Silicon efficacy for the remediation of metal contaminated soil

Abstract

In the course of past two decade anthropogenic activities have reinforced, begetting soil and water defilement. A plethora of heavy metals alters and limits plant growth and yield, with opposing effect on agricultural productivity. Silicon often perceived as plant alimentary ‘nonentity’. A suite of determinants associated with silicon have been lately discerned, concerning plant physiology, chemistry, gene regulation/expression and interaction with different organisms. Exogenous supplementation of silicon renders resistance against heavy-metal stress. Predominantly, plants having significant amount of silicon in root and shoot thus are barely prone to pest onset and manifest greater endurance against abiotic stresses including heavy-metal toxicity. Silicon-mediated stress management involves abatement of metal ions within soil, co-precipitation of metal ions, gene modulation associated with metal transport, chelation, activation of antioxidants (enzymatic and non-enzymatic), metal ion compartmentation and structural metamorphosis in plants. Silicon supplementation also stimulates expression of stress-resistant genes under heavy-metal toxicity to provide plant tolerance under stress conditions. Ergo, to boost metal tolerance within crops, immanent genetic potential for silicon assimilation should be enhanced. Current study, addresses the potential role and mechanistic interpretation of silicon induced mitigation of heavy-metal stress in plants.

Introduction

Silicon, a tetravalent element, is the utmost profuse metalloid within Earth’s crust following oxygen. Primarily, soil retains approximately 14–20 mg/L of silicon (Debona et al. 2017). Dissipation of silicon from organic soil is imperceptible process and its assimilation and resorption by soil fragments and persistent monoculture may entail substantial impoverishment of soil, therefore soil amendment with silicon is requisite to procure high yield and is a cost-effective agronomic practice for preventing the adverse effects (David et al. 2024; Ahmed et al. 2023). Histosols, an organic soil possesses insignificant amount of silicon, other soil orders like oxisols and ultisols are extremely weathered, percolated and poor in base saturation. Soils composed of quartz-sand (silica-SiO₂) like sandy entisols possibly have greater amount of insoluble silicon but lack beneficial silicon for plant uptake. Rest soil orders regarded low/constraining are acidic inceptisols, spodosols, and acidic alfisols (Tubana et al. 2016; Datnoff and Rodrigues 2015). Soil weathering emancipates silica into soil solution, water bodies and surface waters in the form of monosilicic acid, omnipresent and uncharged monomeric substance existing below pH 9 (Kovács et al. 2022; Tubana and Heckman 2015).

Each plant species cultivated in soil contains definite amount of silicon within tissues. When ascertaining whether plant accrues silicon or not, former research has focused mainly on estimation of silicon concentration in foliage only. Recent studies demonstrated that concentrations of plant-available Si vary considerably and show pronounced inter and intra specific variation in foliar Si concentrations (Klotz et al. 2023). Howbeit, tomatoes, coffee and peppers retain silicon more in roots in contrast to shoots (Carre-Missio et al. 2009; French-Monar et al. 2010; Huang et al. 2011). Translocation of silicon from roots to shoots drastically differs among plant varieties and growth rate. Monocots tend to accrue more silicon in shoots juxtapose to dicots. Silicon is reckoned as quasi-essential compound for development/growth of various plant species (Ali et al. 2023a, b; Naz et al. 2023). Silicic acid (H₄SiO₄), accessible form of silicon existing in soil is uptaken by plants and subsequently active or passive distribution of silicon from roots to shoots ensues (Ma et al., 2011). Peculiar transporter proteins are responsible for silicon uptake and accretion from roots to shoots and were initially characterized in specific monocots viz wheat, barley and rice (Montpetit et al. 2012; Chiba et al. 2009; Ma et al. 2006), withal dicots viz soybean, cucumber and pumpkin also possess similar transporter proteins (Deshmukh et al. 2013). Following endodermis penetration, silicon progresses through xylem via transporter proteins or transpirational drift to root endodermis, cell surface of vascular bundle and epidermis of leaf and later deposited underneath the cuticle thus acting as a first line of defense against various kinds of stresses (Kaur and Greger 2019; Ma et al. 2007). Polymerization of silicic acid (H₄SiO₄) into insoluble silica may eventuate in roots but is highly ubiquitous beneath cuticle as well as in plant cell-wall.

Plants being sessile are constantly vulnerable to various abiotic and biotic stresses, impairing their growth, development and yield. Among abiotic stressors, heavy metals are considered most mendacious. Heavy metals are metallic substance with comparatively high density and are noxious yet at low concentration. Atomic density of heavy metal is more than 4 g cm⁻³(Ejaz et al. 2023; Hawkes 1997). Heavy metals comprehend arsenic, aluminum, lead, cadmium, zinc, chromium, nickel, copper, manganese etcetera and majority of these elements play fundamental role in plants. Geologic and anthropogenic proceedings augment heavy-metal concentration, thereby leading to toxic and detrimental effect on different life forms (Chibuike and Obiora 2014). Soil contamination by heavy metal has emanated as perilous and consequential concern due to unfavorable environmental effects. Heavy metals impede plant proliferation by marginalizing activity of lipids, proteins and other elemental constituents of thylakoid membrane (Kim et al. 2014a). Forbye, heavy metals get transferred to animal and human via food chain, begetting risk to human health (Uddin et al. 2023; Nagajyoti et al. 2010). Plants amended with silicon thwart various abiotic stresses particularly mineral deficiency, heavy-metal toxicity, cold, salinity, drought, and heat more proficiently (Adrees et al. 2015; Rizwan et al. 2015). Beneficial impacts of silicon were unperceived prior twentieth century, due to its profusion in environment and lack of evident symptoms of deficiency. Irrespective, in field and greenhouse conditions, plants frequently exposed to various stresses apparently suffer more silicon deficient conditions (Datnoff and Rodrigues 2015). This anatomization intends to dispense the prospective of silicon in mitigating abiotic stress in plants.

