TY - JOUR
AU - Deshmukh,, Rupesh
AB - Abstract Numerous studies have shown the beneficial effects of silicon (Si) for plant growth, particularly under stress conditions, and hence a detailed understanding of the mechanisms of its uptake, subsequent transport, and accumulation in different tissues is important. Here, we provide a thorough review of our current knowledge of how plants benefit from Si supplementation. The molecular mechanisms involved in Si transport are discussed and we highlight gaps in our knowledge, particularly with regards to xylem unloading and transport into heavily silicified cells. Silicification of tissues such as sclerenchyma, fibers, storage tissues, the epidermis, and vascular tissues are described. Silicon deposition in different cell types, tissues, and intercellular spaces that affect morphological and physiological properties associated with enhanced plant resilience under various biotic and abiotic stresses are addressed in detail. Most Si-derived benefits are the result of interference in physiological processes, modulation of stress responses, and biochemical interactions. A better understanding of the versatile roles of Si in plants requires more detailed knowledge of the specific mechanisms involved in its deposition in different tissues, at different developmental stages, and under different environmental conditions. Cell wall stability, phytoliths, silicon transport, specialized cells, stress tolerance, xylem loading Introduction Deposition of silicon (Si) in plant tissues has frequently been associated with stress tolerance mechanisms and better resilience under stress conditions (Epstein, 1994; Ma, 2004; Coskun et al., 2019). Despite numerous reports indicating its beneficial effects, Si has never been considered as an essential element for higher plants. To be categorized as such, an element needs to fulfill specific criteria, the most important of which is that the plant would not be able to complete its life cycle in the absence of the element (Kirkby, 2011). Hence, except for the Equisetaceae and some algae (Pontigo et al., 2015), Si has been categorized separately as a ‘beneficial element’ (Epstein, 1994; Ma et al., 2001). Silicon-based fertilizers are being increasingly used worldwide as a result of the accumulating evidence of the protective effects of Si application, and its promotion as a beneficial element by agencies including the International Plant Nutrition Institute (www.ipni.net/topic/silicon-si). Thousands of published papers have indicated beneficial roles of Si in plants and several review articles have provided summaries of these studies (Ma et al., 2001; Fauteux et al., 2005; Bhat et al., 2019; Coskun et al., 2019; Zargar et al., 2019). However, most research efforts have largely failed to explain the basis of Si-derived benefits to plants. To date, there are no significant reports explaining the distinct roles of Si in plants, and we need a better understanding of its uptake at the root level, subsequent transport, and accumulation in different tissues. The beneficial effects of Si supply have largely been attributed to its deposition in plants (Ma et al., 2001; Sangster et al., 2001; Gong et al., 2006), and considerable variation between species in terms of quantity and deposition patterns have been observed (Guerriero et al., 2019, 2020). High levels of accumulation in some dicots and grasses led to the hypothesis that Si plays a role as a mechanical barrier, but recently Coskun et al. (2019) have proposed a working model termed the ‘apoplastic obstruction hypothesis’ that explains many roles of Si beyond just acting as a mechanical obstruction. However, defining all the observed Si-derived benefits to plants with any single model will be challenging. A simple mechanical role looks most obvious in species that accumulate high levels of Si and in those that have specialized silica cells. In monocots, silica cells are almost filled with solid silica. Mature silica cells are also referred as phytoliths, plant opal, or silica bodies (Kumar et al., 2017, 2020). The shape of silica cells varies among species (Piperno and Pearsall, 1998; Piperno et al., 1999; Dabney et al., 2016). For example, in rice leaves they are found in two different forms, dumbbell-shaped and completely silica-filled bulliform-shaped (Zhang et al., 2013). Mature silica cells impart enhanced abrasiveness to grass leaf blades, which deters herbivores, and they have been found to be associated with photosynthetic activities (Massey et al., 2007; Dabney et al., 2016). Cells filled with Si at the base of wheat awns respond to humidity to provide propulsion that