Ecotoxicology and Environmental Safety 119 (2015) 186–197

Contents lists available at ScienceDirect

Ecotoxicology and Environmental Safety

Review

Mechanisms of silicon-mediated alleviation of heavy metal toxicity

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: [email protected] (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) 186–197 187

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

1. Introduction in the soil are usually present as SiO2 and in various alumino-si-
licate forms. Silicon dioxide comprises about 50–70% of the soil
Soil contamination is indeed considered one of the main mass (Ma and Yamaji, 2006). External sources of Si include calcium
threats to agricultural soil as identified in the European Union soil and magnesium silicates, silicate slag, dolomite, rock phosphate
communication (CEC, 2002). This contamination originates from and diatomite (Savant et al., 1997; Guntzer et al., 2012; Rizwan
natural sources by means of mineral dissociation, weathering of et al., 2012). Silicon compounds exist both in the liquid and in solid
parent material and atmospheric deposition as well as anthro- phase in the soil. In the solid phase, Si compounds can be divided
pogenic sources related to mining, industrial emissions, disposal into amorphous, poorly crystalline and crystalline forms. Amor-
or leakage of industrial wastes, application of sewage sludge to phous silica (ASi) is comprised of both ASi from plants including
agricultural soils, fertilizer and pesticide use (Nagajyoti et al., phytoliths and other inorganic forms of ASi (Sauer et al., 2006) and
2010). Heavy metals like cadmium (Cd), lead (Pb), chromium (Cr), it is considered to be the first pool of available Si for plants
copper (Cu), manganese (Mn) and zinc (Zn) contribute the major (Alexandre et al., 1997). The amount of biogenic silica (phytoliths)
share of soil contamination. Due to the potential toxicity and high in soils ranges from 0.03 to 0.06 wt% (Desplanques et al., 2006).
persistence of heavy metals, soils polluted with such elements Grassland soils contain phytoliths up to only 1–3% of total Si pool
create an environmental problem that threats the plant, animal (Blecker et al., 2006). The phytoliths are mainly composed of about
and human health (do Nascimento and Xing, 2006; Adrees et al., 92 wt% silica and 6 wt% water with small amounts of carbon and
2015). traces of Al and Fe (Meunier et al., 1999). In liquid phase, Si is
Among heavy metals, some metals such as Cd, Pb and Cr have present as mono- and poly-silicic acids, complexed with organic
no known biological role while others such as Cu, Zn and Mn are and inorganic compounds (Cornelis et al., 2011). In natural soil
required in small amount for normal plant growth and develop- solution, Si is mainly present in the form of uncharged orthosilicic
ments but are extremely toxic to plants and animals slightly larger acid, H4SiO4 ranging from 0.1 to 0.6 mM (Epstein, 1994; Sommer
than the required concentrations (Kabata-Pendias and Pendias, et al., 2006) and it is thought to be the only form which is taken up
2001). It has been widely reported that accumulation of heavy by plants (Epstein, 1994, 1999; Ding et al., 2005).
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 3. Silicon uptake and accumulation in plants
photosynthesis (Wuana and Okieimen, 2011; Adrees et al., 2015;
Ali et al., 2015a, 2015b). In an excess, heavy metals also affect the All plants grown in soil contain some Si in their tissues varying
accumulation and translocation of essential elements by plants from 0.1% to 10% by weight of plants (Epstein, 1994, 1999; Ma and
(Wagner, 1993; Wuana and Okieimen, 2011; Zia-ur-Rehman et al., Yamaji, 2008). Silicon uptake by plants varies greatly between
2015). Consequently, there is growing concern related to heavy species and cultivars, i.e., gramineous vs leguminous plants, and
metal pollution issues worldwide in order to reduce toxic metal plants are classified as high-, intermediate-, and non-Si-accumu-
bioavailability and plant uptake for increasing plant growth and lators (Takahashi et al., 1990; Ma et al., 2001). However, Si con-
yield and ultimately safe food production. centration in plant tissues depends upon the characteristics of Si
Silicon is a very important part of the earth's crust and it uptake and transport, variability between species and genotypes
consists about 28% of the earth's crust (Sommer et al., 2006). within a species (Epstein, 1994; Ma and Yamaji, 2008). Plant roots
However, Si is only 0.03% of the biosphere (Fauteux et al., 2005). In take up Si in the form of un-dissociated H4SiO4 (Casey et al., 2003;
fact, Si is accumulated in many plants up to 10% by weight (Hod- Ding et al. 2008) and Si uptake mechanisms differ between plant
son et al., 2005) that is greater than some macronutrients (Epstein, species (Ma and Yamaji, 2006). The mechanisms of Si absorption
1994). Silicon has been shown to alleviate the deleterious effects of by roots are still controversial. However, there are three possible
heavy metals in plants grown on contaminated soils (Chen et al., mechanisms of Si uptake by higher plants namely passive, active
2000). Experiments have demonstrated that certain crops benefit and rejective (Ma et al., 2004; Mitani and Ma, 2005). Passive up-
significantly from Si application (Takahashi et al., 1990). Various take of Si takes place along the transpiration stream and it is
beneficial effects of Si have been identified in plants (Epstein, 1994, shown that most dicotyledonous plants absorb Si passively (Ma
1999). Various studies describe the ameliorative effect of Si ap- et al., 2001). Active Si uptake is dominant in many plant species
plication on plants under heavy metals or dangerous toxic ele- such as rice, maize, sugarcane and wheat (Casey et al., 2003; Rains
ments, like Al, Cd, Pb, Cr or Cu (da Cunha and do Nascimento, et al., 2006). Transporters responsible for Si uptake by roots have
2009; Ali et al., 2013; Li et al., 2013; Shen et al., 2014; Keller et al., been identified in different plant species such as rice, barley,
2015). Thus, use of Si to enhance plant growth and alleviate heavy maize, wheat and cucumber (Ma et al., 2007, 2011; Chiba et al.,
metals toxicity is predicted to become an emerging trend in the 2009; Mitani et al., 2009).
agriculture in near future. This review article summarizes the re- Once absorbed by roots, Si moves to the shoots by transpira-
cent progress in understanding the mechanisms of Si-mediated tional water flow via the xylem (Ma et al., 2006). In many plants,
heavy metal tolerance in 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
2. Silicon in soil (Casey et al., 2003; Mitani and Ma, 2005). Recently, Si transporters
responsible for xylem unloading in leaves (Lsi6) and inter-vascular
Silicon is the second most abundant element in the soil ranging transport have been identified (Yamaji et al., 2008, 2012). After
from 50 to 400 gSi kg  1 of soil (Kovda, 1973). Silicon compounds 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, ameliorative effect of Si on the toxicity of certain metals such as
2002). Once deposited in this form, Si is immobile and not redis- Zn, Mn, Al, Cu and Cd in many plant species. Here, we reviewed
tributed (Hodson and Sangster, 1990). Deposition of Si takes place the recent progress on the effects of Si on metal uptake, photo-
in different parts of plant such as epidermis of shoots but can also synthetic pigments, mineral nutrients uptake and plant growth
occur in cell walls of root endodermis (Lux et al., 2003; Keller et al., and biomass (also see Fig. 1).
2015). However, phytoliths varies greatly between individual plant
families with respect to type, composition and localization, which 5.1. Decrease in metal uptake by plants
depends upon plant species, and environmental conditions
(Guntzer et al., 2012; Li et al., 2014). 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
4. Protective role of silicon tolerance to toxic metals in many plant species by reducing the
uptake and translocation of metals. Silicon application decreased
Although Si is not considered as an essential element for plants, Cd concentration in many plant species such as maize (Liang et al.,
it has been proved to be beneficial for the growth and develop- 2005; Dresler et al., 2015), rice (Shi et al., 2005b; Li et al., 2008),
ment of many plant species (Epstein, 1994). Experiments showed wheat (Rizwan et al., 2012; Naeem et al., 2014; Hussain et al.,
that plants supplied with Si resist lodging by increasing mechan- 2015), cotton (Farooq et al., 2013), peanut (Shi et al., 2010) and in
ical strength of plants enabling them to achieve and maintain an chinese cabbage (Brassica chinensis L.) (Song et al., 2009). It has
erect habit. This might be due to association of Si with cell walls been reported that Si not only reduced Cd uptake by the plants but
which increased the rigidity of plant cell walls (Raven, 1983). also reduced shoot to grain translocation of Cd (Naeem et al., 2014;
Epidermal tissue deposition of Si also protects plants against ex- Hussain et al., 2015). Si-mediated decrease in Cu uptake and
cessive loss of water by transpiration (Emadian and Newton, 1989). translocation was observed in wheat (Nowakowski and Now-
Beneficial effects of Si are studied in many plant species such as akowska, 1997; Keller et al., 2015). Silicon application decreased Al
wheat, rice, cucumber, maize and bamboo, in particular, under in roots, stem and leaves of peanut and rice seedlings (Singh et al.,
stressful conditions (Rogalla and Romheld, 2002; Ma and Taka- 2011; Shen et al., 2014). Furthermore, Si decreased Cr concentra-
hashi, 2002; Shi et al. 2005a; Zhang et al., 2008; Vaculik et al., tion in shoots and roots of rice, barley and wheat (Zeng et al., 2011;
2009; Feng et al., 2010; Collin et al., 2014). Silicon protects the Ali et al., 2013; Tripathi et al., 2015). Application of Si significantly
plants from a number of biotic stresses such as diseases i.e., blast suppressed Zn accumulation in various plant parts, i.e., roots, and
and powdery mildew and pest i.e., stem borer and plant hopper leaves of cotton, maize (Kaya et al., 2009; Anwaar et al., 2014;
(Ma and Yamaji, 2006). Silicon also protects plants from a number Bokor et al., 2014a, 2014b). In addition, it was shown that a sig-
of abiotic stresses such as heavy metals, radiation, heat and nificant negative correlation exist between external Si supply and
drought stresses (Bélanger et al., 2003; Côté -Beaulieu et al., 2009; arsenate and/or arsenite uptake and concentration in rice seed-
Epstein, 2009). 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,
5. Silicon-mediated alleviation of metal toxicity in plants 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
Heavy metal toxicity negatively affects biomass production and both Si and As share the same influx transporter (Low silicon rice 1,
grain yield in almost all major field grown crops (Nagajyoti et al., Lsi1) in rice as suggested by Guo et al. (2009). However, Si effect on
2010; Adrees et al., 2015). Several studies reported the metal uptake and translocation varies with plant species and