Rudimentary role

Despite its ubiquitous characteristics, silicon has been omitted from imperative class of elements, as it fails to appease Arnon and Stout (1939) one criteria of vital element class, precisely, corroboration of its potentiality in plant metabolism. As per redefinition silicon in plant science (higher plants) is dominated by multifarious effects and roles including stress amelioration, gene expression and metabolism (Fig. 1). Silicon is found in each terrestrial plant varying from 0.1 to 10% based on dry biomass, plant species (Zaid et al. 2018). Silicon is absorbed in monosilicic acid form and precipitated within plant parts, viz cell membrane and lumens. Furthermore, it is stored as amorphous silica or phytoliths in inter-cellular locales, where phytolith means ‘stone of plant’ (Piperno 2006). In spines silicon is amassed as amorphous silica and phytoliths. Synthesis of epidermal trichomes and hairs in leaves are reinforced by silicon (Hartley and DeGabriel 2016). Exposure to silicon offers firm lodging in plants by imparting mechanical endurance, enhancing rigidity of cell walls. Silicon deposition within epidermal tissues facilitates excessive loss of water via transpiration (Imtiaz et al. 2016). Plants vary substantially as per the uptake capacity of silicon via various mechanisms and are further categorized as accumulators comprising wet land plants, intermediate accumulators comprising dry-land plants and excluders or non-accumulators consisting dicots. Aquaporins in plants occur in many isoforms, which increases the possibility of transporting various substances in various tissues and improves the selectivity of this process (Deshmukh et al. 2016), both to and from cells. The studies of changes in the expression of AQPs are very useful for the description of water transport regulation under, among others, drought stress conditions, but the effectiveness of AQPs varies greatly depending on the plant’s growth conditions, its stage of development, type of tissue, duration, and intensity of stress. Silicon changes aquaporin expression and antioxidant system activity in a direction which may alleviate the effects of drought stress in oilseed rape (Garbarz et al. 2022). Active, passive and rejective are three forms of silicon assimilation for corresponding accumulators, intermediates and non-accumulators respectively and the corresponding types of Si-accumulator plants are as follows: (1) high accumulators, e.g., rice and sorghum. (2) intermediate accumulators, e.g., cucumber (3) excluders, e.g., tomato (Zhu et al. 2019; Ma et al. 2001, 2006). Subsequent absorption by roots, silicon is transported to shoots via xylem. Generally, plants produce ROS incessantly throughout photosynthesis and respiration within cell organelles viz peroxisomes, mitochondria and chloroplast. Plants perpetuate homeostasis by distinct detoxification techniques comprehending enzymatic antioxidants viz superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX) (Racchi 2013; Kim et al. 2014b, c) and non-enzymatic antioxidants like carotenoids, glutathione, tocopherol, ascorbate (Sytar et al. 2013; Wu et al. 2017). The direct impact of heavy metals on plants is excessive production of ROS that destabilizes the plant’s metabolism and leads to fetal disorders (Awan et al. 2022). Reduction of oxidative damage via decreased production of reactive oxygen species (ROS) and/or increased activity of antioxidant metabolism appears to play an important role in Si-induced abiotic stress alleviation. Furthermore, decreased ROS accumulation, reduced lipid peroxidation, increased concentrations of AsA and GSH, and improved antioxidative capacity are also suggested to explain Si-mediated metal stress tolerance (Jiang et al. 2023). Si also regulates carbohydrates metabolism and proline accumulation that facilitate cell-wall lignification to detoxify ROS, maintain membrane integrity, and stabilize protein (Wang et al. 2021). Supplementation of Si effectively mitigated the oxidative burst by increasing the activity of the antioxidant system, up-regulating the amount of ascorbate (AsA) and glutathione (GSH) and detoxification of methylglyoxal (MG) by increased activities of glyoxalase system in Brassica napus (Hasanuzzaman et al. 2018). Preponderantly, SOD catalyzes systematic eradication of superoxide free radicals within chloroplast because their formation occurs during light reaction in photosystem I. CAT is traced in peroxisomes and is involved in obliteration of H2O2, produced during SOD reaction, similar activity is displayed by another antioxidant namely APX however it is sited in peroxisomes, mitochondria, chloroplast and cytosol (Racchi 2013). The second line of defense toward oxidative stress is non-enzymatic antioxidants classified as hydrophilic substance (ascorbate, glutathione) and lipophilic molecules (carotenoids, α-tocopherol) (Racchi 2013; Suzuki et al. 2014; Gowayed et al. 2017). Ascorbate has potential to scavenge ROS instantly in the cell it also functions as reaction matrix of APX (Szarka et al. 2013) due to its diverse roles ascorbate is deemed as highly potent antioxidant within plant system (Gill and Tuteja 2010; Suzuki et al. 2014). Glutathione, an essential hydrophilic antioxidant irresistibly scavenges ROS from chloroplast. Furthermore, glutathione guards thiol groups of chloroplast based enzymes and partakes in synthesis of ascorbate and α-tocopherol. Glutathione incites physiologic responses for instance modulation of sulfur translocation and defense related gene expression. The multiplicity of these roles probably explains why glutathione status has been implicated in influencing plant responses to many different conditions (Noctor et al. 2024; Racchi 2013). Furthermore, Si activates the antioxidant defense system to decrease the excessive production of ROS and other free radicals under stressful condition (Rahman et al. 2021). Thus, the application of Si decreases oxidative damage in plants by regulating various antioxidants such as SOD, POD, CAT, GR, GPX, proline, ascorbic acid, organic acids, and amino acids, etc. to alleviate metal toxicity (Khan et al. 2022). Silicon accruing species might enact in primary metabolism of plants (Van Bockhaven et al. 2015b). Silicon is acknowledged to benefit wide range of plants globally (Coskun et al. 2016).

Fig. 1.

Possible mechanism of amelioration of abiotic stress via silicon (Modified after Daoqian et al. 2018)

Silicon uptake, transport, and accumulation in plants

Plants diverge noticeably in their ability to absorb Si and due to numerous chemical transformations and differences in the uptake and transport mechanism within plants, various plant tissues have different concentration of Si. Si uptake in plant roots occurs as H₄SiO₄, a neutral monomeric moiety and this uptake is carried out by specific transporters which were first identified in rice (Ma and Yamaji 2015). OsLsi1 is the first Si uptake identified gene which is predominantly expressed in roots and further studies have demonstrated that Si transporters OsLsi1 and OsLsi2 are accountable for greater Si uptake in Oryza sativa (Ma et al. 2006; Fig. 2). Two Si-influx transporters ZmLsi1 and ZmLsi6 found in maize are similar to OsLsi1 and OsLsi6 however, their functional organization and cellular location is dissimilar. Location of OsLsi1 is root exodermis and endodermis while ZmLsi1 is found in lateral roots epidermis and cortex and in seminal roots epidermis and hypodermis (Seal et al. 2018). Those plants which uptake higher amount of Si than water are considered as active, whereas those with similar levels are recognized as passive and those with lower uptake levels are known as rejective (Kaur and Greger 2019).