is essential for seed dispersion (Elbaum et al., 2007). Many other specific Si deposition patterns with important roles have been reported for a variety of species (Sangster et al., 2001). Beneficial effects of Si are not only restricted to species capable of high uptake, similar effects have been observed in species with poor accumulation, which appears puzzling. However, recent studies have shown how Si deposition in cell walls can help improve nutrient transport across the membrane (Sheng et al., 2018). Optimum requirements for Si across different species are not yet well defined, and similarly the physiological effects of different amounts of deposition in different tissues are largely unknown. Over the last 15 years, significant progress has been made towards understanding Si uptake in roots and its subsequent transport to different tissues. However, the transporters at the connecting tissues within specific cell types and organs need further study and characterization. This review discusses our current understanding of the roles of Si, the molecular mechanisms involved in its transport, the pattern of its deposition, and the effects of its accumulation in different tissues. In doing so, we highlight gaps in our knowledge that need to be addressed. Phylogenetic variation in silicon uptake and accumulation Wide variation in accumulation of Si has been observed, with concentrations ranging from 0.1% to 10% on a dry-weight basis (Epstein, 1999; Ma and Takahashi, 2002). Bryophyta, Lycopsida, and Equisetopsida within the Pteridophyta showed higher accumulation of Si as compared to most of the angiosperms (Ma and Takahashi, 2002). In angiosperms, species belonging to the Poaceae and Cyperaceae are known to accumulate relatively high amounts of silicon, whilst the Commelinaceae, Urticaceae, and Cucurbitaceae are intermediate in accumulation (Ma and Takahashi, 2002; Hodson et al., 2005). The Brassicaceae and Solanaceae are well documented as being poor accumulators or Si excluders (Hodson et al., 2005; Sonah et al., 2017). Rice (Poaceae) can accumulate up to 10% Si and is considered as a model species to study its biological roles (Ma et al., 2002). Meta-analysis by Hodson et al. (2005) showed the following order for Si concentrations in various groups (high to low): liverworts > horsetails > clubmosses > mosses > angiosperms > gymnosperms > ferns. Early speculation that considered monocots as strong Si accumulators and dicots as poor accumulators were ruled out by studies conducted by Epstein (1999). The variations in Si uptake and accumulation can be attributed to specific transporter proteins in roots. Silicon uptake and transport Silicon is present in the soil as an inert element. Its uptake and transportability mainly depend on the plant roots and its chemical composition in the soil. Silicon is taken up by roots as monosilicic acid [Si(OH)4], which is the soluble form present in soil at pH<9 and concentration below 2 mM Si. After uptake and transportation to the shoots, as a result of transpiration, Si concentrates and polymerizes into colloidal silica gel (SiO2.·nH2O) (Yoshida et al., 1962), although various other biomolecules are also thought to play a role (Harrison, 1996). Plant species are categorized as accumulators, intermediate, or non-accumulators/excluders (Ma et al., 2001). Uptake of silicic acid in rice is much faster than that of water (Ma et al., 2001), indicating the possibility of an active transport mechanism facilitating Si transport across the cell membrane. Apoplastic pathway in rice roots are blocked by the development of Casparian strip and hence translocation of Si needs to be through the symplastic pathway. Tamai and Ma (2003) studied the uptake kinetics of Si and predicted the involvement of transporter proteins in the uptake mechanism, and numerous subsequent studies have helped to further reveal the molecular mechanisms involved in uptake (e.g. Ma et al., 2006, 2011; Markovich et al., 2019). A seminal study by Ma et al. (2006) using an induced mutagenesis approach identified the first Si transporter protein in rice. A mutant genotype lacking Si uptake, named as the lsi1 mutant, was used to identify the transporter gene Lsi1. Lsi1 is a Si influx transporter belonging to the aquaporin subfamily nodulin 26-like intrinsic proteins (NIPs). All aquaporins have a conserved hourglass structure with six alpha helix transmembrane domains (H1–H6) that are joined by five loops (LA–LE). The loops LB and LE contain a conserved motif, the NPA domain. A pore passing through the aquaporin has two constrictions that have a significant role in defining solute specificity