Fig. 1. Hypothetical mechanisms for Si-mediated alleviation of heavy metal toxicity in plants (for details see the text).
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197 189

genotypes (Liu et al., 2013b; Marmiroli et al., 2014; Hussain et al., 5.2. Enhancement in gas exchange attributes and photosynthetic
2015). pigments
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- Positive effects of Si on chlorophyll biosynthesis and photo-
cium ions and reduced Al uptake by plants (Hammond et al., synthetic machinery under metal toxicity have been widely re-
1995). Silicon may stimulate production of root exudates which ported. For example, Siþ Cd application increased chlorophyll a,
can chelate metals and reduce their uptake by roots (Kidd et al., chlorophyll b and carotenoid contents in leaves as compared to
2001). In addition, this reduction in metal uptake can also be ex- Cd-only treatments in maize (Malčovská et al., 2014), wheat
plained by the fact that Si reduced the apoplasmic transport of (Rizwan et al., 2012; Hussain et al., 2015), cucumber (Feng et al.,
metals by decreasing free metal concentration in the apoplasm 2010) and rice (Nwugo and Huerta, 2008). Silicon application in-
(Iwasaki et al., 2002; Rogalla and Romheld, 2002). Moreover, the creased chlorophyll contents under Al, Cr and As toxicity in rice,
physical barrier formed by the deposition of Si in the vicinity of mongbean, wheat and barley (Yang et al., 1999; Singh et al., 2011;
the endoderm may reduce the cell wall porosity of inner root Ali et al., 2013; Sanglard et al., 2014; Tripathi et al., 2015). Si ap-
tissues, thus reducing the metal concentration in the xylem (Shi plication in hydroponics enhanced the activity of gas exchange
et al. 2005a; da Cunha and do Nascimento, 2009; Keller et al., characteristics (net photosynthetic rate, stomatal conductance,
2015). Similarly, Si decreased apoplasmic transport of Cd through transpiration rate, water use efficiency), chlorophyll, and car-
the enhanced adsorption of Cd on the cell walls (Ye et al., 2012). otenoids contents under Cd stress in cotton, rice and cucumber
Silicon accumulation in the roots endodermis may reduce the (Nwugo and Huerta, 2008; Feng et al., 2010; Farooq et al., 2013).
mobility of heavy metals such as Al (Wang et al., 2004) and Cu Similarly, Si enhanced gas exchange characteristics under Al and
(Keller et al., 2015). Additionally, it has been reported that in Si Cr stress in peanut and barley (Ali et al., 2013; Shen et al., 2014), in
treatments the Si-accumulating ( þSi) cells significantly inhibited cotton under Pb stress (Bharwana et al., 2013) and in rice under Zn
the net Cd2 þ influx, compared with that in Si-limiting (  Si) cells stress (Song et al., 2014).
(Liu et al., 2013a). Decrease in metal uptake by the plants at least Similarly, Hu et al. (2013) reported that Si supply increased net
partially related to development of apoplasmic barriers and ma- photosynthetic rate and reduced stomatal limitation in rice under
turation of vascular tissues root (Greger et al., 2011; Vaculik et al., arsenic (As) stress. Furthermore, Sanglard et al. (2014) studied
detailed gas exchange measurements with chlorophyll fluores-
2012).
cence analysis to examine the effects of Si nutrition on photo-
It has been widely reported that increasing Si treatments in
synthetic performance in rice plants under As (arsenite) toxicity.
hydroponics or in soil increased Si uptake in shoots and roots of
Authors reported that Si considerably reverted As-mediated im-
many plant species while increasing metal concentrations in the
pairment in carbon fixation and leaf conductance at the stomata
growth medium reduced Si uptake by the plants (Shi et al., 2005b;
and mesophyll levels and the response was time and genotype-
Li et al., 2008; Guo et al., 2009; Naeem et al., 2014; Keller et al.,
dependent manner. Furthermore, Si increased photosynthetic ac-
2015). Therefore, it could be concluded that Si reduced the heavy
tivity, chlorophyll fluorescence, in many plant species under metal
metal toxicity in plants by decreasing metal uptake and blocking
stress such as in barley and wheat under Cr stress (Ali et al., 2013;
metal transfer in plants. It has also been reported that Si appli-
Tripathi et al., 2015). Moreover, Nwugo and Huerta (2010) reported
cation increased metal accumulation by plants. For example, Si
that in rice leaves Si enhanced the Cd tolerance by increasing in-
application in soil in the form calcium silicate (CaSiO3) increased
stantaneous water-use-efficiency, carboxylation efficiency of ri-
Cd and Zn accumulation in maize plants (da Cunha and do Nas-
bulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO), and
cimento, 2009). Liang et al. (2005) reported that total Cd was
light-use efficiency.
significantly higher in the shoots and roots of maize plants in the
In general, positive effect of Si on photosynthetic machinery
Si-amended Cd treatments than in the non-Si-amended Cd treat-
might be due to lower uptake of metal by the plants (as reported
ments. Similarly, Vaculik et al. (2009, 2012) showed that Si did not in Section 5.1) which reduced the damage to photosynthetic ma-
reduce the total Cd uptake in maize plant. In Chinese Kale, po- chinery and/or due to activation of plant defense system and
tassium silicate application in soil increased the Si contents in morphological, anatomical and ultrastructual alterations in pho-
shoots while increased Cd concentration in roots without affecting tosynthetic apparatus (see the details later in the text).
Cd concentration in leaves as compared to control (Lu et al., 2014).
Additionally, Cocker et al. (1998) reported that total Al in- 5.3. Changes in mineral nutrients uptake and plant growth and
creased in wheat plants in the presence of Si, suggesting a Si- biomass
mediated mechanism in plants. Furthermore, Collin et al. (2013)
reported that in bamboo plants Cu concentration was higher in Mineral nutrients are the major constituents of the plant
roots followed by stem and leaves and Si did not alter the ab- structural component and provide mechanical, biochemical, and
sorption of Cu by plants grown in hydroponics. Similarly, Si did not physical strengths to the plants. Mineral nutrients also play a
affect the Mn concentration in roots and leaves of cucumber plants major role in the growth and development of plants and heavy
(Dragišić Maksimović et al., 2007). This showed that Si-mediated metals may interfere with essential nutrient uptake and transport,
alleviation of metal phytotoxicity is not only due to the decreased thereby disturbing the mineral nutrition composition. Therefore,
metal uptake by plants but there might be Si-mediated mechan- informations, qualitative and quantitative, about the mineral up-
isms of metal detoxification in plant. Decrease in metal uptake by take and transport with Si application under metal stress may
plants might be due to immobilization of metals in the growth provide a deeper insight of the mechanisms by which Si reduce
media and/or modulation of influx transporters which reduced metal toxicity in plants. Silicon plays an important role in the
metal transport from root surface to root xylem. Decrease in metal absorption of nutrients by the plants under metal stress. Si ap-
translocation from roots to shoot and grains might be due to plication in hydroponic solution increased the content and accu-
structural alterations in shoots and roots and/or co-precipitation, mulation of micro-, Zn and Mn, and macro-nutrients, Ca, Mg, P and
chelation and compartmentation of metals in plants. These Si- K, by wheat plants under Cr, Cd and Cu (Rizwan et al., 2012; Keller
mediated metal tolerance mechanisms in plants are described et al., 2015; Tripathi et al., 2015). Similarly, Wang et al. (2014)
latter in the text (mechanisms of Si-mediated metal detoxification reported that foliar application with nano-Si increased Mg, Fe, and
in plants). 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 enhancing photosynthesis and uptake of mineral elements. These
roots of rice as compared to Al treatment alone while Si did not positive effects of Si might be due to different mechanisms un-
affect the Mn concentration in both parts (Singh et al., 2011). derlying at the soil and plant levels. A good understanding of the
Moreover, Si influenced mineral nutrient concentrations, either as mechanisms of Si-mediated metal detoxification in plants is very
a main effect or as an interactive effect, in zinnia (Zinnia elegans) important for the targeted application of Si. Silicon-mediated
and Erica andevalensis plants under Cu stress (Frantz et al., 2011; metal detoxification mechanisms have been extensively studied in
Oliva et al., 2011). Under Zn toxicity, Si þZn application increased many plant species. At soil level, these mechanisms may include
K, P and Fe in maize ad rice seedling as compared to Zn stress immobilization of metals in the soil. At plant levels, these me-
alone (Kaya et al., 2009; Mehrabanjoubani et al., 2014). chanisms include reduction in oxidative stress by enhancing the
Although Si application increased mineral nutrient under dif- activities of antioxidant enzymes, structural alterations in different
ferent metal stress but recently Bokor et al. (2014b) reported that in parts of plants, compartmentation of metals into metabolically
maize plants Si application decreased mineral elements Mn, Fe, Ca, inactive parts, co-precipitation of metals with Si, chelation and
P, Mg, Ni, Co, and K in shoots and roots in Siþ Zn treatment as modification of gene expression. The following sections, we dis-
compared to the corresponding Zn treatment without Si. This cussed these mechanisms in detail in the light of recent reports.
showed that homeostatic network of mineral elements was dis-
rupted and caused negative alterations in mineral nutrition. Taken 6.1. Immobilization of toxic metal in the growth media
together, Si could reduce metal toxicity in plants by the interaction
with other elements but there is still need to explore the me- Silicon-mediated alleviation of metal toxicity to plants might
chanisms of mineral nutrient absorption in the presence of Si in be due to an external plant effect by decreasing availability of
multi-metal contaminated and texturally different soils. Moreover, phytotoxic metals in the culture media (Liang et al., 2005; da
it remains for future studies why this positive or negative correla- Cunha et al., 2008; Naeem et al., 2014). It has been shown that Si
tion occurred between Si and mineral nutrients under different application in the soil affects the soil properties which in turn
metal toxicity and study expression level of other transporter genes. control heavy metals availability to plants (Liang et al., 2007;
Role of Si in the growth and biomass of plants has been widely Rizwan et al., 2012). Among soil factors, pH and organic matter are
accepted. Si supply may increase the biomass of plants under two of the most important factors that control metal availability
metal stress and may decrease the metal toxicity by dilution effect and it has been shown that Si decreased metal bioavailability by
(the same uptake but larger biomass). However, this mechanism is increasing soil pH (Chen et al., 2000; Morikawa and Saigusa, 2002;
not well understood and is still controversial. Several authors have Liang et al., 2005; Treder and Cieslinski, 2005; Gu et al., 2011). Li
observed beneficial effects of Si on plants biomass under heavy et al. (2012) reported that addition of sodium metasilicate
metal stress in soil or in nutrient solution. Si supply increased the (800 mg kg  1 Si) in Pb contaminated soil significantly increased
dry weight of both shoots and roots of many plant species under soil pH and decreased the proportion of exchangeable Pb in soil,
Cd stress including maize (Liang et al., 2005; da Cunha and do thus reducing Pb bioavailability but the affect was not clear at
Nascimento, 2009; Vaculik et al., 2009), wheat (Rizwan et al., lower (100 mg kg  1) amendments. Additionally, Rizwan et al.
2012; Naeem et al., 2014), strawberry (Treder and Cieslinski, 2005) (2012) reported that ASi application in the soil slightly increased
and rice (Nwugo and Huerta, 2008; Zhang et al., 2008; Gu et al., soil pH and reduced bioavailable Cd in the soil. Silicon application
2011; Tripathi et al., 2012a, 2012b; Srivastava et al., in press). In increased Si and decreased pH and Cd in the soil solution. How-
addition, Si supply increased the shoot and root dry weights under ever, Naeem et al. (2014) reported that calcium silicate,
Al stress in maize (Corrales et al., 1997), rice (Hara et al., 1999; 150 mg kg  1, decreased plant available soil Cd without affecting
Singh et al., 2011), mongbean (Yang et al., 1999) and barley soil pH. Similarly, da Cunha et al. (2008) reported no change in soil
(Morikawa and Saigusa, 2002). Similarly, Si supply increased plant pH associated with decrease in bioavailable Cd concentration in
biomass under Cr stress in barley (Ali et al., 2013), pakchoi (B. soil. More recently, it was reported that sodium silicate amend-
chinensis L.) (Zhang et al., 2013a, 2013b), wheat (Tripathi et al., ment in the soil significantly increased soil pH and decreased Cd
2015) and rice (Zeng et al., 2011). Recently it has been shown that and Cr bioavailability compared to control (Zhang et al., 2013b; Lu
Si supply also increased plant biomass of wheat, Arabidopsis et al., 2014).
thaliana and E. andevalensis under Cu stress grown in hydroponics Silicon can also change the speciation of metals in soil solution
(Khandekar and Leisner, 2011; Oliva et al., 2011; Keller et al., 2015). by the formation of silicate complexes (Ma et al., 1997; Liang et al.,
Silicon application also positively affected the biomass of maize 2007; Putwattana et al., 2010). It has been reported that the higher
and rice under Zn stress (Kaya et al., 2009; Song et al., 2011, 2014; Si concentration due to added furnace slag reduced bioavailable
Gu et al., 2012; Mehrabanjoubani et al.. 2014). Contrary, it was Cd. In addition, more Cd was found in the form of oxides or ad-
reported that 5 mM Si þ150 mM Zn in hydroponic reduced shoot sorbed Fe–Mn oxides bound and organic matter fractions in the Si-
and roots biomass of sorghum as compared to corresponding Zn amended soil (Chen et al., 2000; Liang et al., 2005). Hara et al.
treatment during 20 days (Masarovic et al., 2012). Similarly, 5 mM (1999) reported that Si changed the chemical forms of Al in the
Si þ800 mM Zn addition decreased shoot and root biomass of solution and Hodson and Evans (1995) hypothesized that Al
maize plants, grown in hydroponics for 10 days, as compared to formed hydroxyaluminosilicate (HAS) species in solutions or
same Zn treatment without Si (Bokor et al., 2014a, 2014b). growth media by the addition of Si which seems to contribute Si-
In general, increase in plant growth and biomass might be due mediated detoxification of Al in plants. However, Cocker et al.
to decrease in toxic metal uptake by plants and/or increase in (1998) did not observed significant formation of HAS in the growth
nutrient uptake by plants and increase in photosynthetic pigments media. Zhang et al. (2013b) reported that addition of Si markedly
and maintenance in the structure of photosynthetic machinery. decreased the proportion of exchangeable Cr in Cr-contaminated
Overall, Si is beneficial to plants under metal toxicity and in- soil by increasing the proportion of precipitation-bound, organic
creased plant biomass under metal stress. matter bound Cr fraction, thus reducing Cr availability in the soil.
Silicon application in the form of calcium silicate also altered
6. Mechanisms of Si-mediated metal detoxification in plants the Cd and Zn distribution in the soil and both metals were found
in more stable fractions such as complexed with organic matter
In the above section, we reported that Si application reduced and crystalline iron oxides (da Cunha et al., 2008). Gu et al. (2011)
the metal uptake by plants and enhanced the plant growth by reported that Si rich amendments immobilized Cu, Cd and Zn in
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197 191

