needed to better understand Si-
mediated metal detoxification in plants.
6.4. Co-precipitation of silicon with metals
The co-precipitation of Si with metals in plants might be a
mechanism which reduced metal toxicity in plants. However,
controversial reports have been found in the literature related to Si
and metal co-precipitation in plants. Many studies reported Si and
metal co-precipitation in leaves and roots of many plant species.
For example, Neumann et al. (1997) reported that in Minuartia
verna, Si accumulating dicotyledon, Zn was co-precipitated as Zn
silicates in the cell walls of leaf epidermis. Neumann and Zur
Nieden (2001) also proposed Si–Zn complexes in leaves surface of
Cardaminopsis halleri grown on a Zn contaminated soil amended
with Si. Gu et al. (2012) suggested the possible effect of silicate on
the formation of Zn–Si precipitates in the cell wall of less bioactive
tissues of rice. Additionally, Gu et al. (2011) proposed that lower
Cd in rice leaves might be due to co-precipitation of Si with heavy
metals in stem. Iwasaki et al. (2002) suggested co-precipitation of
Si and Mn in leaf apoplast of cowpea plants. Oliva et al. (2011)
detected Cu in phytoliths of E. andevalensis shoots and suggested
that Si may alleviate Cu stress in shoots by reducing free Cu. Zhang
et al. (2008) reported that in rice both Si and Cd accumulated
synchronously in the border and middle of phytoliths of the
shoots.
Previous studies also showed Si and metal complex formation
in the roots. For example, da Cunha and do Nascimento (2009)
showed simultaneous presence of silica, Cd, and Zn deposits in
root mesophyll cells of maize plants and suggested Si-metal
complexes in plants. Liu et al. (2013a) and Ma et al., (2015) re-
ported the co-deposition of Si and Cd in the root cell walls via a
[Si-wall matrix]Cd complex formation might reduce the Cd uptake
by the plants suggesting in vivo detoxification of Cd in rice. Shi
et al. (2005b) reported that in rice roots Si and Cd was mainly
deposited in endodermis and reduced the cell wall porosity of
inner root tissues and they hypothesized the co-precipitation of Si
with cadmium. Cocker et al. (1998) and Wang et al. (2004) sug-
gested that Si treatment under Al stress leads to the formation of
HAS complexes in the apoplast of the root apex of maize and
wheat plants and suggested that the formation of HAS for Al de-
toxification in plants. Similarly, Prabagar et al. (2011) reported that
the Si reduced the concentration of free Al in the root cell wall, and
authors proposed the formation of aluminosilicate complexes in
the cell wall.
The literature also showed that there might be no co-pre-
cipitation of metals with Si in many plant species. For example, it
was reported that in wheat plants Cu and Cd were not detected in
leaf phytoliths (Rizwan et al., 2012; Keller et al., 2015) and sug-
gested that co-precipitation might not be a mechanism in Cu de-
toxification in wheat plants. Similarly, Collin et al. (2014) reported
that microscopic findings did not confirm co-precipitation of Si
and Cu at the root level in bamboo plants grown in hydroponics.
Dresler et al. (2015) reported that no evidence of Si–Cd complexes
was found in maize plants grown in hydroponics under Cd stress
with increasing Si levels. From the above information it can be
concluded that co-precipitation of Si with heavy metals might not
be a crucial mechanism for metal detoxification in plants. Thus,
further studies are still needed to clarify this mechanism in plants.
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
6.5. Chelation
The mechanisms by which Si mitigates heavy metal stress in
plants might be related to the chelation of flavonoid-phenolics or
organic acids with metals. It has been reported that phenol exu-
dation increased in maize plants in Siþ Al treatments as compared
to Al treatment alone and phenolics such as catechin and quer-
cetin have strong Al-chelating abilities which might be a factor
contributing to Si-enhanced Al resistance in root tip apoplast of
maize (Kidd et al., 2001; Wang et al., 2004). Similarly, Barceló et al.