Fig. 2.

Diagrammatic representation of Si uptake and transport (A) in rice (B) in maize (modified after Pontigo et al. 2015)

Active Si-uptake process in plants causes noteworthy reduction in Si thus decreasing Si amount in the nutrient solution; whereas through passive mechanism, Si amount remain unaltered in the nutrient solution and those with rejective mechanism enhances Si amount in the nutrient solution. Facilitated or simple diffusion mediated passive process is a concentration-dependent constituent of Si uptake in plants irrespective of their Si accumulation capacity (Raven 2003; Yan et al. 2018). Si has been found in all plant tissues based on dry mass, with its amount in stem changing amid 0.1 and 10 percent (Ma et al. 2011; Liang et al. 2015).

Si is translocated to the upper part of the plant by transpirational H₂O flow by means of xylem afterward its absorption by roots (Ma et al. 2006) and greater than 90 percent of Si absorbed via roots are transferred to the upper parts of many plants (Ma and Takahashi 2002). Si deposition occurs in various plant parts for instance shoot epidermis, root endodermis cell wall (Lux et al. 2003; Keller et al. 2015). After transfer of Si from the xylem apparatus into the leaf sheaths and blades, Si is concentrated due to transpiration and then transformed into amorphous silica (SiO₂enH₂O) via Si polymerization in shoots and then this SiO₂enH₂O is deposited in cell wall, roots cells, cell lumen, intracellular spaces, and trichomes which ultimately provides tissue strength and is also observed in the upper and lower side cuticle (Bakhat et al. 2018). Si-influx transporters Lsi1 and Lsi6 which are aquaporin family transporters are associated with Si distribution in root and shoot tissues (Mitani et al. 2011). Si accumulation mainly takes place in those areas where higher rate of transpiration occurs for instance leaf epidermis near the stomatal guard cells, trichomes and thorns that are involved in alleviation of harmful effects of abiotic and biotic stresses.

Silicon potentiates against metal toxicity

Heavy-metal toxicity destructively influences the various biological developments of plants which ultimately affects growth and productivity in almost all plant species. Si is useful in alleviating metal toxicity by escalating the plant morphology, functioning of gas exchange attributes, stomatal movement, regulating transpiration rate and H₂O usage efficacy, photosynthetic activity, nutrient balance, regulating level of plant hormones and antioxidant defense system (Malhotra and Kapoor 2019).

Silicon mediated cadmium tolerance

Cadmium (Cd) antagonistically competes with nutrients acquisition and disturbs plant physiologic attributes, thus restricting plant survival in polluted soils. Cd toxicity causes obnoxious effects on various plant basic functions at physiologic, biochemical, and molecular level from seed germination till maturation and final seed dispersal (Zhou et al. 2021; Wu et al. 2022). These includes reduced crops nutrition values, inhibition of carbon fixation, reduced chlorophyll content, photosynthetic efficiency, suppression of antioxidant, chlorosis, stomatal density and conductance. Further it alters protein patterning and inhibits storage protein catabolism. There is also inhibition of radical–formation and lateral root–formation, reduction in root respiration, reduction in transpiration and leaf relative water content. The yield is affected by irregular uptake and transportation of mineral elements, destruction and damage to plant membranes and membranous organelles, disrupted cellular osmoregulation, and ROS generation viz., hydrogen peroxide (H₂O₂), hydroxyl radical (.OH), superoxide radicals (O₂⁻) and singlet oxygen (¹O₂) (Aslam et al. 2023; Li et al. 2023), silicon can palliate above mentioned conditions (Thakral et al. 2024; Pan et al. 2023). Silicon can abate cadmium mediated plant growth inhibition. Cadmium inhibits photosynthesis in vascular plants. Higher concentration of cadmium within leaves negatively correlates elements of chlorophyll and carotenoids (Prasad 1995). Silicon mitigates the impediment of photosynthesis induced by cadmium toxicity in cucumber. Impairment of photosynthetic machinery following cadmium toxicity within cucumber can be relieved by silicon, significantly diminishing blade chlorosis, guards thylakoid membrane and chloroplast membrane, preclude chloroplast swelling and increasing pigment content (Khodarahmi et al. 2012). Compared to cadmium treatment solely, silicon and cadmium treatment remarkably enhanced chlorophyll and carotenoids contents, photosynthetic rate, water retention, stomatal conductance, but declined intracellular CO₂ level. Pursuant cadmium toxicity, administration of silicon considerably escalates the quantum yield of photosystem II in the dark state, substantial quantum efficiency of photosystem II (Feng et al. 2010). Further clarity gained regarding silicon incited alleviation of cadmium stress at molecular level in rice plants through leaf proteome study. It also improved rice plant biomass and photosynthetic rate under cadmium toxicity (Nwugo and Huerta 2011). ROS have immense reactions, critical to respiration, photosynthesis, fatty acids and plasma membrane. ROS scavenging under cadmium stress is mediated by silicon through activation of antioxidant defense system (enzymatic and non-enzymatic). To mitigate cadmium stress, silicon regulates the activity of APX, CAT and SOD, but lowers the levels of malonaldehyde (MDA) and H2O2 in Brassica chinensis (Song et al. 2009). Cadmium toxicity drastically raised the concentration of non-protein Thiols, GSH and AsA, and much elevated levels were observed under cadmium and silicon exposure (Shi et al. 2010). Cadmium is uptaken and stored easily within plants. Silicon reduces cadmium assimilation in rice plant (Zhang et al. 2008) cucumber (Feng et al. 2010) and pakchoi (Song et al. 2009). Supplementation of silicon notably reduces the cadmium concentration in leaf cell organelles of peanut (Shi et al. 2010).