multi-metal contaminated acidic soils by increasing soil pH. They metal stress. Si also stimulated the antioxidant enzymes under Mn
also showed that metals were mainly deposited as their silicates, toxicity in cucumber (Shi et al., 2005b) and Mn-tolerant (Zhu-
phosphates and hydroxides in amended treatments. Recently, liangyou 99) cultivar of rice but decreased in Mn-sensitive (Xin-
Shim et al. (2014) reported that corn cob silica application in xiangyou 640) cultivar of rice (Li et al., 2012), under Zn toxicity in
contaminated soil reduced metal mobility in the soil and x-ray rice roots (Song et al., 2011) and under Cu toxicity in A. thaliana
diffraction data indicated the formation of insoluble lead silicate in (Khandekar and Leisner, 2011). Similarly, the application of Si
soil. The above studies suggest an external interaction between Si significantly enhanced the activities of POD, SOD and CAT of pak-
and heavy metals. Taken together, Si application can immobilize choi and rice under excess Cr (Zeng et al., 2011; Zhang et al.,
toxic metals in the soil by increasing soil pH and changing metal 2013b) and of cotton and banana under Pb stress (Li et al., 2012;
speciation in soil. The above studies showed that the metal spe- Bharwana et al., 2013). Under Zn and Fe toxicity, Si application
ciation and pH was observed in the bulk soil, soil which is not part increased antioxidant enzymes activities in rice and cotton
of the rhizosphere, after crop harvest. However, pH and metal (Chalmardi et al., 2014; Anwaar et al., 2014). Silicon application
speciation in rhizosphere, the narrow region of soil that is directly enhanced the activities of non-enzymatic antioxidants (glu-
influenced by root secretions and associated soil microorganisms, tathione (GSH), non-protein thiols (NPT) and ascorbic acid (AsA))
and in the soil solution needs to be explored to better understand in rice cucumber and pakchoi under Mn and Cd stress (Shi et al.,
Si-mediated metal immobilization in the growth media and up- 2005b; Song et al., 2009; Li et al., 2012; Wang et al., 2014).
take by plants. Moreover, there is still a need to evaluate the effect On the other hand, several studies reported that Si reduced the
of more Si amendments/sources on the metal speciation in the antioxidant enzymes activities in the presence of heavy metals. For
soil. examples, the activities of SOD, CAT, POD and APX significantly
decreased in functional leaves of Solanum nigrum L. in the pre-
6.2. Enhancement in antioxidant defense system sence of Si under Cd stress as compared to Cd treatments alone
(Liu et al., 2013b). Similarly, foliar application with 2.5 mM nano-
Oxidative stress may occur in plants when they are exposed to silicon decreased POD and CAT activities in rice roots and shoots
various environmental stresses, both biotic and abiotic, including respectively while POD and CAT activities increased in shoots and
heavy metal stress (Adrees et al., 2015; Ali et al., 2015a, 2015b; roots respectively under Cd stress as compared to Cd treatment
Habiba et al., 2015; Noman et al., 2015). However, Si application alone (Wang et al., 2014). Furthermore, it was reported that Si
may reduce oxidative stress in plants by reducing the production application significantly decreased CAT, SOD and POD activities in
of reactive oxygen species (ROS) and by enhancing the activities of roots of peanut and maize under Al and Zn stress as compared to
antioxidant enzymes. For example, it was reported that Si de- the same metal treatments without Si supply (Bokor et al., 2014a;
creased the contents of malondialdehyde (MDA), hydrogen per- Shen et al., 2014). The root application of Si decreased POD ac-
oxide (H2O2) and electrolytic leakage (EL) in shoots and roots of tivities in both roots and leaves of cucumber plants under Mn
cotton plants under Cd, Zn and Pb stress (Bharwana et al., 2013; stress (Dragišić Maksimović et al., 2007). The activity of SOD and
Farooq et al., 2013; Anwaar et al., 2014). Silicon decreased MDA POD was also negatively affected by the combination of Si and Zn
concentration in Nigella sativa, peanut, pakchoi and rice under Cd or As (Masarovic et al., 2012; Hu et al., 2013).
stress (Song et al. 2009; Shi et al., 2010; Kim et al., 2014; Rad et al., These changes in activities of antioxidant enzymes might be
2014; Wang et al., 2014) and in peanut under Al stress (Shen et al., due to difference in plant species, age, duration of treatment and
2014). Similarly, Liu et al. (2013b) reported that Si application re- experimental conditions (Sharma and Dietz, 2009; Shi et al., 2010;
duced the H2O2 and EL in S. nigrum seedlings under Cd stress. Hussain et al. 2015; Tang et al., 2015). Above literature showed that
Silicon application decreased H2O2, superoxide anion (O2∙−), and Si application could notably increase plant defense system by re-
TBARS (thiobarbituric acid reactive substances) contents in leaves ducing oxidative damage and by altering the activities of anti-
and roots of maize and rice plants under Cd stress (Malčovská oxidant enzymes up to a certain level of metal stress. However,
et al., 2014; Srivastava et al., in press). Similarly, Si application under higher metal stress this mechanism seems ineffective in
decreased H2O2 and MDA contents in spinach, rice and wheat many plant species as the activities of antioxidant enzymes de-
shoots and roots under Cd, Zn, Fe, B, As and Mn toxicity (Gunes creased under higher metal stress. Thus, it could be concluded that
et al., 2007a, 2007b; Song et al., 2011; Li et al., 2012; Tripathi et al., Si-mediated enhancement in the activities of antioxidants works
2012a, 2012b, 2013; Chalmardi et al., 2014). Furthermore, Si re- only under mild metal stress and under higher metal stress; other
duced the TBARS contents in leaves and roots of rice under Cr mechanisms might be actively involved in metal detoxification
stress (Zeng et al., 2011). than this one.
Plants have developed a complex antioxidative defense system
including both enzymatic and non-enzymatic antioxidants (Suzuki 6.3. Compartmentation within plants
et al., 2011; Gill et al., 2015). Stimulation of antioxidants under
metal stress appears a mechanism that accounts for increased Several studies have observed the compartmentation of metals
metal tolerance in plants. However, antioxidant enzymes activities in shoots and roots of plants to understand Si detoxification me-
decreased under higher metal stress (Ehsan et al. 2014; Adrees chanisms in plants. For the first time in 1957, Williams and Vlamis
et al., 2015). Silicon supply may enhance the activity of antioxidant (1957) showed that Si application did not affect Mn concentration
(e.g. superoxide dismutase (SOD), peroxidases (POD), catalase in barley leaves but Mn was evenly distributed in leaves instead of
(CAT), ascorbate peroxidase (APX) under metal stress to help discrete necrotic spots, so in this way Si reduced the effect of Mn
plants to cope with metal stress. toxicity. It has been widely reported that Si increased metal con-
This Si stimulation effect on antioxidants has been observed centrations in plants roots as compared to shoots (Lukacova Ku-
under Cd stress in maize (Lukacova et al., 2013), wheat (Hussain likova and Lux, 2010; Rizwan et al., 2012; Srivastava et al., in press;
et al., 2015), cotton (Farooq et al., 2013), pakchoi (Song et al., Keller et al., 2015). Gu et al. (2011) observed higher metal con-
2009), rice (Tripathi et al., 2012a, 2012b; Srivastava et al., in press) centrations in roots followed by stem and leaves of rice plants
and peanut (Shi et al., 2010). Khodarahmi et al. (2012) reported grown on multimetal contaminated soils. More recently, Naeem
that in cucumber cultivars Si application increased CAT activity in et al. (2014) reported that in wheat plants Si application increased
Negin cultivar under Cd stress but did not affect in Super Dominus Cd in roots and decreased translocation to shoots and grains. Jú-
cultivar which showed cultivar dependent response of Si under 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 endodermis might serve as a barrier to block heavy metal entrance
only treated plants. Similarly, Shi et al. (2005b) showed that in rice into cells. Taken together, effects of Si on metal compartmentation
plant, Si application decreased the translocation of Cd from roots in the leaves and roots might be the crucial mechanism in metal
to shoots by 33%. They showed that Cd was mainly deposited in uptake and detoxification in plants. However, this mechanism
the vicinity of the endodermis and epidermis and Si was more differ with plant species, genotypes and metal stress imposed.
deposited in the vicinity of the endodermis than in the epidermis. Therefore, a detailed understanding of the Si effects on metal lo-
Deposition of Si in endodermis may play a role in the decrease of calization and transformation is needed to better understand Si-
Cd translocation. Similar results were also reported in wheat mediated metal detoxification in plants.
plants under Cu stress (Keller et al., 2015).
Sequestration of heavy metals in metabolically less active cell 6.4. Co-precipitation of silicon with metals
compartments, such as the cell walls, might be an important
mechanism for Si-mediated heavy metal tolerance in plants. Zhang The co-precipitation of Si with metals in plants might be a
et al. (2008) observed that Si decreased Cd accumulation in rice mechanism which reduced metal toxicity in plants. However,
shoots by compartmentalization of Cd in the root cell walls. Liu controversial reports have been found in the literature related to Si
et al. (2009) reported that Si foliar application increased Cd con- and metal co-precipitation in plants. Many studies reported Si and
centration and percentage bound to cell wall of shoots but did not metal co-precipitation in leaves and roots of many plant species.
affect the Cd distribution in cell wall of roots. Similarly, Vaculik For example, Neumann et al. (1997) reported that in Minuartia
et al. (2012) reported that Si application considerably decreased verna, Si accumulating dicotyledon, Zn was co-precipitated as Zn
symplasmic and increased apoplasmic concentration of Cd in silicates in the cell walls of leaf epidermis. Neumann and Zur
maize shoots but did not affect the distribution in roots. It was
Nieden (2001) also proposed Si–Zn complexes in leaves surface of
found that in the presence of Si, Mn fraction increased in the cell
Cardaminopsis halleri grown on a Zn contaminated soil amended
wall of shoots of cucumber plants (Rogalla and Romheld, 2002;
with Si. Gu et al. (2012) suggested the possible effect of silicate on
Maksimović et al., 2012). Similar results were also reported by
the formation of Zn–Si precipitates in the cell wall of less bioactive
Iwasaki et al. (2002) in cowpea under Mn stress. Doncheva et al.
tissues of rice. Additionally, Gu et al. (2011) proposed that lower
(2009) suggested that excess Cu might be sequestrated in non-
Cd in rice leaves might be due to co-precipitation of Si with heavy
photosynthetically active leaf epidermal cells could be a Mn tol-
metals in stem. Iwasaki et al. (2002) suggested co-precipitation of
erance mechanism in maize. Effect of Si on metal distribution
Si and Mn in leaf apoplast of cowpea plants. Oliva et al. (2011)
varies not only among plant species but also among genotypes. For
detected Cu in phytoliths of E. andevalensis shoots and suggested
example, Shi et al. (2010) reported that in leaves of peanut culti-
that Si may alleviate Cu stress in shoots by reducing free Cu. Zhang
vars, Si pretreatment significantly decreased Cd content in cell
et al. (2008) reported that in rice both Si and Cd accumulated
organelle fractions in Luhua 11, while remain unaffected in Luzi
synchronously in the border and middle of phytoliths of the
101 cultivar. By contrast, in Luzi 101, the reduction of Cd content by
shoots.
Si pretreatment was pronounced in cell wall fractions and re-
Previous studies also showed Si and metal complex formation
mained unaffected in Luhua 11. Li et al. (2009) reported that Si
in the roots. For example, da Cunha and do Nascimento (2009)
application in soil decreased the inorganic As concentration in
showed simultaneous presence of silica, Cd, and Zn deposits in
grain by 59% while increasing the concentration of dimethylarsinic
root mesophyll cells of maize plants and suggested Si-metal
acid (DMA) by 33% but the response varies between two rice
complexes in plants. Liu et al. (2013a) and Ma et al., (2015) re-
genotypes. More recently, scanning electron microscopy (SEM)
analysis showed that As was more concentrated in tomato shoots ported the co-deposition of Si and Cd in the root cell walls via a
external tissues, epidermis and parenchyma while Si was ubiqui- [Si-wall matrix]Cd complex formation might reduce the Cd uptake
tously distributed throughout the root and shoots in Si þAs by the plants suggesting in vivo detoxification of Cd in rice. Shi
treatments but localization varied from cultivar to cultivar (Mar- et al. (2005b) reported that in rice roots Si and Cd was mainly
miroli et al., 2014). deposited in endodermis and reduced the cell wall porosity of
Ye et al. (2012) reported that in Kandelia obovata plant Si en- inner root tissues and they hypothesized the co-precipitation of Si
hanced binding of Cd to the cell walls and restricted the apo- with cadmium. Cocker et al. (1998) and Wang et al. (2004) sug-
plasmic transport of Cd in root tips. Additionally, Zhang et al. gested that Si treatment under Al stress leads to the formation of
(2014) reported that in Avicennia marina plants Si increased Cd in HAS complexes in the apoplast of the root apex of maize and
the apoplasm and decreased in the symplasm of root tips but did wheat plants and suggested that the formation of HAS for Al de-
not affect the distribution in leaf apoplasm and symplasm. This toxification in plants. Similarly, Prabagar et al. (2011) reported that
showed that Si-mediated changes in the distribution of Cd in the the Si reduced the concentration of free Al in the root cell wall, and
root tips might also be an important mechanism for Si-induced Cd authors proposed the formation of aluminosilicate complexes in
tolerance. Luo et al. (2013) reported that Si application might the cell wall.
modify the Cd binding properties of S. nigrum root cell walls and The literature also showed that there might be no co-pre-
resultantly increased the relative proportion of ethanol-ex- cipitation of metals with Si in many plant species. For example, it
tractable, water-extractable and NaCl-extractable Cd in roots by was reported that in wheat plants Cu and Cd were not detected in
adding Si. Keller et al. (2015) studied the localization of Cu in leaf phytoliths (Rizwan et al., 2012; Keller et al., 2015) and sug-
wheat roots with and without Si application. In the presence of Si, gested that co-precipitation might not be a mechanism in Cu de-
root adsorbed Cu concentration increased especially with highest toxification in wheat plants. Similarly, Collin et al. (2014) reported
Cu (30 mM) concentration. In the absence of Si, Cu was mainly that microscopic findings did not confirm co-precipitation of Si
localized in the central cylinder of root while in the presence of Si, and Cu at the root level in bamboo plants grown in hydroponics.
Cu was mainly localized in the vicinity of root epidermis while Si Dresler et al. (2015) reported that no evidence of Si–Cd complexes
was localized mainly in the endodermis irrespective Cu treatment. was found in maize plants grown in hydroponics under Cd stress
In rice plant, Gu et al. (2012) reported that Zn and Si was co-lo- with increasing Si levels. From the above information it can be
calized in the cell wall of metabolically less active tissues, espe- concluded that co-precipitation of Si with heavy metals might not
cially in sclerenchyma of root and Si supply increased about 10% be a crucial mechanism for metal detoxification in plants. Thus,
the cell wall bound fraction of zinc. Thus, Si localization in the root further studies are still needed to clarify this mechanism in plants.
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197 193