and transport kinetics. One of the constriction is formed by two conserved NPA domains and the second constriction is formed by an ar/R selectivity filter consisting of four amino acids, which are from the helices H2 and H5, and loop LE. Lsi1, which transports uncharged silicic acid in particular, belongs to the NIP III group, comprising a unique selectivity filter Gly (G), Ser (S), Gly (G), and Arg (R) (Mitani-Ueno et al., 2011). Shortly after the discovery of Lsi1, a second Si transporter gene, Lsi2, was identified by the same group using the same mutagenesis approach (Ma et al., 2007). Lsi2 is an efflux transporter that actively pumps Si out of the cell with the help of a proton gradient. As an active transporter, its homology and mechanism are completely different from Lsi1. Lsi2 is an anion transporter coupled with a proton antiport having 9–12 transmembrane domains (Ma et al., 2007, 2011). The identification of the Lsi1 and Lsi2 transporters has largely explained the molecular mechanism involved in the uptake of Si by roots. Rice takes up Si as monosilicic acid through Lsi1 present on the distal side of the exodermis and pumps it in a de-protonated form out in aerenchyma by Lsi2 at the proximal side of the cell (Fig. 1a). Silicic acid then passes through the apoplast of aerenchyma. In the endodermis, the apoplastic pathway is blocked by the Casparian strip, which forces Si to be transported via the symplastic pathway through Lsi1 and then Lsi2 to the xylem. The silicic acid moves upwards to the shoot via the transpiration stream, where Lsi6 (an influx transporter, homolog of Lsi1) unloads Si from the xylem and facilitates its transport to the different aerial parts of the plant. Fig. 1. Open in new tabDownload slide Schematic representation of silicon transport and xylem loading. (a) Silicon (Si) transport through roots. Lsi1, which is a passive transporter, facilitates the entry of Si (as silicic acid) into the exodermis. Silicic acid exits the exodermis and enters the cortex through the active transporter Lsi2, and it then moves apoplastically through aerenchyma to reach the endodermis. Lsi1 and Lsi2 transport silicic acid through the endodermis and it is loaded into the xylem. (b) The transport of Si in node I. Lsi6, a polar transporter, transfers the silicic acid into the xylem transfer cells, from where it moves through the plasmodesmata to the bundle sheath cells. Lsi2 located at the distal ends of these cells transports some of the silicic acid into the apoplast, from where it moves into the xylem of diffused vascular bundles, whilst the rest of the Si is exported and loaded into the xylem by Lsi3. EVB, enlarged vascular bundle; BS, bundle sheath; XTC, xylem transfer cells; NVA, nodal vascular anastomosis; DVB, diffuse vascular bundle. (c) Xylem unloading into silica cells in leaves. Silicon is pumped into the xylem parenchyma cells by the Lsi6 transporter and is transported through them to be deposited into the silica cells. The transporter involved in transferring Si against a concentration gradient into the silica cells remains unknown. Fig. 1. Open in new tabDownload slide Schematic representation of silicon transport and xylem loading. (a) Silicon (Si) transport through roots. Lsi1, which is a passive transporter, facilitates the entry of Si (as silicic acid) into the exodermis. Silicic acid exits the exodermis and enters the cortex through the active transporter Lsi2, and it then moves apoplastically through aerenchyma to reach the endodermis. Lsi1 and Lsi2 transport silicic acid through the endodermis and it is loaded into the xylem. (b) The transport of Si in node I. Lsi6, a polar transporter, transfers the silicic acid into the xylem transfer cells, from where it moves through the plasmodesmata to the bundle sheath cells. Lsi2 located at the distal ends of these cells transports some of the silicic acid into the apoplast, from where it moves into the xylem of diffused vascular bundles, whilst the rest of the Si is exported and loaded into the xylem by Lsi3. EVB, enlarged vascular bundle; BS, bundle sheath; XTC, xylem transfer cells; NVA, nodal vascular anastomosis; DVB, diffuse vascular bundle. (c) Xylem unloading into silica cells in leaves. Silicon is pumped into the xylem parenchyma cells by the Lsi6 transporter and is transported through them to be deposited into the silica cells. The transporter involved in transferring Si against a concentration gradient into the silica cells remains unknown. The molecular mechanism of Si uptake varies amongst species. Homologs of both Lsi1 and Lsi2 have been identified in monocot crops such as wheat, barley, sorghum, and