(1993) reported that addition of Si increased the malic acid con-
centration in maize plants under Al stress which can reduce the Al
toxicity by chelating with malic acid. Furthormore, Collin et al.
(2014) reported that Si was not directly involved in Cu speciation
in bamboo roots but Si increased the proportion of Cu(I)S-ligands
(organic and inorganic) in leaves and these ligands can chelate Cu
and can increase the Cu sequestration in a less toxic form. Fur-
thermore, Si addition increased citrate, malate and aconitate
concentration in roots of wheat seedlings treated with 30 mM Cu
as compared to the same treatment without Si. Authors suggested
that Cu could form complex with organic acids and reduced the Cu
translocation to shoots (Keller et al., 2015). These studies showed
that Si-mediated release of chelates, those can complex metals,
might be a mechanism which could reduce the toxic effects of
metal in plants up to certain level along with other mechanisms.
However, more studies are still needed to highlight the role of Si-
mediated chelation of metals in plants or in growth media.
6.6. Modification of gene expression
To clarify the roles of Si in mitigating heavy toxicity at genes
level, Kim et al. (2014) investigated that in rice plant Si application
significantly activated OsHMA3 and OsLsi genes under Cu/Cd stress
as compared to metal treatments alone which might counteract
the negative impacts of the metal stress in plants. Similarly, Li et al.
(2008) showed that 1.5 mM Si application under Cu stress stimu-
lated the genes responsible for the production of metallothioneins
(MTs) in A. thaliana that can chelate toxic metals. COPT1 and HMA5
transporter genes were induced by Cu and Si þCu supply reduced
these genes. In addition, Si may decrease the expression of PAL
(phenylalanine ammonialyase) genes under Cu stress. However
their role in decreasing Cu toxicity is not well understood (Khan-
dekar and Leisner, 2011). More recently, Bokor et al. (2014b) re-
ported that in maize plants treated with Zn and also with Zn and Si
showed downregulation of ZmLsi1 and ZmLsi2 genes in roots and
upregulated expression level of ZmLsi6 in the first leaf and de-
creased expression of ZmLsi6 in the second leaf. Nwugo and Huerta
(2010) investigated the effect of Si on the leaf proteome of rice
plants under Cd stress and identified 60 protein spots that were
differentially regulated due to Cd and/or Si treatments. More re-
cently, Ma et al. (2015) reported that in rice plants expression of
Lsi1 gene was up regulated in the presence of Si in the medium,
whereas expression of natural resistance-associated macrophage
protein 5 (Nramp5) gene, involved in the transport of Cd, was
down-regulated. In addition, Song et al. (2014) reported that Si
application enhanced the expression of genes (Os08g02630 (PsbY),
Os05g48630 (PsaH), Os07g37030 (PetC), Os03g57120 (PetH),
Os09g26810 and Os04g38410) associated with photosynthesis in
rice under Zn toxicity. So far, mechanisms of Si-mediated allevia-
tion of heavy metal toxicity is poorly understood at the molecular
and genetic levels, more genetic experiments are required to de-
termine linkage relationships between Si and metal stress to study
expression level of genes related to transport, deposition, and
translocation of metals and Si in different plant species.
193
6.7. Structural alterations in plants
Furthermore, Si þCd supply increased length of leaves, leaf
area, root length of maize plant (Vaculik et al., 2009), and in-
creased the total root length, total root surface area of rice plants
as compared to Cd-only treated plants (Tripathi et al., 2012a,
2012b). Si application increased the plant height, root length,
number of leaves per plant and leaf area of cotton plants under Cd,
Zn and Pb stress (Bharwana et al., 2013; Farooq et al., 2013; An-
waar et al., 2014). Keller et al. (2015) reported that Si increased
root length of wheat seedlings under Cu stress. Si supply also in-
creased the total root length, total root surface area and total root
tip amount of rice plants under Zn stress (Song et al., 2011).