6.5. Chelation 6.7. Structural alterations in plants

The mechanisms by which Si mitigates heavy metal stress in Furthermore, Si þCd supply increased length of leaves, leaf
plants might be related to the chelation of flavonoid-phenolics or area, root length of maize plant (Vaculik et al., 2009), and in-
organic acids with metals. It has been reported that phenol exu- creased the total root length, total root surface area of rice plants
dation increased in maize plants in Siþ Al treatments as compared as compared to Cd-only treated plants (Tripathi et al., 2012a,
to Al treatment alone and phenolics such as catechin and quer- 2012b). Si application increased the plant height, root length,
cetin have strong Al-chelating abilities which might be a factor number of leaves per plant and leaf area of cotton plants under Cd,
contributing to Si-enhanced Al resistance in root tip apoplast of Zn and Pb stress (Bharwana et al., 2013; Farooq et al., 2013; An-
maize (Kidd et al., 2001; Wang et al., 2004). Similarly, Barceló et al. waar et al., 2014). Keller et al. (2015) reported that Si increased
(1993) reported that addition of Si increased the malic acid con- root length of wheat seedlings under Cu stress. Si supply also in-
centration in maize plants under Al stress which can reduce the Al creased the total root length, total root surface area and total root
toxicity by chelating with malic acid. Furthormore, Collin et al. tip amount of rice plants under Zn stress (Song et al., 2011).
(2014) reported that Si was not directly involved in Cu speciation However, Si (5 mM) þZn (800 mM) application did not affect the
in bamboo roots but Si increased the proportion of Cu(I)S-ligands total root length, total root surface area, root volume and number
(organic and inorganic) in leaves and these ligands can chelate Cu of root tips in maize plants as compared to same Zn treatment
alone (Bokor et al., 2014b). Similarly, length of primary seminal
and can increase the Cu sequestration in a less toxic form. Fur-
root, leaf area of first and second leaves of maize significantly
thermore, Si addition increased citrate, malate and aconitate
decreased with Siþ Zn treatment as compared to the same Zn
concentration in roots of wheat seedlings treated with 30 mM Cu
treatment without Si supply (Bokor et al., 2014a). Similarly, Si
as compared to the same treatment without Si. Authors suggested
supply under Al stress decreased root diameter and increased root
that Cu could form complex with organic acids and reduced the Cu
surface area of peanut seedlings (Shen et al., 2014). Additionally, Si
translocation to shoots (Keller et al., 2015). These studies showed
under Al exposure increased the frequency of stomata and root
that Si-mediated release of chelates, those can complex metals,
hairs, length of root hairs and leaf epidermal cells, and maintained
might be a mechanism which could reduce the toxic effects of
the structure and integrity of mesophyll cells and phloem as
metal in plants up to certain level along with other mechanisms. compared to Al treatment alone (Singh et al., 2011). Similarly, Kim
However, more studies are still needed to highlight the role of Si- et al. (2014) reported that Si decreased the leaf damage and ne-
mediated chelation of metals in plants or in growth media. crosis under Cu stress in rice plants and also decreased metal toxic
effects on root architecture and increased the root length as
6.6. Modification of gene expression compared with plants treated metals only.
It has also been reported that Cdþ Si treatments accelerated
To clarify the roles of Si in mitigating heavy toxicity at genes suberin lamellae, Casparian bands and root vascular tissues de-
level, Kim et al. (2014) investigated that in rice plant Si application velopment. Si enhanced the tertiary endodermal cell walls for-
significantly activated OsHMA3 and OsLsi genes under Cu/Cd stress mation in comparison with Cd treatments alone which showed
as compared to metal treatments alone which might counteract enhanced endodermal apoplasmic barrier development in the
the negative impacts of the metal stress in plants. Similarly, Li et al. presence of Si in maize (Vaculik et al., 2009, 2012; Lukacova et al.,
(2008) showed that 1.5 mM Si application under Cu stress stimu- 2013). Silicon prompted the development of the apoplasmic bar-
lated the genes responsible for the production of metallothioneins rier in the roots of A. marina under Cd stress (Zhang et al., 2013a).
(MTs) in A. thaliana that can chelate toxic metals. COPT1 and HMA5 Vatehová et al. (2012) also reported the Si-mediated more ex-
transporter genes were induced by Cu and Si þCu supply reduced tensive development of suberin lamellae in endodermis closer to
these genes. In addition, Si may decrease the expression of PAL the root tips of rapeseed and Indian mustard under Cd stress. Si-
(phenylalanine ammonialyase) genes under Cu stress. However milarly, Greger et al. (2011) reported that in the presence of Si þCd
their role in decreasing Cu toxicity is not well understood (Khan- treatments, apoplasmic barriers in endodermis were formed closer
to the wheat root apex as compared to Cd-stressed wheat roots. Si
dekar and Leisner, 2011). More recently, Bokor et al. (2014b) re-
application significantly increased xylem diameter, mesophyll and
ported that in maize plants treated with Zn and also with Zn and Si
epidermis thickness, and decreased transversal area occupied by
showed downregulation of ZmLsi1 and ZmLsi2 genes in roots and
collenchyma in maize plants under Cd and Zn stress (da Cunha and
upregulated expression level of ZmLsi6 in the first leaf and de-
do Nascimento, 2009). Silicon together with Cd also reduced the
creased expression of ZmLsi6 in the second leaf. Nwugo and Huerta
abnormalities in leaf mesophyll cells and vascular bundles of rice
(2010) investigated the effect of Si on the leaf proteome of rice
as compared to Cd treatment alone (Tripathi et al., 2012a, 2012b).
plants under Cd stress and identified 60 protein spots that were
Also in cucumber plants, Si supply also inhibited the Mn toxicity
differentially regulated due to Cd and/or Si treatments. More re-
symptoms (Shi et al., 2005a). Similarly, Si substantially increased
cently, Ma et al. (2015) reported that in rice plants expression of the thickness of the leaf epidermal layers suggest that Mn storage
Lsi1 gene was up regulated in the presence of Si in the medium, in non-photosynthetic tissue could be a Mn tolerance mechanism
whereas expression of natural resistance-associated macrophage in maize (Doncheva et al., 2009). Júnior et al. (2010) reported that
protein 5 (Nramp5) gene, involved in the transport of Cd, was Si þMn supply to the rice plants decreased the leaf insertion angle
down-regulated. In addition, Song et al. (2014) reported that Si of the rice plant so improved its architecture.
application enhanced the expression of genes (Os08g02630 (PsbY), There are several evidences that Si ameliorated the ultra-
Os05g48630 (PsaH), Os07g37030 (PetC), Os03g57120 (PetH), structural disorders caused by chromium stress in many plant
Os09g26810 and Os04g38410) associated with photosynthesis in species (Ali et al., 2013). Chromium stress caused ultrastructural
rice under Zn toxicity. So far, mechanisms of Si-mediated allevia- disorders in leaves and roots of barley including increased amount
tion of heavy metal toxicity is poorly understood at the molecular of plastoglobuli, disintegrated and disappeared thylakoid mem-
and genetic levels, more genetic experiments are required to de- branes in leaves, and increased vacuolar size, disruption and dis-
termine linkage relationships between Si and metal stress to study appearance of nucleus in roots (Ali et al., 2013). Further, Tripathi
expression level of genes related to transport, deposition, and et al. (2015) reported that under Si þCr(VI) treatment, suberization
translocation of metals and Si in different plant species. 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- different environmental conditions to validate the Si-mediated
lings. Fu et al. (2012) studied the ameliorative effect of Si on rice alleviation of metal toxicity on large scale.