maize, with variations in their localization (Mitani et al., 2009). In maize, Si deposition is mediated by two genes, ZmLsi1 and ZmLsi6. ZmLsi1 is responsible for the uptake of Si through roots, whilst ZmLsi6 is located in the parenchyma cells of the leaves and is responsible for xylem unloading (Bokor et al., 2015). Homologs of OsLsi2 responsible for efflux have been found in barley (HvLsi2) and maize (ZmLsi2) and functions in a similar manner, but they are present only in the endodermis and do not show polar localization (Mitani et al., 2009). Another Si efflux transporter, Lsi3, which is a homolog of Lsi2, has been identified in rice. An explanation for the high accumulation of Si in rice leaves and inflorescences was provided by Yamaji et al. (2015), who found localization of Lsi2, Lsi3, and Lsi6 at the nodes of the stem and demonstrated the involvement of these three transporters in intervascular Si transport (Fig. 1b). Such transport is needed for preferential distribution. Although the identification of Lsi1, Lsi2, Lsi3, and Lsi6 has defined the path of Si uptake at the root level and its subsequent transport to the aerial tissues, the transporter involved in Si loading in the xylem is not yet known (Fig. 1c). Similarly, the transporters for silica cells, in which very high amounts of Si accumulate, are not known. These represent large gaps in our knowledge that need to be filled to have a full understanding of the transport and deposition of Si in different plant tissues. Silicon deposition in different parts of the plant The accumulation and deposition of Si in plants have been extensively studied. Sites of silicification include the cell wall, wholly or partially filled cell lumens, the intercellular spaces of the roots and shoots, and in specialized silica cells. Silicification mainly occurs in sclerenchyma, fibers, storage tissues, epidermis, and vascular tissues. The pattern of Si deposition, the amount, and its role drastically vary among tissue types. Silicon deposition in the roots Silicon is known to be present in the roots of several members of the Poaceae, with the endodermis being most common site of silicification. The endodermal deposition of Si in rice roots was first reported by Parry and Soni (1972), and it is found to be localized as a ring in endodermal cell walls with no differences in the proximal and distal parts of tissue (Moore et al., 2011). The heaviest deposition is found in the inner tangential wall (ITW) and sometimes in the endodermis radial walls (Fig. 2). Silicon deposition is also found in the ITW of endodermis in the proximal end of the seminal root in barley, oats, and wheat (Bennett, 1982). In sorghum, two distinct types of silica deposition were found (Sangster and Parry (1976). One is similar to rice in that it is associated with the ITW of the endodermis. The other type, a phytolith (Metcalfe, 1960), is a discrete dome-shaped structure, normally attached to the ITW and protruding into the cell lumen. Silica deposition in sorghum starts simultaneously with the secondary wall formation of the endodermal cell, and these silica aggregates penetrate deep into the secondary walls (Sangster and Parry, 1976). Hodson (1986) examined adventitious roots of Phalaris canariensis and found that whilst silica was deposited in both the ITW and radial walls of the endodermis in underground roots, it was absent in the endodermis of adventitious aerial roots. Silica deposition is observed in intracellular spaces just outside the outer tangential wall of the root endodermis of Molinea ceruleae (Montgomery and Parry, 1979). In date palm (Phoenix dactylifera), Si deposition occurs in specialized cells known as stegmata cells, which are arranged in rows surrounding the sclerenchyma bundles in the roots (Bokor et al., 2019) (Fig. 3). As roots age, deposition can also occur in other parts such as the stele, sclerenchyma, and conductive tissues (Parry and Kelso, 1975). No expression of Lsi1 and Lsi2 is observed in the root hairs of rice, implying that the hairs have no role in Si uptake (Ma et al., 2006). Fig. 2. Open in new tabDownload slide Schematic representation of silicon deposition on the inner tangential wall of the root endodermis. Fig. 2. Open in new tabDownload slide Schematic representation of silicon deposition on the inner tangential wall of the root endodermis. Fig. 3. Open in new tabDownload slide Scanning electron microscopy–energy-dispersive X-ray imaging for silicon in Phoenix dactylifera root tissues. (A) Cross-section of adventitious root. The white arrowheads indicate deposition of silicon (Si) in stegmata cells (specialized cells in palm species) and