However, Si (5 mM) þZn (800 mM) application did not affect the
total root length, total root surface area, root volume and number
of root tips in maize plants as compared to same Zn treatment
alone (Bokor et al., 2014b). Similarly, length of primary seminal
root, leaf area of first and second leaves of maize significantly
decreased with Siþ Zn treatment as compared to the same Zn
treatment without Si supply (Bokor et al., 2014a). Similarly, Si
supply under Al stress decreased root diameter and increased root
surface area of peanut seedlings (Shen et al., 2014). Additionally, Si
under Al exposure increased the frequency of stomata and root
hairs, length of root hairs and leaf epidermal cells, and maintained
the structure and integrity of mesophyll cells and phloem as
compared to Al treatment alone (Singh et al., 2011). Similarly, Kim
et al. (2014) reported that Si decreased the leaf damage and ne-
crosis under Cu stress in rice plants and also decreased metal toxic
effects on root architecture and increased the root length as
compared with plants treated metals only.
It has also been reported that Cdþ Si treatments accelerated
suberin lamellae, Casparian bands and root vascular tissues de-
velopment. Si enhanced the tertiary endodermal cell walls for-
mation in comparison with Cd treatments alone which showed
enhanced endodermal apoplasmic barrier development in the
presence of Si in maize (Vaculik et al., 2009, 2012; Lukacova et al.,
2013). Silicon prompted the development of the apoplasmic bar-
rier in the roots of A. marina under Cd stress (Zhang et al., 2013a).
Vatehová et al. (2012) also reported the Si-mediated more ex-
tensive development of suberin lamellae in endodermis closer to
the root tips of rapeseed and Indian mustard under Cd stress. Si-
milarly, Greger et al. (2011) reported that in the presence of Si þCd
treatments, apoplasmic barriers in endodermis were formed closer
to the wheat root apex as compared to Cd-stressed wheat roots. Si
application significantly increased xylem diameter, mesophyll and
epidermis thickness, and decreased transversal area occupied by
collenchyma in maize plants under Cd and Zn stress (da Cunha and
do Nascimento, 2009). Silicon together with Cd also reduced the
abnormalities in leaf mesophyll cells and vascular bundles of rice
as compared to Cd treatment alone (Tripathi et al., 2012a, 2012b).
Also in cucumber plants, Si supply also inhibited the Mn toxicity
symptoms (Shi et al., 2005a). Similarly, Si substantially increased
the thickness of the leaf epidermal layers suggest that Mn storage
in non-photosynthetic tissue could be a Mn tolerance mechanism
in maize (Doncheva et al., 2009). Júnior et al. (2010) reported that
Si þMn supply to the rice plants decreased the leaf insertion angle
of the rice plant so improved its architecture.
There are several evidences that Si ameliorated the ultra-
structural disorders caused by chromium stress in many plant
species (Ali et al., 2013). Chromium stress caused ultrastructural
disorders in leaves and roots of barley including increased amount
of plastoglobuli, disintegrated and disappeared thylakoid mem-
branes in leaves, and increased vacuolar size, disruption and dis-
appearance of nucleus in roots (Ali et al., 2013). Further, Tripathi
et al. (2015) reported that under Si þCr(VI) treatment, suberization
and lignification was well developed and xylem and phloem were
194 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197
well arranged compared to the Cr(VI) alone treated wheat seed-
lings. Fu et al. (2012) studied the ameliorative effect of Si on rice
plants under Fe toxicity. Authors reported that exposed to Fe2 þ
toxicity, the root epidermal cells were severely injured. Cell wall
was deformed, organelles of the cytoplasm were dissolved, and
some cells died. Addition of Si along with Fe2 þ in the solution
significantly ameliorated Fe2 þ toxicity to root cells.
Silicon plays important roles in protecting photosynthetic ma-
chinery from damaging under metal stress. Silicon protected the
chloroplast ultrastructure from disorganization due to Cd, Cr and
Zn stress in cucumber, rice, barley and maize plants (Doncheva,
et al., 2009; Kaya et al., 2009; Feng et al., 2010; Ali et al., 2013;
Song et al., 2014). Added Si decreased the permeability of plasma
membrane of leaf cells of barley and maize under excess Zn (Liang
et al., 1996; Kaya et al., 2009).