plants under Fe toxicity. Authors reported that exposed to Fe2 þ We reviewed that most experiments have utilized the Si under
toxicity, the root epidermal cells were severely injured. Cell wall hydroponic conditions and with a single metal toxicity under
was deformed, organelles of the cytoplasm were dissolved, and controlled conditions. This can result overestimation of metal
some cells died. Addition of Si along with Fe2 þ in the solution uptake and translocation. There is need to study the mechanisms
significantly ameliorated Fe2 þ toxicity to root cells. under naturally contaminated soils as the soil is a complex system
Silicon plays important roles in protecting photosynthetic ma- and these soils may have mixed contamination. Such studies will
chinery from damaging under metal stress. Silicon protected the help to use Si in farming practices because in the field many heavy
chloroplast ultrastructure from disorganization due to Cd, Cr and metals could be simultaneously present in the soil. For silicon and
Zn stress in cucumber, rice, barley and maize plants (Doncheva, metal toxicity, most of the experiments are conducted in soil un-
et al., 2009; Kaya et al., 2009; Feng et al., 2010; Ali et al., 2013; der short term, which poses an interrogation on long-term effect
Song et al., 2014). Added Si decreased the permeability of plasma of Si on these heavy metals. In fact, it could be expected that, due
membrane of leaf cells of barley and maize under excess Zn (Liang to aging processes, the ability of silicates to sequester heavy metals
et al., 1996; Kaya et al., 2009). decrease with time. More research will be needed to understand
In conclusion, Si application under metal stresses protected the the aging process in soil with application of silicates.
plant structures which might be due to compartmentation, co- Taken together, well-designed, large-scale and long-term field
precipitation and/or chelation of heavy metals in different plant trials are required to evaluate the feasibility of Si application for
parts and as a result free metal ion concentration decreased and the remediation of metal contaminated soils and economic feasi-
plant growth and biomass increased. However, the relevant mor- bility of different Si sources should also be investigated.
phological and ultrastructural mechanisms still remained to be
investigated.
Acknowledgments
6.8. Other
Financial support from Government College University Faisa-
Silicon application increased the xylem sap in rice and banana labad and HEC (Higher Education Commission) of Pakistan (IPFP/
plants under Cd, Zn and Pb stress and decreased the Cd, Zn and Pb HRD/HEC/2014/1035)is gratefully acknowledged.
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 References
by xylem flow. Recently, Feng et al. (2010) reported that Si supply
decreased the inhibiting effects of Cd on the enzymes of nitrogen Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., Farid, M., Zia-ur-Rehman, M.,
metabolism including nitrogen reductase (NR), glutamine syn- Irshad, M.K., Bharwana, S.A., 2015. The effect of excess copper on growth and
thetase (GS), glutamate synthase (GOGAT) and glutamate dehy- physiology of important food crops: a review. Environ. Sci. Pollut. Res. . http:
//dx.doi.org/10.1007/s11356-015-4496-5 (in press)
drogenase (GDH) in cucumber plants. Dragišić Maksimović et al. Afshan, S., Ali, S., Bharwana, Saima Aslam, Rizwan, S.A., Farid, M., Abbas, M., Ibra-
(2007) suggested that Si nutrition modulates the metabolism and him, F., Mehmood, M., Abbasi, G.H., M.A., 2015. Citric acid enhances the phy-
utilization of phenols mainly at the leaf level by stimulating the toextraction of chromium, plant growth 2 and photosynthesis by alleviating the
oxidative damages in Brassica napus L. Environ. Sci. Pollut. Res. . http://dx.doi.
formation of Si polyphenol complexes in cucumber plants.
org/10.1007/s11356-015-4396-8
Alexandre, A., Meunier, J.D., Lezine, A.M., Vincens, A., Schwartz, D., 1997. Phytoliths:
indicators of grassland dynamics during the late Holocene in intertropical
7. Conclusions and perspectives Africa. Palaeogeogr. Palaeoclimatol. Palaeoecol. 136, 213–229.
Ali, S., Bharwana, S.A., Rizwan, M., Farid, M., Kanwal, S., Ali, Q., Ibrahim, M., Gill, R.A.,
Khan, M.D., 2015a. Fulvic acid mediates chromium (Cr) tolerance in wheat
Heavy metal toxicity causes huge losses in agriculture pro- (Triticum aestivum L.) through lowering of Cr uptake and improved antioxidant
ductivity worldwide. It is widely accepted that Si can alleviate var- defense system. Environ. Sci. Pollut. Res. . http://dx.doi.org/10.1007/s11356-
015-4271-7
ious biotic and abiotic including heavy metal stress in plants. Silicon Ali, S., Chaudhary, A., Rizwan, M., Anwar, H.T., Adrees, M., Farid, M., Irshad, M.K.,
could reduce heavy metals uptake in various plants species and en- Hayat, T., Anjum, S.A., 2015b. Alleviation of chromium toxicity by glycinebe-
hanced the plant growth and biomass. The key mechanisms evoked taine is related to elevated antioxidant enzymes and suppressed chromium
uptake and oxidative stress in wheat (Triticum aestivum L.). Environ. Sci. Pollut.
include reducing active heavy metal ions in growth media, chelation
Res. . http://dx.doi.org/10.1007/s11356-015-4193-4
and stimulation of antioxidant systems in plants, complexation and Ali, S., Farooq, M.A., Yasmeen, T., Hussain, S., Arif, M.S., Abbas, F., Bharwana, S.A.,
co-precipitation of toxic metals with Si, compartmentation and Zhang, G.P., 2013. The influence of silicon on barley growth, photosynthesis and
ultra-structure under chromium stress. Ecotoxicol. Environ. Saf. 89, 66–72.
structural alterations in plants and regulation of the expression of
Anwaar, S.A., Ali, S., Ali, S., Ishaque, W., Farid, M., Farooq, M.A., Najeeb, U., Abbas, F.,
metal transport genes. However, these mechanisms might be asso- Sharif, M., 2014. Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc
ciated with plant species, genotypes, metal elements, growth con- (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ. Sci.
ditions, duration of the stress imposed and so on. Therefore, the Pollut. Res. . http://dx.doi.org/10.1007/s11356-014-3938-9
Barceló, J., Guevara, P., Poschenrieder, C., 1993. Silicon amelioration of aluminium
generalization of Si-mediated alleviation of metal toxicity should be toxicity in teosinte (Zea mays L. sp. mexicana). Plant Soil 154, 249–255.
therefore made with caution. This review could contribute to better Bélanger, R.R., Benhamou, N., Menzies, J.G., 2003. Cytological evidence of an active
understanding of the mechanisms of Si-mediated enhanced metal role of silicon in wheat resistance to powdery mildew (Blumeria graminis f. sp
tritici). Phytopathology 93, 402–412.
tolerance of plants as well as in increasing productivity of crops Bharwana, S.A., Ali, S., Farooq, M.A., Iqbal, N., Abbas, F., Ahmad, M.S.A., 2013. Alle-
under stress conditions. However, more work needs to be done to viation of lead toxicity by silicon is related to elevated photosynthesis, anti-
explore fully the mechanisms involved. oxidant enzymes suppressed lead uptake and oxidative stress in cotton. J.
Bioremediat. Biodegrad. 4, 1–11.
We anticipated that there would be a growing interest to study
Blecker, S.W., McCulley, R.L., Chadwick, O.A., Kelly, E.F., 2006. Biologic cycling of
the mechanisms of Si-mediated heavy metal tolerance in plants in silica across a grassland bioclimosequence. Glob. Biogeochem. Cycles 20 10.
near future, so we identify the next areas as the ones warranting 1029/2006GB002690.
research. Current knowledge of Si functions under metal toxicity is Bokor, B., Bokorová, S., Ondoš, S., Švubová, R., Lukačová, Z., Hýblová, M., Szemes, T.,
Lux, A., 2014a. Ionome and expression level of Si transporter genes (Lsi1, Lsi2,
developing especially in individual plant species. However, there is and Lsi6) affected by Zn and Si interaction in maize. Environ. Sci. Pollut. Res. .
still need to better understand its function in more species under http://dx.doi.org/10.1007/s11356-014-3876-6
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197 195