the red arrowhead indicates the position of a fiber band. (B) Silicon deposition (violet colour) in multiple phytoliths in a cross-section of an adventitious root. (C) Longitudinal section through a fiber band of an adventitious root. The white arrowheads indicate Si deposition in disrupted stegmata cells and the red arrowhead indicates a fiber. (D) Silicon deposition (violet) in a longitudinal section of an adventitious root. The figure is reproduced from Bokor et al. (2019). Fig. 3. Open in new tabDownload slide Scanning electron microscopy–energy-dispersive X-ray imaging for silicon in Phoenix dactylifera root tissues. (A) Cross-section of adventitious root. The white arrowheads indicate deposition of silicon (Si) in stegmata cells (specialized cells in palm species) and the red arrowhead indicates the position of a fiber band. (B) Silicon deposition (violet colour) in multiple phytoliths in a cross-section of an adventitious root. (C) Longitudinal section through a fiber band of an adventitious root. The white arrowheads indicate Si deposition in disrupted stegmata cells and the red arrowhead indicates a fiber. (D) Silicon deposition (violet) in a longitudinal section of an adventitious root. The figure is reproduced from Bokor et al. (2019). Silicon loading into the xylem and unloading at aerial tissues The silicon content is generally higher in transpirational organs such as leaves and lower in absorptive organs such as roots, indicating that deposition is influenced by upward flow of the evapotranspiration stream. Following primary uptake in the roots, Si is transported to the shoots via the xylem. Uptake in the roots involves at least two major processes. First, Si from external solutions is transferred via transporters and passive diffusion into the cortical cells, and, second, it is released into the transpiration stream via xylem loading. Silicon accumulation in the aerial parts of the plant mainly depends on these two processes. Interestingly, rapid release of Si into the xylem is observed against a concentration gradient. In rice, Mitani et al. (2005) found that the concentration in the xylem sap reached 6.0 mM within 30 mins of exposure to only 0.5 mM Si in the growth medium (Fig. 4). Furthermore, the concentration increased to 18 mM in the next 8.5 h, indicating that xylem loading is a rapid process that is accomplished against a concentration gradient. However, the rate of xylem loading varies in plants and also depends on Si uptake and xylem loading processes (Mitani et al., 2005). In the aerial tissues, Si is unloaded from the xylem and transported to peripheral tissues in the leaves and inflorescences. In hemp (Cannabis sativa), Si is observed in various tissues, but in the bast fiber cells deposition occurs explicitly at the distal end of the cell wall (Guerriero et al., 2019). These Si-impregnated walls are thought to strengthen the plant and provide resistance to lodging (Fig. 5). Fig. 4. Open in new tabDownload slide Schematic representation of uptake, transport, and deposition of silicon. Plants take up silicon as orthosilicic acid from the soil where the concentration ranges between 0.2–0.6 mM. On uptake, orthosilicic acid is transported from the roots to the xylem, where its level transiently reaches up to 6–18 mM. The orthosilicic acid moves from the xylem to leaves where it undergoes auto-polymerization and is deposited as silica. Fig. 4. Open in new tabDownload slide Schematic representation of uptake, transport, and deposition of silicon. Plants take up silicon as orthosilicic acid from the soil where the concentration ranges between 0.2–0.6 mM. On uptake, orthosilicic acid is transported from the roots to the xylem, where its level transiently reaches up to 6–18 mM. The orthosilicic acid moves from the xylem to leaves where it undergoes auto-polymerization and is deposited as silica. Fig. 5. Open in new tabDownload slide High-resolution secondary ion mass spectrometry (Nano-SIMS) analysis of xylem cells and bast fibers of hemp plants with or without silicon (Si) treatment. The arrowheads in the treated samples indicate the deposition of Si at the distal end of the fibers. Increasing intensity of deposition is indicated by colour scale, which ranges from black to red. Reprinted from Guerriero et al. (2019) with permission from Elsevier. Fig. 5. Open in new tabDownload slide High-resolution secondary ion mass spectrometry (Nano-SIMS) analysis of xylem cells and bast fibers of hemp plants with or without silicon (Si) treatment. The arrowheads in the treated samples indicate the deposition of Si at the distal end of the fibers. Increasing intensity of