Silicon mediated lead tolerance

An agricultural area defiled with lead (Pb) is a concern for bionomics posing lethality on fauna and flora. Moreover, lead uptake and its nocuous effect depends upon plant variety and soil properties (Imtiaz et al. 2016). To fathom the impact of silicon in mitigating lead stress a trial was conducted in which nano silicon and normal silicon were implemented to monitor the translocation and absorption of lead in rice cultivars, where it demonstrated restricted uptake and distribution. Augment in biomass of rice cultivars from 3.3 to 11.8% and 1.8 to 5.2% in silicon amended soil with 500 and 1000 mg/kg respectively in comparison to control rice plants. Besides, rice plants accumulated very less amount of lead and reduced translocation from roots to other plant parts under silicon treatment (Liu et al. 2015). In another study accumulation of silicon in shoots reduces lead uptake, but does not affect lead precipitation, cellular localization of lead in roots, or root-to-shoot transport of lead. Si-induced reduction of lead uptake in rice roots is most likely caused by down-regulation of genes encoding proteins that take up and/or transport lead along with other nutrients (Gong et al. 2023). Remediating lead induced toxicity in rice plants through silicon is an appropriate technique. To neutralize lead toxicity in cotton plants an experiment was conducted where silicon treatment significantly lowered the lead assimilation, electrolyte leakage, melondialdehyde and hydrogen peroxide contents (Bharwana et al. 2013). Silicon implementation in cotton cultivars also increased the antioxidant activities within roots and leaves. The results also signified higher biomass, growth, photosynthetic and chlorophyll content via silicon treatment under lead stress.

Silicon mediated arsenic tolerance

Arsenic (As) a metalloid is a major carcinogen and ubiquitous ecological contaminant (Li et al. 2016). Ecological contamination lead by arsenic is critical predicament owing to detrimental effect on soil, plants vigor and human wellbeing. Arsenic contamination is rampant, attributable to anthropogenic activities (industrialization) and naturogenic events (weathering) and the toxicity and harmful impacts on human health have made arsenic a persistent global concern. (Rahman et al. 2024). Phyto accessibility of arsenic is reliant on concentration of availability of phosphorus in soil. Arsenate existing as an analog of phosphate, uses several phosphate channels within roots to penetrate plant cells, while arsenite ingression is induced through aquaporin channels which are silicon transporters. Arsenic, following its absorption as arsenate, it is transformed to arsenite that generates ROS, alters morphology, biochemistry and physiology of plants and interrupts ion homeostasis (Ghulam Abbas et al. 2018). Silicon intervened allaying arsenic stress is preferable strategy to decontaminate arsenic polluted sites. Silicon-mediated upsurge in antioxidant defense system efficaciously reduces the oxidative impairment and improves phyto tolerance toward arsenic stress. Increase in pigment levels, photosynthetic rate, chloroplast stability and photosystem II integrity are achieved via silicon treatment under arsenic stress (Sil et al. 2019). Silicon effectively remediated noxious aftermath of arsenic in rice cultivars. Silicon amendment remarkably neutralized the negative effect of arsenic on carbohydrate levels and photosynthesis. Addition of silicon further reduced the arsenic uptake and transport within rice cultivars by expressing certain genes (Lilian et al. 2016). Another investigation specified that silicon administration considerably improved straw biomass and impeded arsenic deposition in roots and shoots of six rice species (Chuan et al. 2015). Likewise, silicon boosts arsenic tolerance in rice cultivars specifically Triguna species, by remediating oxidative stress triggered by arsenic and further obstructing arsenic assimilation and enhancing antioxidant defense system and thiolic system (Preeti et al. 2013). Increase in seed germination rate in tomato plants under arsenic stress is achieved by silicon treatment. Restricted accretion and translocation of arsenic in shoots and roots of Solanum lycopersicum plant via silicon treatment, withal accumulation of arsenic is plant dependent (Marmiroli et al. 2014).

Silicon-mediated chromium tolerance

Chromium (Cr) is potentially hazardous and serves no vital role in plant metabolism. Lately, environment defilement with chromium via anthropogenic activities and industrialization is a matter of concern. Emission of chromium globally exceeded other heavy metals viz cadmium, lead and mercury. It is the second most frequent metal pollutant in soil, groundwater, and sediment, and it poses a serious environmental risk (Ali et al. 2023a, b; Zulfikar et al. 2023). Chromium occurs in heterogeneous forms howbeit, the exceedingly noxious form to living beings is chromium VI due to it easy penetration through cell-wall and enter cytoplasm, affecting metabolic pathways (Singh et al. 2013). Chromium elicits detrimental effect on plant’s development and growth, it induces limited seed germination, leads to oxidative stress, perturbs nutrient intake, photosynthesis and water balance (Ali et al. 2011; Gangwar and Singh 2011; Singh et al. 2013). Mitigation of chromium toxicity is requisite in order to improve crop yield and diminish chromium entry in food chain. A research conducted to determine the impact of silicon on chromium induced toxicity demonstrated that silicon supplementation considerably assuages the pernicious effect of chromium in wheat cultivars. Findings from laser induced breakdown spectroscopy (LIBS) exhibited diminution in chromium accretion in Triticum plants after silicon administration. The results acquired from LIBS and inductively coupled plasma atomic emission spectroscopy (ICAP-AES) manifested that silicon treatment augments nutrient (potassium, calcium, sodium and magnesium) uptake in wheat plants subjected to chromium stress (Tripathi et al. 2015). Another study revealed that application of silicon significantly alleviated toxic impact of chromium in barley cultivars by boosting plant growth, stomatal conductance, total photosynthetic rate, chlorophyll fluorescence efficacy, carbon dioxide levels and transpiration rate. Moreover, silicon treatment reduces ultra-structural changes viz alteration in leaves and root morphology, impair thylakoid membrane, higher plastoglobulin levels, swelling in chloroplast, accretion of chromium in cell walls and nucleus disruption mediated by chromium stress in roots as well as shoots (Ali et al. 2013).