Bokor, B., Vaculik, M., Slováková, L., Masarovič, D., Lux, A., 2014b. Silicon does not Gill, R.A., Zang, L., Ali, B., Farooq, M.A., Cui, P., Yang, S., Ali, S., Zhou, W., 2015.
always mitigate zinc toxicity in maize. Acta Physiol. Plant. 36, 733–743. Chromium-induced physio-chemical and ultrastructural changes in four culti-
Casey, W.H., Kinrade, S.D., Knight, C.T.G., Rains, D.W., Epstein, E., 2003. Aqueous vars of Brassica napus L. Chemosphere 120, 154–164.
silicate complexes in wheat, Triticum aestivum L. Plant Cell Environ. 27, 51–54. Greger, M., Landberg, T., Lux, A., Singh, B.R., 2011. Influence of Si on Cd uptake and
CEC (Commission of the European Communities), 2002. COM(2002) 179: Com- accumulation in wheat. In: Proceedings of the 5th International Conference on
munication from the commission to the council, the European Parliament, the Silicon in Agriculture, Beijing, China, September 13–18.
Economic and Social Committee and the Committee of the Regions – Towards a Gu, H.H., Qiu, H., Tian, T., Zhan, S.S., Deng, T.H.B., Chaney, R.L., Wang, S.Z., Tang, Y.T.,
thematic strategy for soil protection. Final, 35p. Morel, J.L., Qiu, R.L., 2011. Mitigation effects of silicon rich amendments on
Chalmardi, Z.K., Abdolzadeh, A., Sadeghipour, H.R., 2014. Silicon nutrition potenti- heavy metal accumulation in rice (Oryza sativa L.) planted on multi-metal
ates the antioxidant metabolism of rice plants under iron toxicity. Acta Physiol. contaminated acidic soil. Chemosphere 83, 1234–1240.
Plant. 36, 493–502. Gu, H.H., Zhan, S., Wang, S.Z., Tang, Y.T., Chaney, R.L., Fang, X.H., Cai, X.D., Qiu, R.L.,
Chen, H.M., Zheng, C.R., Tu, C., She, Z.G., 2000. Chemical methods and phytor- 2012. Silicon-mediated amelioration of zinc toxicity in rice (Oryza sativa L.)
emediation of soil contaminated with heavy metals. Chemosphere 41, 229–234. seedlings. Plant Soil 350, 193–204.
Chiba, Y., Mitani, N., Yamaji, N., Ma, J.F., 2009. HvLsi1 is a silicon influx transporter Gunes, A., Inal, A., Bagci, E.G., Coban, S., Sahin, O., 2007a. Silicon increases boron
in barley. Plant J. 57, 810–818. tolerance and reduces oxidative damage of wheat grown in soil with excess
Cocker, K.M., Evans, D.E., Hodson, M.J., 1998. The amelioration of aluminium toxi- boron. Biol. Plant. 51, 571–574.
city by silicon in higher plants: solution chemistry or an in planta mechanism. Gunes, A., Inal, A., Bagci, E.G., Pilbeam, D.J., 2007b. Silicon-mediated changes of
Physiol. Plant. 104, 608–614. some physiological and enzymatic parameters symptomatic for oxidative stress
Collin, B., Doelsch, E., Keller, C., Cazevieille, P., Tella, M., Chaurand, P., Panfili, F., in spinach and tomato grown in sodic-B toxic soil. Plant Soil 290, 103–114.
Hazemann, J.L., Meunier, J.D., 2014. Copper distribution and speciation in Guntzer, F., Keller, C., Meunier, J.D., 2012. Benefits of plant silicon for crops: a re-
bamboo exposed to a high Cu concentration and Si supplementation. First view. Agron. Sustain. Dev. 32, 201–213.
evidence on the presence of reduced copper bound to sulfur compounds in Guo, W., Hou, Y.L., Wang, S.G., Zhu, Y.G., 2005. Effect of silicate on the growth and
Poaceae. Environ. Pollut. 187, 22–30. arsenate uptake by rice (Oryza sativa L.) seedlings in solution culture. Plant Soil
Collin, B., Doelsch, E., Keller, C., Panfili, F., Meunier, J.D., 2013. Effects of silicon and 272, 173–181.
copper on bamboo grown hydroponically. Environ. Sci. Pollut. Res. 20, Guo, W., Zhang, J., Teng, M., Wang, L.H., 2009. Arsenic uptake is suppressed in a rice
6482–6495. mutant defective in silicon uptake. J. Plant Nutr. Soil Sci. 172, 867–874.
Cornelis, J.T., Titeux, H., Ranger, J., Delvaux, B., 2011. Identification and distribution Guo, W., Zhu, Y.G., Liang, Y.C., Liu, W.J., Chen, Z., 2006. Effect of application of silicon
of the readily soluble silicon pool in a temperate forest soil below three distinct on arsenic uptake by rice seedlings in soil. Environ. Sci. 27, 1393–1397.
tree species. Plant Soil 342, 369–378. Guo, W., Zhu, Y.G., Liu, W.J., Liang, Y.C., Geng, C.N., Wang, S.G., 2007. Is the effect of
Corrales, I., Poschenrieder, C., Barceló, J., 1997. Influence of silicon pretreatment on silicon on rice uptake of arsenate (AsV) related to internal silicon concentra-
aluminium toxicity in maize roots. Plant Soil 190, 203–209. tions, iron plaque and phosphate nutrition? Environ. Pollut. 148, 251–257.
Côté -Beaulieu, C., Chain, F., Menzies, J.G., Kinrade, S.D., Bélanger, R.R., 2009. Ab- Habiba, U., Ali, S., Farid, M., Shakoor, M.B., Rizwan, M., Ibrahim, M., Abbasi, G.H.,
sorption of aqueous inorganic and organic silicon compounds by wheat and Hayat, T., Ali, B., 2015. EDTA enhanced plant growth, antioxidant defense sys-
their effect on growth and powdery mildew control. Environ. Exp. Bot. 65, tem, and phytoextraction of copper by Brassica napus L. Environ. Sci. Pollut. Res.
155–161. 22, 1534–1544.
da Cunha, K.P.V., do Nascimento, C.W.A., 2009. Silicon effects on metal tolerance Hammond, K.E., Evans, D.E., Hodson, M.,J., 1995. Aluminium/silicon interactions in
and structural changes in maize (Zea mays L.) grown on a cadmium and zinc barley (Hordeum vulgare L.) seedlings. Plant Soil 173, 89–95.
enriched soil. Water Air Soil Pollut. 197, 323–330. Hara, T., Gu, M.H., Koyama, H., 1999. Ameliorative effect of silicon on aluminum
da Cunha, K.P.V., do Nascimento, C.W.A., Silva, A.J., 2008. Silicon alleviates the injury in the rice plant. Soil Sci. Plant Nutr. 45, 929–936.
toxicity of cadmium and zinc for maize (Zea mays L.) grown on contaminated Hodson, M.J., Evans, D.E., 1995. Aluminium/silicon interactions in higher plants. J.
soil. J. Plant Nutr. Soil Sci. 171, 849–853. Exp. Bot. 46, 161–171.
Desplanques, V., Cary, L., Mouret, J.C., Trolard, F., Bourrié, G., Grauby, O., Meunier, J. Hodson, M.J., Sangster, A.G., 1990. Techniques for the microanalysis of higher
D., 2006. Silicon transfers in a rice field in Camargue (France). J. Geochem. plants, with particular reference to silicon in cryofixed wheat tissues. Scanning
Explor. 88, 190–193. Microsc. 4, 407–418.
Ding, T.P., Ma, G.R., Shui, M.X., Wan, D.F., Li, R.H., 2005. Silicon isotope study on rice Hodson, M.J., White, P.J., Mead, A., Broadley, M.R., 2005. Phylogenetic variation in
plants from the Zhejiang province, China. Chem. Geol. 218, 41–50. the silicon composition of plants. Ann. Bot. 96, 1027–1046.
Ding, T.P., Zhou, J.X., Wan, D.F., Chen, Z.Y., Zhang, F., 2008. Silicon isoope fractio- Hu, H., Zhang, J., Wang, H., Li, R., Pan, F., Wu, J., Liu, Q., 2013. Effect of silicate
nation in bamboo and its significance to the biogeochemical cycle of cilicon. supplementation on the alleviation of arsenite toxicity in 93-11 (Oryza sativa L.
Geochim. Cosmochim. Acta 72, 1381–1395. indica). Environ. Sci. Pollut. Res. 20, 8579–8589.
do Nascimento, C.W.A., Xing, B., 2006. Phytoextraction: a review on enhanced Hussain, I., Ashraf, M.A., Rasheed, R., Asghar, A., Sajid, M.A., Iqbal, M., 2015. Exo-
metal availability and plant accumulation. Sci. Agric. 3, 299–311. genous application of silicon at the boot stage decreases accumulation of
Doncheva, S.N., Poschenrieder, C., Stoyanova, Z.I., Georgieva, K., Velichkova, M., cadmium in wheat (Triticum aestivum L.) grains. Braz. J. Bot. . http://dx.doi.org/
Barcelo, J., 2009. Silicon amelioration of manganese toxicity in Mn-sensitive 10.1007/s40415-014-0126-6
and Mn-tolerant maize varieties. Environ. Exp. Bot. 65, 169–197. Iwasaki, K., Maier, P., Fecht, M., Horst, W.J., 2002. Leaf apoplastic silicon enhances
Dragišić Maksimović, J., Bogdanović, J., Maksimović, V., Nikolic, M., 2007. Silicon manganese tolerance of cowpea (Vigna unguiculata). J. Plant Physiol. 159, 167–173.
modulates the metabolism and utilization of phenolic compounds in cucumber Júnior, L.A.Z., Fontes, R.L.F., Neves, J.C.L., Korndörfer, G.H., Ávila, V.T.D., 2010. Rice
(Cucumis sativus L.) grown at excess manganese. J. Plant Nutr. Soil Sci. 170, grown in nutrient solution with doses of manganese and silicon. Rev. Bras.
739–744. Ciênc. Solo 34, 1629–1639.
Dresler, S., Wójcik, M., Bednarek, W., Hanaka, A., Tukiendorf, A., 2015. The effect of Kabata-Pendias, A., Pendias, H., 2001. Trace Elements in Soils and Plants, 3rd ed.
silicon on maize growth under cadmium stress. Russ. J. Plant Physiol. 62, 86–92. CRC Press, Boca Raton, FL.
Ehsan, S., Ali, S., Noureen, S., Mehmood, K., Farid, M., Ishaque, W., Shakoor, M.B., Kaya, C., Tuna, A.L., Sonmez, O., Ince, F., Higgs, D., 2009. Mitigation effects of silicon
Rizwan, M., 2014. Citric acid assisted phytoremediation of Cd by Brassica napus on maize plants grown at high zinc. J. Plant Nutr. 32, 1788–1798.
L. Ecotoxicol. Environ. Saf. 106, 164–172. Keller, C., Rizwan, M., Davidian, J.C., Pokrovsky, O.S., Bovet, N., Chaurand, P., Meu-
Emadian, S.F., Newton, R.J., 1989. Growth enhancement of loblolly pine (Pinus taeda nier, J.D., 2015. Effect of silicon on wheat seedlings (Triticum turgidum L.) grown
L.) seedlings by silicon. J. Plant Physiol. 134, 98–103. in hydroponics and exposed to 0 to 30 mM Cu. Planta 241, 847–860.
Epstein, E., 1994. The anomaly of silicon in plant biology. Proc. Natl. Acad. Sci. USA Khandekar, S., Leisner, S., 2011. Soluble silicon modulates expression of Arabidopsis
91, 11–17. thaliana genes involved in copper stress. J. Plant Physiol. 168, 699–705.
Epstein, E., 1999. Silicon. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50, 641–664. Khodarahmi, S., Khoshgoftarmanesh, A.H., Mobli, M., 2012. Effect of silicon nutri-
Epstein, E., 2009. Silicon: its manifold roles in plants. Ann. Appl. Biol. 155, 155–160. tion on alleviating cadmium toxicity-induced damage on cucumber (Cucumis
Farooq, M.A., Ali, S., Hameed, A., Ishaque, W., Mahmood, K., Iqbal, Z., 2013. Alle- sativus L.) at vegetative stage. J. Sci. Technol. 3, 103–110.
viation of cadmium toxicity by silicon is related to elevated photosynthesis, Kidd, P.S., Llugany, M., Poschenrieder, C., Gunsé, B., Barceló, J., 2001. The role of root
antioxidant enzymes; suppressed cadmium uptake and oxidative stress in exudates in aluminum resistance and silicon-induced amelioration of alumi-
cotton. Ecotoxicol. Environ. Saf. 96, 242–249. num toxicity in three varieties of maize (Zea mays L.). J. Exp. Bot. 52, 1339–1353.
Fauteux, F., Remus-Borel, W., Menzies, J.G., Belanger, R.R., 2005. Silicon and plant Kim, Y.H., Khan, A.L., Kim, D.H., Lee, S.Y., Kim, K.M., Waqas, M., Lee, I.J., 2014. Silicon
disease resistance against pathogenic fungi: mini review. FEMS Microbiol. Lett. mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza
249, 1–6. sativa low silicon genes, and endogenous phytohormones. BMC Plant Boil. 14,
Feng, J., Shi, Q., Wang, X., Wei, M., Yang, F., Xu, H., 2010. Silicon supplementation 13 〈http://www.biomedcentral.com/1471-2229/14/13〉.
ameliorated the inhibition of photosynthesis and nitrate metabolism by cad- Kovda, V.A., 1973. The Bases of Learning About Soils. vol. 2. Nayka, Moscow.
mium (Cd) toxicity in Cucumis sativus L. Sci. Hortic. 123, 521–530. Li, J., Leisner, M., Frantz, J., 2008. Alleviation of copper toxicity in Arabidopsis thaliana
Fleck, A.T., Mattusch, J., Schenk, M.K., 2013. Silicon decreases the arsenic level in by silicon addition to hydroponic solutions. J. Am. Soc. Hortic. Sci. 133, 670–677.
rice grain by limiting arsenite transport. J. Plant Nutr. Soil Sci. 176, 785–794. Li, L., Zheng, C., Fu, Y., Wu, D., Yang, X., Shen, H., 2012. Silicate-mediated alleviation
Frantz, J.M., Khandekar, S., Leisner, S., 2011. Silicon differentially influences copper of Pb toxicity in banana grown in Pb-contaminated soil. Biol. Trace Elem. Res.
toxicity response in silicon-accumulator and non-accumulator species. J. Am. 145, 101–108.
Soc. Hortic. Sci. 136, 329–338. Li, P., Song, A., Li, Z., Fan, F., Liang, Y., 2013. Silicon ameliorates manganese toxicity
Fu, Y.Q., Shen, H., Wu, D.M., Cai, K.Z., 2012. Silicon-mediated amelioration of Fe2 þ by regulating manganese transport and antioxidant reactions in rice (Oryza
toxicity in rice (Oryza sativa L.) roots. Pedosphere 22, 795–802. sativa L.). Plant Soil. 354, 407–419.
196 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197