In conclusion, Si application under metal stresses protected the
plant structures which might be due to compartmentation, co-
precipitation and/or chelation of heavy metals in different plant
parts and as a result free metal ion concentration decreased and
plant growth and biomass increased. However, the relevant mor-
phological and ultrastructural mechanisms still remained to be
investigated.
6.8. Other
Silicon application increased the xylem sap in rice and banana
plants under Cd, Zn and Pb stress and decreased the Cd, Zn and Pb
concentration in the xylem sap which might be due to dilution of
metals in the sap (Liang et al., 2005; Gu et al., 2012; Li et al., 2012).
This indicated that Si addition inhibited toxic metal translocation
by xylem flow. Recently, Feng et al. (2010) reported that Si supply
decreased the inhibiting effects of Cd on the enzymes of nitrogen
metabolism including nitrogen reductase (NR), glutamine syn-
thetase (GS), glutamate synthase (GOGAT) and glutamate dehy-
drogenase (GDH) in cucumber plants. Dragišić Maksimović et al.
(2007) suggested that Si nutrition modulates the metabolism and
utilization of phenols mainly at the leaf level by stimulating the
formation of Si polyphenol complexes in cucumber plants.
7. Conclusions and perspectives
Heavy metal toxicity causes huge losses in agriculture pro-
ductivity worldwide. It is widely accepted that Si can alleviate var-
ious biotic and abiotic including heavy metal stress in plants. Silicon
could reduce heavy metals uptake in various plants species and en-
hanced the plant growth and biomass. The key mechanisms evoked
include reducing active heavy metal ions in growth media, chelation
and stimulation of antioxidant systems in plants, complexation and
co-precipitation of toxic metals with Si, compartmentation and
structural alterations in plants and regulation of the expression of
metal transport genes. However, these mechanisms might be asso-
ciated with plant species, genotypes, metal elements, growth con-
ditions, duration of the stress imposed and so on. Therefore, the
generalization of Si-mediated alleviation of metal toxicity should be
therefore made with caution. This review could contribute to better
understanding of the mechanisms of Si-mediated enhanced metal
tolerance of plants as well as in increasing productivity of crops
under stress conditions. However, more work needs to be done to
explore fully the mechanisms involved.
We anticipated that there would be a growing interest to study
the mechanisms of Si-mediated heavy metal tolerance in plants in
near future, so we identify the next areas as the ones warranting
research. Current knowledge of Si functions under metal toxicity is
developing especially in individual plant species. However, there is
still need to better understand its function in more species under
different environmental conditions to validate the Si-mediated
alleviation of metal toxicity on large scale.
We reviewed that most experiments have utilized the Si under
hydroponic conditions and with a single metal toxicity under
controlled conditions. This can result overestimation of metal
uptake and translocation. There is need to study the mechanisms
under naturally contaminated soils as the soil is a complex system
and these soils may have mixed contamination. Such studies will
help to use Si in farming practices because in the field many heavy
metals could be simultaneously present in the soil. For silicon and
metal toxicity, most of the experiments are conducted in soil un-
der short term, which poses an interrogation on long-term effect
of Si on these heavy metals. In fact, it could be expected that, due
to aging processes, the ability of silicates to sequester heavy metals
decrease with time. More research will be needed to understand
the aging process in soil with application of silicates.
Taken together, well-designed, large-scale and long-term field
trials are required to evaluate the feasibility of Si application for
the remediation of metal contaminated soils and economic feasi-
bility of different Si sources should also be investigated.
Acknowledgments
Financial support from Government College University Faisa-
labad and HEC (Higher Education Commission) of Pakistan (IPFP/
HRD/HEC/2014/1035)is gratefully acknowledged.
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