Silicon-mediated zinc tolerance

Exorbitant amount of zinc (Zn) induces toxicity in plants and eventually quietus of plants (Kaya et al. 2018). Plant raised in presence of higher levels of zinc had reduced chlorophyll levels, root browning, anomalous plant growth, decreased uptake and translocation of nutrients, chlorosis, and less biomass yield (Andrejic et al. 2018). Above optimum concentration that is 300 mg kg⁻¹, zinc becomes fatal for plant species within soil (Ehsan et al. 2013). Yet, silicon amendment in Schizolobium amazonicum plants lowered the zinc stress via protecting cell membrane permeability susceptible to high zinc concentration, lowered zinc accumulation in shoots (Albuquerque et al. 2020). Silicon evinced salutary role in vegetative growth of Zea mays (de Sousa Paula et al. 2015), Gossypium hirsutum (Anwaar et al. 2015) and Oryza sativa (Mehrabanjoubani et al. 2015) exposed to zinc. Probably the higher phyto biomass in silicon amended soil induced dilution effect on zinc levels, thus reducing zinc mediated destruction of plants. Silicon positively effects iron concentration in leaves of maize and tobacco promoting chlorophyll synthesis under zinc stress. Silicon immensely reduces zinc accumulation in Gossypium hirsutum thereby limiting zinc bioavailability via altering solution pH (Anwaar et al. 2015). Within plant cells, silicon augments tolerance toward zinc toxicity through formation of zinc-silicate inside cytoplasm (Gong et al. 2005). Silicon inhibits distribution of zinc to shoots by getting deposited on cell membranes thereby forming barrier to apoplastic route. Additionally, silicon up-regulates antioxidative enzymes such as SOD and POD stimulating plants to withstand zinc elicited oxidative damage (Farid et al. 2013).

Si-mediated nickel tolerance

Nickel (Ni), is amongst the noxious heavy metals whose source of contamination are Ni coating industries, waste water disposal, mining actions, fossil fuels scorching, supplementation of chemicals etc. (Turan et al. 2018, Rizwan et al. 2018). Ni at high amounts causes oxidative burst by generating plethora of ROS (Khan et al. 2016, Turan et al. 2018, alters the photosynthetic functioning, and suppresses photosynthetic pigments biosynthesis (Sirhindi et al. 2016), ultimately affecting various biological processes of the plants. Si application alleviates the Ni induced damages by improving plant growth, chlorophyll level, functioning of SOD, CAT and APX enzymes, decline ROS level by decreasing the MDA content, H₂O₂ and electrolyte leakage (EL), in Brassica juncea and this Si triggered reduction of Ni stress is because of enhancement in the functioning of antioxidant system, glyoxalase detoxification structures and compatible solutes accumulation (Abd-Allah et al. 2019). Si supplementation increased the tolerances of Oryza sativa to Ni toxicity by escalating the function of APX, SOD, GST and antioxidants (AsA, GSH/GSSG ratio) and also improved functioning of enzymes associated with glyoxalase systems which helps to diminish the ROS levels (Hasanuzzaman et al. 2019). Ni decreased the plant growth, biomass and altered the functioning of antioxidant system. Ni exposure also increased the level of MDA, H₂O₂ and EL in cotton plants but Si supplementation improved the plant growth, lowered the ROS level and reduced the amount of MDA, H₂O₂ and EL. Si treatment further enhanced the activities of antioxidative enzymes and also decreased Ni uptake and accumulation in various parts of plant under Ni stress (Khaliq et al. 2016). Si induced escalation in plant growth is due to elevation in plant nutrient absorption and regulating root organization under Ni stress (Keller et al. 2015).

Si-mediated copper tolerance

High levels of copper (Cu) in plants induces phytotoxicity and reduced plant development, photosynthesis, relative H₂O content and mineral nutrients (Christiansen et al. 2015). High accumulation of Cu in cells alters functioning of lipid membrane by the formation of ROS in different plant parts due to its redox active nature (Habiba et al. 2015). Si alleviated the Cu toxicity in cotton by amplifying growth, photosynthesis, optimal functioning of antioxidative enzyme and declines ROS level by reducing electrolyte leakage, H₂O₂ and thiobarbituric acid reactive substances (TBARS) level and also condensed the Cu levels in various plant parts (Ali et al. 2016). Si restricts Cu uptake and transfer to upper parts by restricting translocation due to increased condensing of Si containing endodermis, disabling its transport in the root epidermis and enhanced Cu complexation (Keller et al. 2015). Si expressively strengthens plant tolerance to Cu toxicity by activating the Cu-binding molecules via escalating the expression of SOD genes i.e., CSD1 and CSD2 in Arabidopsis thaliana (Khandekar and Leisner 2011). Si alleviated Cu toxicity by reducing upward translocation of Cu to the shoots and leaf phytoliths produced in Si supplemented plants, also strengthens plant tolerance to Cu toxicity by Cu immobilization and inactivation in Erica andevalensis (Oliva et al. 2011).

Si-mediated manganese tolerance

Manganese (Mn), an essential micronutrient which is beneficial for plants in minute amounts but higher Mn amounts results in toxic effects in plants and generates plethora of ROS generation ultimately affects plant productivity. For most plants, approximately 20–40 mg per kg (dry weight) is enough for normal development. The contents of Mn in leaves of various kinds of plants are different, generally 30–500 mg per kg (dry weight). However, Mn is extremely toxic to plants when its concentration exceeds the threshold in crops (Wang et al. 2023).Mn toxicity in cucumber results in escalated generation of OH^. ions in the leaf apoplast but application of Si mitigated the Mn toxicity by declining OH^. radicals through lessening the apoplastic Mn²⁺ level (Dragišić Maksimović et al. 2012). Si abridged the mass of brown spots per leaf area, improved plant morphologic parameters and maintains the membrane integrity by maintaining the lipid peroxidation in Zea mays under Mn toxicity (Stoyanova et al. 2008). Si mechanism of Mn storage in non-photosynthetic tissue of maize is an important strategy for improving plant tolerance to Mn noxiousness (Doncheva et al. 2009). Application of Si significantly improved Mn tolerance in Oryza sativa by increased root and shoot length, and diminished ROS level by up-regulating the functioning of SOD, CAT and APX, and level of AsA and GSH and also decreased the MDA and H₂O₂ levels (Li et al. 2012a, b). Treatment with Si alleviated Mn toxicity in Oryza sativa by enhancing plant growth, content of chlorophyll, promoted CO₂ assimilation by stabilizing the structure of PSI and enhanced the expression of photosynthetic related genes i.e., HemD, Lhcb3 (Li et al. 2015). Si rice plants tolerance to Mn toxicity by reducing the uptake of Mn (Tavakkoli et al. 2011).