Li, P., Wang, X., Zhang, T., Zhou, D., He, Y., 2008. Effects of several amendments on wheat grains by silicon is related to its application rate and cadmium accu-
rice growth and uptake of copper and cadmium from a contaminated soil. J. mulating abilities of cultivars. J. Sci. Food Agric. . http://dx.doi.org/10.1002/
Environ. Sci. 20, 449–455. jsfa.6976
Li, R.Y., Stroud, J.L., Ma, J.F., McGrath, S.P., Zhao, F.J., 2009. Mitigation of arsenic Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and
accumulation in rice with water management and silicon fertilization. Environ. toxicity for plants: a review. Environ. Chem. Lett. 8, 199–216.
Sci. Technol. 43, 3778–3783. Neumann, D., zur Nieden, U., Schwieger, W., Leopold, I., Lichtenberger, O., 1997.
Li, Z., Song, Z., Cornelis, J.T., 2014. Impact of rice cultivar and organ on elemental Heavy metal tolerance of Minuartia verna. J. Plant Physiol. 151, 101–108.
composition of phytoliths and the release of bio-available silicon. Front Plant Neumann, D.E., Zur Nieden, U., 2001. Silicon and heavy metal tolerance of higher
Sci. 5. http://dx.doi.org/10.3389/fpls.2014.00529. plant. Phytochemistry 56, 685–692.
Liang, Y., Sun, W., Zhu, Y.G., Christie, P., 2007. Mechanisms of siliconmediated al- Noman, A., Ali, S., Naheed, F., Ali, Q., Farid, M., Rizwan, M., Irshad, M.K., 2015. Foliar
leviation of abiotic stresses in higher plants: a review. Environ. Pollut. 147, application of ascorbate enhances the physiological and biochemical attributes
422–428. of maize (Zea mays L.) cultivars under drought stress. Arch. Agron. Soil Sci. .
Liang, Y.C., Shen, Q.R., Shen, Z.G., Ma, T.S., 1996. Effects of silicon on salinity toler- http://dx.doi.org/10.1080/03650340.2015.1028379
ance of two barley cultivars. J. Plant Nutr. 19, 173–183. Nowakowski, W., Nowakowska, J., 1997. Silicon and copper interaction in the
Liang, Y.C., Wong, J.W.C., Long, W., 2005. Silicon-mediated enhancement of cad- growth of spring wheat seedlings. Biol. Plant. 39, 463–466.
mium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Nwugo, C.C., Huerta, A.J., 2008. Effects of silicon nutrition on cadmium uptake:
Chemosphere 58, 475–483. growth and photosynthesis of rice plants exposed to lowlevel cadmium. Plant
Liu, C., Li, F., Luo, C., Liu, X., Wang, S., Liu, T., Li, X., 2009. Foliar application of two Soil 311, 73–86.
silica sols reduced cadmium accumulation in rice grains. J. Hazard. Mater. 161, Nwugo, C.C., Huerta, A.J., 2010. The effect of silicon on the leaf proteome of rice
1466–1472. (Oryza sativa L.) plants under cadmium-stress. J. Proteom. Res. 10, 518–528.
Liu, J., Ma, J., He, C., Li, X., Zhang, W., Xu, F., Wang, L., 2013a. Inhibition of cadmium Oliva, S.R., Mingorance, M.D., Leidi, E.O., 2011. Effects of silicon on copper toxicity in
ion uptake in rice (Oryza sativa) cells by a wall‐bound form of silicon. New Erica andevalensis Cabezudo and Rivera: a potential species to remediate
Phytol. 200, 691–699. contaminated soils. J. Environ. Monit. 13, 591–596.
Liu, J., Zhang, H., Zhang, Y., Chai, T., 2013b. Silicon attenuates cadmium toxicity in Prabagar, S., Hodson, M.J., Evans, D.E., 2011. Silicon amelioration of aluminium
Solanum nigrum L. by reducing cadmium uptake and oxidative stress. Plant toxicity and cell death in suspension cultures of Norway spruce (Picea abies (L.)
Physiol. Biochem. 68, 1–7. Karst.). Environ. Exp. Bot. 70, 266–276.
Lu, H.P., Zhuang, P., Li, Z.A., Tai, Y.P., Zou, B., Li, Y.W., McBride, M.B., 2014. Contrasting Putwattana, N., Kruatrachue, M., Pokethitiyook, P., Chaiyarat, R., 2010. Im-
effects of silicates on cadmium uptake by three dicotyledonous crops grown in mobilization of cadmium in soil by cow manure and silicate fertilizer, and re-
contaminated soil. Environ. Sci. Pollut. Res., 1–10. duced accumulation of cadmium in sweet basil (Ocimum basilicum). Sci. Asia
Lukacova Kulikova, Z., Lux, A., 2010. Silicon influence on maize, Zea mays L., hybrids 36, 349–354.
exposed to cadmium treatment. Bull. Environ. Contam. Toxicol. 85, 243–250. Rad, S.J., Rad, M.S., Teixeira da Silva, J.A., 2014. Effects of exogenous silicon on
Lukacova, Z., Svubova, R., Kohanova, J., Lux, A., 2013. Silicon mitigates the Cd cadmium accumulation and biological responses of Nigella sativa L. (black cu-
toxicity in maize in relation to cadmium translocation, cell distribution, anti- min). Commun. Soil Sci. Plant Anal. 45, 1918–1933.
oxidant enzymes stimulation and enhanced endodermal apoplasmic barrier Rains, D.W., Epstein, E., Zasoski, R.J., Aslam, M., 2006. Active silicon uptake by
development. Plant Growth Regul. 70, 89–103. wheat. Plant Soil 280, 223–228.
Lux, A., Luxová, M., Abe, J., Tanimoto, E., Hattoriand, T., Inanaga, S., 2003. The dy- Raven, J.A., 1983. The transport and function of silicon in plants. Biol. Rev. Camb.
namics of silicon deposition in the sorghum root endodermis. New Phytol. 158, Philos. Soc. 58, 179–207.
437–441. Rizwan, M., Meunier, J.D., Miche, H., Keller, C., 2012. Effect of silicon on reducing
Ma, J., Cai, H., He, C., Zhang, W., Wang, L., 2015. A hemicellulose‐bound form of cadmium toxicity in durum wheat (Triticum turgidum L. cv. Claudio W.) grown
silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol. . in a soil with aged contamination. J. Hazard. Mater. 209–210, 326–334.
http://dx.doi.org/10.1111/nph.13276 Rogalla, H., Romheld, V., 2002. Role of leaf apoplast in silicon-mediated manganese
Ma, J.F., Mitani, N., Nagao, S., Konishi, S., Tamai, K., Iwashita, T., Yano, M., 2004. tolerance of Cucumic sativus L. Plant Cell Environ. 25, 549–555.
Characterization of the silicon uptake system and molecular mapping of the Sanglard, L.M.V.P., Martins, S.,C.V., Detmann, K.C., Silva, P.E.M., Lavinsky, A.O., Silva,
silicon transporter gene in rice. Plant Physiol. 136, 3284–3289. M.M., Detmann, E., Araújo, W.L., DaMatta, F.M., 2014. Silicon nutrition alleviates
Ma, J.F., Miyake, Y., Takahashi, E., 2001. Silicon as a beneficial element for crop the negative impacts of arsenic on the photosynthetic apparatus of rice leaves:
plants. In: Datnoff, L.E., Snyder, G.H., Korndorfer, G.H. (Eds.), Silicon in Agri- an analysis of the key limitations of photosynthesis. Physiol. Plant . http://dx.
culture. Elsevier Science Publishing, Amsterdam, pp. 17–39. doi.org/10.1111/ppl.12178.
Ma, J.F., Sasaki, M., Matsumoto, H., 1997. Al-induced inhibition of root elongation in Sauer, D., Saccone, L., Conley, D.J., Herrmann, L., Sommer, M., 2006. Review of
corn, Zea mays L., is overcome by Si addition. Plant Soil 188, 171–176. methodologies for extracting plant-available and amorphous Si from soils and
Ma, J.F., Takahashi, E., 2002. Soil, Fertiliser, and Plant Silicon Research in Japan. aquatic sediments. Biogeochemistry 80, 89–108.
Elsevier. Savant, N.K., Snyder, G.H., Datnoff, L.E., 1997. Silicon management and sustainable
Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., Ishiguro, M., rice production. Adv. Agron. 58, 151–199.
Murata, Y., Yano, M., 2006. A silicon transporter in rice. Nature 440, 688–691. Sharma, S.S., Dietz, K.J., 2009. The relationship between metal toxicity and cellular
Ma, J.F., Yamaji, N., 2006. Silicon uptake and accumulation in higher plants. Trends redox imbalance. Trends Plant Sci. 14, 43–50.
Plant Sci. 11, 392–397. Shen, X., Xiao, X., Dong, Z., Chen, Y., 2014. Silicon effects on antioxidative enzymes
Ma, J.F., Yamaji, N., 2008. Functions and transport of silicon in plants. Cell Mol. Life and lipid peroxidation in leaves and roots of peanut under aluminum stress.
Sci. 65, 3049–3057. Acta Physiol. Plant. 36, 3063–3069.
Ma, J.F., Yamaji, N., Mitani, N., Tamai, K., Konishi, S., Fujiwara, T., Katsuhara, M., Yano, Shi, G.R., Cai, Q.S., Liu, C.F., Wu, L., 2010. Silicon alleviates cadmium toxicity in
M., 2007. An efflux transporter of silicon in rice. Nature 448, 209–212. peanut plants in relation to cadmium distribution and stimulation of anti-
Ma, J.F., Yamaji, N., Mitani-Ueno, N., 2011. Transport of silicon from roots to panicles oxidative enzymes. Plant Growth Regul. 61, 45–52.
in plants. Proc. Jpn. Acad. Ser. B: Phys. Biol. Sci. 87, 377. Shi, Q., Bao, Z., Zhu, Z., He, Y., Qian, Q., Yu, J., 2005a. Silicon-mediated alleviation of
Maksimović, J.D., Mojović, M., Maksimović, V., Römheld, V., Nikolic, M., 2012. Silicon Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase
ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical and ascorbate peroxidase. Phytochemistry 66, 1551–1559.
accumulation in the leaf apoplast. J. Exp. Bot. 63, 2411–2420. Shi, X., Zhang, C., Wang, H., Zhang, F., 2005b. Effect of Si on the distribution of Cd in
Malčovská, S.M., Dučaiová, Z., Maslaňáková, I., Bačkor, M., 2014. Effect of silicon on rice seedlings. Plant Soil 272, 53–60.
growth, photosynthesis, oxidative status and phenolic compounds of maize Shim, J., Shea, P.J., Oh, B.T., 2014. Stabilization of heavy metals in mining site soil
(Zea mays L.) grown in cadmium excess. Water Air Soil Pollut. 225, 1–11. with silica extracted from corn cob. Water Air Soil Pollut. 225, 1–12.
Marmiroli, M., Pigoni, V., Savo-Sardaro, M.L., Marmiroli, N., 2014. The effect of si- Singh, V.P., Tripathi, D.K., Kumar, D., Chauhan, D.K., 2011. Influence of exogenous
licon on the uptake and translocation of arsenic in tomato (Solanum lyco- silicon addition on aluminium tolerance in rice seedlings. Biol. Trace Elem. Res.
persicum L.). Environ. Exp. Bot. 99, 9–17. 144, 1260–1274.
Masarovic, D., Slovakova, L., Bokor, B., Bujdos, M., Lux, A., 2012. Effect of silicon Sommer, M., Kaczorek, D., Kuzyakov, Y., Breuer, J., 2006. Silicon pools and fluxes in
application on Sorghum bicolor exposed to toxic concentration of zinc. Biologia soils and landscapes: a review. J. Plant Nutr. Soil Sci. 169, 310–329.
67, 706–712. Song, A., Li, P., Fan, F., Li, Z., Liang, Y., 2014. The effect of silicon on photosynthesis
Mehrabanjoubani, P., Abdolzadeh, A., Sadeghipour, H.R., Aghdasi, M., 2014. Impacts and expression of its relevant genes in rice (Oryza sativa L.) under high-zinc
of silicon nutrition on growth and nutrient status of rice plants grown under stress. PLoS One 9 (11). http://dx.doi.org/10.1371/journal.pone.0113782.
varying zinc regimes. Theor. Exp. Plant Physiol. . http://dx.doi.org/10.1007/ Song, A., Li, P., Li, P., Fan, F., Nikolic, M., Liang, Y., 2011. The alleviation of zinc toxicity
s40626-014-0028-9 by silicon is related to zinc transport and antioxidative reaction in rice. Plant
Meunier, J.D., Colin, F., Alarcon, C., 1999. Biogenic silica storage in soils. Geology 27, Soil 344, 319–333.
835–838. Song, A.L., Li, Z.J., Zhang, J., Xue, G.F., Fan, F.L., Liang, Y.C., 2009. Silicon-enhanced
Mitani, N., Ma, J.F., 2005. Uptake system of silicon in different plant species. J. Exp. resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si sup-
Bot. 56, 1255–1261. pressed cadmium uptake and transport and Si-enhanced antioxidant defense
Mitani, N., Yamaji, N., Ma, J.F., 2009. Identification of maize silicon influx trans- capacity. J. Hazard. Mater. 172, 74–83.
porters. Plant Cell Physiol. 50, 5–12. Srivastava, R.K., Pandey, P., Rajpoot, R., Rani, A., Gautam, A., Dubey, R.S., 2014.
Morikawa, C.K., Saigusa, M., 2002. Si amelioration of Al toxicity in barley (Hordeum Exogenous application of calcium and silica alleviates cadmium toxicity. by
vulgare L.) growing in two Andosols. Plant Soil 240, 161–168. suppressing oxidative damage in rice seedlings. http://dx.doi.org/10.1007/
Naeem, A., Ghafoor, A., Farooq, M., 2014. Suppression of cadmium concentration in s00709-014-0731-z.
 M. Adrees et al. / Ecotoxicology and Environmental Safety 119 (2015) 186–197 197

Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G., 2011. ROS and redox signalling in Williams, E.D., Vlamis, J., 1957. The effect of silicon on yield and manganese-54
the response of plants to abiotic stress. Plant Cell Environ. 35, 259–270. uptake and distribution in the leaves of barley plants grown in culture solu-
Takahashi, E., Ma, J.F., Miyake, Y., 1990. The possibility of silicon as an essential tions. Plant Physiol. 32, 404–409.
element for higher plants. Comm. Agric. Food Chem. 2, 99–122. Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: a review of
Tang, H., Liu, Y., Gong, X., Zeng, G., Zheng, B., Wang, D., Sun, Z., Zhou, L., Zeng, X., sources, chemistry, risks and best available strategies for remediation. ISRN
2015. Effects of selenium and silicon on enhancing antioxidative capacity in Ecol. . http://dx.doi.org/10.5402/2011/402647
ramie (Boehmeria nivea (L.) Gaud.) under cadmium stress. Environ. Sci. Pollut. Yamaji, N., Chiba, Y., Mitani-Ueno, N., Ma, J.F., 2012. Functional characterization of a
Res. . http://dx.doi.org/10.1007/s11356-015-4187-2 silicon transporter gene implicated in silicon distribution in barley. Plant Phy-
Treder, W., Cieslinski, G., 2005. Effect of silicon application on cadmium uptake and siol. 160, 1491–1497.
distribution in strawberry plants grown on contaminated soils. J. Plant Nutr. 28, Yamaji, N., Mitatni, N., Ma, J.F., 2008. A transporter regulating silicon distribution in
917–929. rice shoots. Plant Cell 20, 1381–1389.
Tripathi, D.K., Singh, V.P., Kumar, D., Chauhan, D.K., 2012a. Impact of exogenous Yang, Y.H., Chen, S.M., Chen, Z., Zhang, H.Y., Shen, H.G., Hua, Z.C., Li, N., 1999. Silicon
silicon addition on chromium uptake, growth, mineral elements, oxidative effects on aluminum toxicity to mungbean seedling growth. J Plant Nutr. 22,
stress, antioxidant capacity, and leaf and root structures in rice seedlings ex- 693–700.
posed to hexavalent chromium. Acta Physiol. Plant. 34, 279–289. Ye, J., Yan, C., Liu, J., Lu, H., Liu, T., Song, Z., 2012. Effects of silicon on the distribution
Tripathi, D.K., Singh, V.P., Kumar, D., Chauhan, D.K., 2012b. Rice seedlings under of cadmium compartmentation in root tips of Kandelia obovata (S., L.) Yong.
cadmium stress: effect of silicon on growth, cadmium uptake, oxidative stress, Environ. Pollut. 162, 369–373.
antioxidant capacity and root and leaf structures. Chem. Ecol. 28, 281–291. Zeng, F.R., Zhao, F.S., Qiu, B.Y., Ouyang, Y.N., Wu, F.B., Zhang, G.P., 2011. Alleviation of
Tripathi, D.K., Singh, V.P., Prasad, S.M., Chauhan, D.K., Dubey, N.K., Rai, A.K., 2015. chromium toxicity by silicon addition in rice plants. Agric. Sci. China 10,
Silicon-mediated alleviation of Cr (VI) toxicity in wheat seedlings as evidenced 1188–1196.
by chlorophyll florescence, laser induced breakdown spectroscopy and anato- Zhang, C., Wang, L., Nie, Q., Zhang, W., Zhang, F., 2008. Long-term effects of exo-
mical changes. Ecotoxicol. Environ. Saf. 113, 133–144. genous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.).
Tripathi, P., Tripathi, R.D., Singh, R.P., Dwivedi, S., Goutam, D., Shri, M., Chakrabarty, Environ Exp Bot. 62, 300–307.
D., 2013. Silicon mediates arsenic tolerance in rice (Oryza sativa L.) through Zhang, Q., Yan, C., Liu, J., Lu, H., Duan, H., Du, J., Wang, W., 2014. Silicon alleviation of
lowering of arsenic uptake and improved antioxidant defence system. Ecol. cadmium toxicity in mangrove (Avicennia marina) in relation to cadmium
Eng. 52, 96–103. compartmentation. J. Plant Growth Regul. 33, 233–242.
Vaculik, M., Landberg, T., Greger, M., Luxova, M., Stolarikova, M., Lux, A., 2012. Si- Zhang, Q., Yan, C., Liu, J., Lu, H., Wang, W., Du, J., Duan, H., 2013a. Silicon alleviates
licon modifies root anatomy, and uptake and subcellular distribution of cad- cadmium toxicity in Avicennia marina (Forsk.) Vierh. seedlings in relation to
mium in young maize. Ann. Bot. 110, 433–443. root anatomy and radial oxygen loss. Mar. Pollut. Bull. 76, 187–193.
Vaculik, M., Lux, A., Luxova, M., Tanimoto, Li, 2009. Silicon mitigates cadmium in- Zhang, S., Li, S., Ding, X., Li, F., Liu, C., Liao, X., Wang, R., 2013b. Silicon mediated the
hibitory effects in young maize plants. Environ. Exp. Bot. 67, 52–58. detoxification of Cr on pakchoi (Brassica chinensis L.) in Cr-contaminated soil. J.
Vatehová, Z., Kollárová, K., Zelko, I., Richterová-Kučerová, D., Bujdoš, M., Lišková, D., Food Agric. Environ. 11, 814–819.
2012. Interaction of silicon and cadmium in Brassica juncea and Brassica napus. Zia-ur-Rehman, M., Sabir, M., Rizwan, M., Saifullah, Ahmad, H.R., Nadeem, M., 2015.
Biologia 67, 498–504. Remediating cadmium-contaminated soils by growing grain crops using in-
Wagner, G.J., 1993. Accumulation of cadmium in crop plants and its consequences organic amendments. In: Hakeem, K.R., Sabir, M., Ozturk, M., Murmet, A. (Eds.),
to human health. Adv. Agric. 51, 173–212. Soil Remediation and Plants: Prospects and Challenges. Elsevier Inc.,/Academic
Wang, S., Wang, F., Gao, S., 2014. Foliar application with nano-silicon alleviates Cd Press, pp. 367–396.
toxicity in rice seedlings. Environ. Sci. Pollut. Res., 1–9.
Wang, Y., Stass, A., Horst, W.J., 2004. Apoplastic binding of aluminum is involved in
silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol. 136,
3762–3770.