deposition is indicated by colour scale, which ranges from black to red. Reprinted from Guerriero et al. (2019) with permission from Elsevier. Silicon deposition in leaves The leaves are the major site of Si deposition among the shoot tissues. In the rice leaf blade, deposition results in the formation of a 2.5-μm thick double layer of Si beneath the cuticle (Yoshida et al., 1962c; Ma and Yamaji, 2006). The formation of this layer is believed to occur by an active process in which Si particles are attracted by the ionic forces of the membrane surface. The layer continues to thicken by deposition of monomeric silicic acid from a supersaturated solution, which is the result of active metabolic processes rather than being caused by evaporation (Kaufman et al., 1981; Sangster et al., 2001). Silicification occurs in almost all the cells of the leaf blade and more than 90% of the total Si in the leaf is deposited in the epidermis, as a result of the transpirational stream (Yoshida et al., 1962b). Silicon is deposited in the epidermal cell walls, middle lamella, and intercellular spaces of the subepidermal tissues of rice (Kim et al., 2002). Variations in Si content occur in different leaves of the same plant, as well as at different positions within a leaf. The older leaves have more deposition and it gradually decreases from the apex to the base of the leaves (Sangster, 1970). In young leaves, Si is only detected in specialized silica cells and in bulliform or ‘motor cells’ whereas in senescing leaves it is present in virtually all cell types (Sangster et al., 2001), thus showing that Si deposition increases as the plant ages. Deposition differs between the adaxial and abaxial surfaces of the leaves. In bread grass (Brachiaria brizantha) Si accumulates mainly in the upper epidermis (de Melo et al., 2010), whilst in other species deposition is observed in both the adaxial and abaxial surfaces. For example, bamboo has accumulation in cork cells, bulliform cells, silica cells, long cells, and guard cells on both sides of the leaf (Motomura et al., 2002). In Pleioblastus chino the densest deposition is in the epidermis and the least dense is in the mesophyll and vascular bundles (Motomura et al., 2006). Deposition in silica cells Understanding the deposition of Si in the silica cells, as well as the evolution of such specialized cells, is of great importance in revealing its role in plants. Prat (1948) divided the epidermal silica-depositing cells of grasses into three subgroups, namely differentiated elements, fundamental elements, and bulliform elements. Differentiated elements include silica cells and exodermic components, for example micro- and macrohairs, trichomes, cork cells, and stomata. Fundamental elements include epidermal cells that are greatly elongated. Bulliform cells are present between the vascular bundles and on the adaxial surfaces of the leaf blade. In grasses, cell division in leaf epidermal tissues is restricted to the base of the growing leaf. The newly formed cells elongate and in doing so push the older cells upwards and out of the leaf sheath (Skinner and Nelson, 1995). In rice, silica cells are usually present in pairs that are tandemly repeated and run parallel to each other (Kaufman et al., 1985). Silica cells and cork cells located close by are thought to originate from a single mother cell in Avena (Kaufmian et al., 1969). After disintegration of the protoplasm, the lumens of the silica cells become filled with Si, eventually becoming a mass of solid, hydrated, amorphous silica that results in cell death (Kumar et al., 2017). Suberized cork cells, which remain unsilicified, may be involved in the metabolism of silica cells. The two are connected to each other and to neighboring cells by plasmodesmata (Lawton, 1980). Silica cells are the first cells that undergo silicification in the tissue, even before the tissue is exposed to the outer atmosphere (Kaufmian et al., 1969; Ma and Takahashi, 2002). Deposition in silica cells only occurs during leaf development (Sangster, 1970), and initially transpiration was thought to be responsible for silicification. However, Kumar et al. (2017) demonstrated that while transpiration is required to pull Si up and into the leaves, silicification in silica cells is an active process and does not depend upon evapotranspiration of water. The mechanism of silicification in silica cells involves the presence of specific material in the apoplast that enhances Si deposition. This material may include proteins, peptides, or sugars that are capable of polymerizing soluble silicic acid to solid silica. Polymerization and deposition of silicic