Si-mediated aluminum tolerance

Abundance of aluminum (Al) in plants results in elevated ROS level by production of plethora of O2⁻, OH, and H₂O₂ ions (Singh et al. 2017). Si alleviated Al toxicity in Arachis hypogaea by upgraded root and stem length, fresh and dry mass, photosynthetic apparatus functioning and also diminished the ROS level by elevating the actions of CAT, SOD and POD enzymes (Shen et al. 2014). Al-stimulated lipid peroxidation in ryegrass but Si application mitigates Al-induced oxidative stress by improving phenols amount, functioning of SOD, CAT, POX and APX enzymes and also via enhancing the expression of Si-transporter genes i.e., Lsi1 and Lsi2 (Pontigo et al. 2017). Si alleviated Al toxicity in the rice by improved plant growth and declined Al transport to the plant shoots (de Freitas et al. 2017). Si reduced Al accumulation, improved stomatal frequency, length of root hairs and maintained the assembly and internal structure of mesophyll cells and phloem and maintained mineral-nutrients levels in rice against Al toxicity (Singh et al. 2011).

Molecular mechanisms of silicon-mediated detoxification under heavy-metal stress

Si-facilitated mechanisms for metal decontamination has been widely researched in several plant varieties. Well recognized Si-mediated mechanisms involve immobilization of metals (at soil level) and diminishing ROS level by improving the antioxidant system, compartmentation of metals in plant tissues, chelation, regulation of gene expression and structural modifications in various portions of plants (at plant level; Fig. 3).

Fig. 3.

Si-mediated mechanisms for alleviation of heavy-metal toxicity (modified after Imtiaz et al. 2016)

Silicon-mediated immobilization of toxic metal in the soil

One of the straightforward mechanisms of Si by its treatment is immobilization of noxious metal in the soil. Supplementation with high amounts of Si (sodium metasilicate) triggers increase in soil pH or alters metal speciation in soil solution via the production of silicate complexes which ultimately diminishes heavy-metal bioavailability (Liang et al. 2007; Rizwan et al. 2012). Si supplementation decreased the absorption of Pb in banana, when sown in Pb polluted soil and this reduced absorption of Pb was related with considerably escalated soil pH and declined fraction of exchangeable Pb (Li et al. 2012a, b). Si also reduced the heavy-metal detoxification by modifying the form of metals in soil solution by converting toxic metal to non-toxic form via making silicate molecules (Putwattana et al. 2010). Si significantly lessened the exchangeable Cr level in soil by escalating the precipitation of Cr fraction which is bound with organic matter (Ding et al. 2013). Si decreased Pb metal mobility in soil by converting Pb into non-toxic insoluble Pb-silicate (Shim et al. 2014) and reduced Cr availability in soil by enhancing proportion of precipitation-bound, organic matter bound Cr fraction and by reducing the proportion of commutable Cr (Zhang et al. 2013).

Stimulation of antioxidant defense system

Heavy-metal stress triggers production of plethora of ROS, which disrupts the functioning of antioxidant system and also causes several biological and metabolic alterations. However, Plants have an extremely useful and effective antioxidant system which involves enzymatic and non-enzymatic antioxidants in order to mitigate the excessive ROS generation and guard plants against oxidative damage. Treatment with Si diminishes heavy metal caused oxidative burst by declining the ROS level and by improving the action of plants antioxidant system which defend plants by sustaining the internal structure of chloroplast, mitochondria and nucleus (Nwugo and Huerta 2008; Song et al. 2009; Shi et al. 2010). Si is beneficial in maintaining membrane integrity in cotton plants by reducing the level of MDA, H₂O₂ and EL in roots and stem under Cd (Farooq et al. 2013), Zn (Anwaar et al. 2015) and Pb stress (Bharwana et al. 2013). Elevation in the antioxidative enzyme activities after Si treatment maintains the balance amid ROS generation and ROS detoxification, thereby defending plants from the oxidative injury. Heavy-metal stress reduces the functioning of antioxidant enzymes but Si improves the action of SOD, POD, CAT, APX under stress conditions to enable plants to survive in the stress circumstances and escalated activities of these antioxidative enzymes are extensively recognized useful for mitigation of heavy-metal stress. These alterations in functioning of antioxidative enzymes vary with plant variety, age of the plant, duration of treatment and environmental circumstances (Hussain et al. 2015).

Compartmentation within plants

Compartmentation of metals in various plant roots and shoots is extensively studied to recognize Si-mediated metal detoxification strategies in plants. This mechanism of Si-mediated compartmentation for metal detoxification varies with plant species, genotypes and category of heavy-metal stress imposed. Si-mediated metal compartmentation in the leaves and roots of plants might be vital machinery for metal absorption and detoxification, ultimately showing the positive influence of Si. Williams and Vlamis (1957) showed for the 1st time that influence of Si in mitigating Mn toxicity is due to enhanced compartmentation within the leaf tissues of barley, not because of decline in Mn amount. Rice plants have more metal amounts in roots as compared to stem and leaves when cultivated on mixture of metal polluted soils (Gu et al. 2011). Si supplementation enhanced Cd level in roots of wheat plants and declined transfer to upper parts of plant (Naeem et al. 2015). Si treatment abridged the transfer of Cd from root to stem in rice plant by 33% and found that deposition of Cd was predominantly in the endodermis and epidermis and Si was more concentrated in the endodermis in comparison to epidermis hence, Si concentration in endodermis is a crucial factor for decline in Cd translocation (Shi et al. 2005). Transport of heavy metals to metabolically less active cellular tissues for instance to the cell walls, is a significant strategy for Si-induced plant tolerance to heavy-metal stress (Adrees et al. 2015). Si did not alter the dispersal of Cd in roots of maize but substantially reduced symplastic and enhanced apoplastic level of Cd in stems (Vaculik et al. 2012).

Chelation-mediated metal toxicity rReduction with silicon application

Flavonoid, other phenol compounds or organic acids triggered metal chelation is one of the major mechanisms for metal detoxification through Si supplementation. Si reduces the metal toxicity in plants by indirectly encouraging the chelation of heavy-metals. Phenolics such as catechin and quercetin mitigate Al-metal toxicity in the root tip apoplast due to its chelating activity. Si enhanced the ratio of organic and inorganic Cu(I)S-ligands in leaves and these ligands can chelate Cu and can elevate the Cu sequestration to smaller noxious form in bamboo (Collin et al. 2014). Malate, citrate and aconitate amount is enhanced in roots by Si application in wheat under Cu stress and due to Si, Cu forms compounds with organic acids and declines the Cu transfer to upper plant parts (Keller et al. 2015).

Regulation of gene expression

Si alters the gene expression to reduce the metal-induced toxicity. Si addition stimulated expression of OsHMA3 and OsLsi genes under Cu/Cd stress to provide plant tolerance to stress conditions in Oryza sativa plants (Kim et al. 2014a, b, c). Si reduced the Cu metal-induced adverse effects in Arabidopsis by escalating the expression of phytochelatin synthase 1 (PCS1) gene and declining the expression of metallothionein gene (MT1a) (Khandekar and Leisner 2011). Si application reduced Cd toxicity in wheat plants by escalating the activity of Lsi1 gene and decreasing the function of natural resistance-associated macrophage protein5 (Nramp5) gene (Ma et al. 2015). Si addition in rice plants lowers Zn metal stress, improves the functioning of Os08g02630 (PsbY), Os05g48630 (PsaH), Os07g37030 (PetC), Os03g57120 (PetH), Os09g26810 and Os04g38410 genes that are related with photosynthetic activity of rice plants (Song et al. 2014). It is reported that Si causes Arabidopsis thaliana call walls to bind more strongly to Cu as has been proposed for Mn (Liang, 2007). The stronger binding to the wall caused by Si should sequester Cu so the metal would not enter cells and influence expression of Cu-binding molecules. Therefore, we would expect gene expression levels of Cu-binding molecules (MTs and SOD) as well as PCS1, to increase in the presence of toxic levels of Cu and to decline in response to Si. Leaf PAL activity was previously found to mirror Cu toxicity symptoms in Arabidopsis thaliana (Li et al. 2023). Therefore, it is hypothesized that all four Arabidopsis thaliana PAL genes would show the same pattern of expression and that this would closely follow the changes in enzyme activity reported by Li et al. (2023). Finally, it is expected that the expression of several genes induced in Arabidopsis thaliana roots by Cu identified by Zhao et al. (2009), would be down-regulated in plants provided with Si because the Cu would be sequestered in the cell wall. Drought stress causes shortage of water, nutrient imbalances, ion toxicity, and oxidative stress (Thorne et al. 2020). Common plant responses include a decline in growth that is expressed by the down-regulation of protein encoding genes involved in cell-wall expansion, DNA and protein synthesis, inhibition of photosynthesis by down-regulation of photosynthetic genes encoding basic components of photosystem I and II and also by closing of stomata and destroying photosynthetic apparatus and chlorophyll material (Waraich et al. 2011). It has been described that Si enters the plant by specific Si-influx transporters (Lsi1) from the outside environment and is translocated by efflux transporters (Lsi2) into xylem and then into the aerial parts of the plants where it deposits as amorphous silica in various organs and cells (Mandlik et al. 2020). These Si-influx transporters are part of large family of aquaporin’s (AQPs), a class of channel-forming proteins that facilitates water transport and several other tiny solutes throughout the cell membrane. The mechanism involved in Si-mediated drought alleviation in crop plants at molecular level can be illustrated as follows: Secondary messengers such as Ca2 + , ROS, ABA and phospholipids send initial signals to drought-responsive genes via kinases (Malik et al., 2014). These genes encode functional proteins that protect cellular proteins, maintain membrane integrity besides water absorption and transport (Hu and Xiong, 2014). Transcription factors (TFs) regulate transcription activity either by activating or repressing genes and ultimately leading to downstream plant responses, especially during stressful conditions (Ahammed et al. 2020). The WRKY transcription factors (TFs) regulate the growth, development and stress responses of plants (Jiang et al., 2017). The SlWKRY81 transcript has been found to reduce drought tolerance in tomato by inhibiting proline biosynthesis (Ahammed et al. 2020) and stomatal closure (Ahammed et al. 2020). Preliminary studies have shown that Si supplementation to the plants increases the expression level of several genes associated with the mitigation of drought stress. Liu et al. (2015) revealed that Si application enhances plant-drought resistance by controlling root hydraulic conductance via up-regulating the transcription of several root aquaporin [SbPIP1;3/1;4(2), SbPIP1;6, SbPIP2;2, and SbPIP2;6] gene expression under drought stress. This upregulation of aquaporin gene expression helps in rapid absorption of water that results in dilution of excess concentration of Na + ions which are otherwise toxic to the plants (Gao et al. 2010). Thus, augmenting expression levels of aquaporin genes by Si-application result in maintaining water status and ion balance helping plants to recover from stress (Manivannan and Ahn 2017). Moreover, Si supply up-regulated the expression level of important polyamine biosynthesis genes (ADC, CAP, ODC1, ODC2, ODC3, SAMDC04, SAMDC06 and SPDS) and down regulated the expression level of the ACC synthesis-related genes (ACS1 and ACS2) in Sorghum under drought stress (Yin et al. 2014). These polyamines contribute to stress mitigation by affecting different physiologic and biochemical functions of plants (Milon et al. 2020). To present day, the Si-induced strategies to decline the metal toxicity in plants are less studied at the molecular levels therefore, a well considerable knowledge of the expression of genes that are associated with Si-facilitated extenuation of metal toxicity, is required to accurately explore the molecular mechanisms.

Structural alterations in plants

Si-mediated improvement in the plants morphologic and anatomic features are beneficial to mitigate the harmful consequences of heavy-metal stress. Application of Si in combination with Cr enhanced shoot and root length, number of tillers and leaf area in comparison to Cr treated alone, to reduce detrimental properties of Cr metal in barley (Ali et al. 2013). Si diminishes the leaf damage, necrosis and damage to root organization and improved the root length under Cu stress in rice (Kim et al. 2014a). Si established endodermis apoplastic barriers which are nearer to the root apex in Cd stressed wheat (Greger et al. 2011). Si condensed the collenchyma transversal area and enhanced xylem diameter, mesophyll and epidermis width to mitigate adverse effects of Cd and Zn metal stress in Zea mays (da Cunha and do Nascimento 2009). In Si-treated wheat plants, xylem and phloem were properly organized and suberization and lignification was well established under Cr stress (Tripathi et al. 2015). These Si triggered structural alterations may reveal the strategy of mitigating heavy-metal toxicity.

Role of silicon in plant biology

Silicon is often regarded as a plant nutritional ‘non-entity’. Suites of factors associated with Si have been recently identified, relating to plant chemistry, physiology, gene regulation and interactions with other organisms. In some high Si-accumulating species, Si could play an important role in plant primary metabolism. The current foundation of knowledge from studies in rice and in non-Si-accumulating species that respond to Si application, including A. thaliana (Markovich et al. 2017) and tomato (Solanum lycopersicum) (Li et al., 2015), provide a starting point for future mechanistic studies. These systems, along with those high Si-accumulators such as rice, barley and wheat, should be employed incrementally across multiple experiments to evaluate the impacts of Si in unstressed situations as well as under single and multiple abiotic and biotic stresses. These should focus, in particular, on those primary metabolic processes revealed in recent research to potentially interact with Si (e.g., oxidation metabolism). As highlighted, Si may interact with primary photosynthetic processes (photorespiration), but this requires clarification as these interactions are likely to differ between C3-, C4- and CAM-type plants due to the differential physiologic and enzymatic carbon-fixation processes employed. The form in which Si is delivered to the plant may also strongly impact its effects on plant metabolism. The delivery mode of Si, in terms of formulation (e.g., calcium silicate, sodium silicate), should be further evaluated with emphasis on optimal translocation and accumulation in planta, as uptake and concentration at the site of action may prove critical to impacts on plant defense and growth. As a parallel priority, it is also important to investigate the role of Si in plant community structure and its ecological impact on mutualists and plant–plant interactions, including allelopathic effects of invasive species. The activity of photorespiration and antioxidative enzymes as well as expression of key photorespiratory genes have been linked to increased abiotic stress tolerance (Rojas et al. 2012). Moreover, evidence suggests that Si-enhanced abiotic stress tolerance is linked to accumulation of photorespiratory enzymes (Nwugo and Huerta 2011). Of course Si not only acts on C3 plants (where photorespiration is a major component of the photosynthetic processes) (Frew et al. 2018), highlighting that if Si-driven photorespiration is a mechanism, it may not necessarily be a comprehensively unifying one. Nevertheless, this suggests Si may impact primary metabolic processes in higher plants, rather than its role being confined solely to plant responses to external stress.

Strategy to facilitate silicon accumulation in plants

Application of Si-rich fertilizers or by improving soil characteristics can improve soil Si availability while genetic selection or improvement can enhance the inherent ability of Si accumulation in plants (Bhat et al. 2019; Fig. 4). Si quantity which is reachable to plants in the soil can be declined by continuous and exhaustive cultivation of Si-accumulator plants (Meena et al. 2021; Meunier et al. 2008). Amount of soil H₄SiO₄ can be enhanced by fertilization and hence, fertilization is recognized as an effective cultivation strategy in those areas where intensive cropping strategies are carried out particularly in soils that have fundamentally low soluble Si content (Tubaña and Heckman 2015; Guntzer et al. 2012). Lower amount of Zn and Cu was found in rice and cucumber when applied with Si-based fertilizer to mitigate the adverse effects caused by heavy metals (Jarosz 2013; Ning et al. 2014). Soil pH, moisture, quantity of clay, nutrient balance, temperature, weathering of soil, redox potential, organic matter are major factors which influence the soil H₄SiO₄ amount. Supplementation of acid-producing fertilizer enhanced the level of H₄SiO₄ in the soil solution, whereas presence of organic matter declines the H₄SiO₄ amount and mobility and reduction in soil pH improves the soil Si availability to plants (Höhn et al. 2008). Lsi1 and Lsi2 genes was advantageous to reveal the method of Si absorption by root and its transport to the plant shoots and also provides a prospect to discover transgenic strategies to improve Si-uptake, particularly in poor accumulator plants (Pandey et al. 2019). Heterologous expression of Si-transporter TaLsi1 exhibited enhancement in the uptake of Si by several folds in Arabidopsis which is a poor accumulator plant (Deshmukh et al. 2013). Research related to the characterization of such genes will benefits to produce superior Si-uptake cultivars via breeding methods.

Fig. 4.

Different approaches for improving Si accumulation to enhance plant tolerance to heavy-metal stress (modified after Bhat et al. 2019)

Conclusion

Natural and anthropogenic actions result in elevated amounts of toxic metals in the soil which lead to harmful consequences on plants growth and yield altogether with human health. In this context, Si is recognized as an efficient strategy to decrease metal uptake, toxic metal accumulation, improve plant growth and biomass, diminish phytotoxicity and also acts as a mechanical and physical barrier in adverse environmental circumstances in plants. It is well recognized that heavy-metal stress induces oxidative stress by generating number of ROS for instance O2^•−, OH^•, 1O₂, H₂O₂ in plants. Application of SI efficiently guards plant tissues from oxidative burst by diminishing the formation of plethora of ROS by activating antioxidative defense system. Usage of Si is a promising strategy to mitigate heavy-metal toxicity therefore, well- designed, large-scale and long-term field studies are essential to assess the Si efficacy for the remediation of metal contaminated soils.

Author contributions

Sadaf Jan: Idea, literature search, drafted and revised the work; Savita Bhardwaj: literature Search, drafted and revised the work; Bhupender Singh: Revision and final draft; Dhriti Kapoor: Revision; Renu Bhardwaj: Revision; Rattandeep Singh: Revision.

Funding

The authors did not receive support from any organization for the submitted work.

Declarations

Conflict of interest

The authors declare that they have no conflicts of interest.