acid at the cell wall possibly creates a concentration gradient within the leaf, thereby drawing silicic acid towards the silica cell (Gallagher et al., 2015). Silicon deposition in trichomes Deposition of Si is also found in the cells surrounding the base of trichome hairs and in the trichomes themselves. Abe (2019) studied deposition in the trichomes of six different species of Cucurbitaceae, namely cucumber, pumpkin, melon, watermelon, sponge gourd, and bottle gourd. They found that in watermelon leaves, Si is located in both the trichomes and the cells surrounding their bases, whilst in cucumber, pumpkin, and melon Si is deposited only in the cells at the bases and calcium is present in the hairs themselves. This combined deposition of calcium and Si gives rigidity to the trichomes, which in turn makes the plants more rigid. In contrast, SEM–energy-dispersive X-ray imaging of wheat has shown high levels of Si accumulation in trichomes but no differences in calcium compared with the surrounding cells (Fig. 6). An earlier study by Samuels et al. (1991) also reported deposition of Si in the bases of the trichomes and they concluded that these base cells differ from surrounding cells. Their results suggested that cells at the base of the trichomes transform in a way that supports the polymerization of Si. Silicon accumulated in trichomes is found to efficiently propagate far-infrared light inside the trichomes and leaves, which can be helpful in warming the tissues (Takeda et al., 2013). However, the precise roles of Si-filled trichomes are not well understood. Similarly, the transporters involved in the accumulation of Si in trichomes have not yet been identified. Fig. 6. Open in new tabDownload slide Energy-dispersive X-ray (EDX) assisted SEM images of the adaxial surface of leaves from 1-month-old wheat plants grown in soil with silicon supplementation. (A) Image showing bulliform cells. (B) Silicon (Si) deposition in bulliform cells, indicated by the white arrowheads. Si detected with EDX-SEM is highlighted by the red colour (C) Image showing calcium deposition in the leaf; however, no deposition was observed together with silicon. Calcium detected with EDX-SEM is highlighted by the orange colour. (D) EDX results showing the relative concentrations of various elements in the leaves. (E) Trichomes on the adaxial surface of the leaf (F) Deposition of Si in the trichomes, indicated by the white arrowheads. (G) Calcium deposition in the trichomes; no deposition was observed together with silicon. H) EDX results showing the relative concentrations of various elements in the trichomes. Fig. 6. Open in new tabDownload slide Energy-dispersive X-ray (EDX) assisted SEM images of the adaxial surface of leaves from 1-month-old wheat plants grown in soil with silicon supplementation. (A) Image showing bulliform cells. (B) Silicon (Si) deposition in bulliform cells, indicated by the white arrowheads. Si detected with EDX-SEM is highlighted by the red colour (C) Image showing calcium deposition in the leaf; however, no deposition was observed together with silicon. Calcium detected with EDX-SEM is highlighted by the orange colour. (D) EDX results showing the relative concentrations of various elements in the leaves. (E) Trichomes on the adaxial surface of the leaf (F) Deposition of Si in the trichomes, indicated by the white arrowheads. (G) Calcium deposition in the trichomes; no deposition was observed together with silicon. H) EDX results showing the relative concentrations of various elements in the trichomes. Silicon deposition that affects physiological plasticity under stress conditions Biotic stress Pathogens need to overcome the physical and chemical barriers presented by plant cells for successful infection (Ferreira et al., 2006), and Si is known to enhance these barriers, thereby helping to mitigate the biotic stress (Epstein, 1999). Onodera (1917) was the first to correlate Si content in rice with resistance to bacterial blight, caused by Pyriculria oryza. This triggered further such studies, most of which revolved around the development of puncture resistance due to Si deposition. Yoshida et al. (1962c) demonstrated the deposition of a layer of Si under the leaf cuticle, on which basis the hypothesis of Si forming a mechanical barrier was proposed. Plant pathogens secrete molecules known as effectors, which help them in colonization (Snelders et al., 2018). According to the apoplast obstruction hypothesis proposed by Coskun et al. (2019), Si deposition interferes with the host–pathogen specificity by forming barriers that prevent the movement of effectors within the plant. Silicon is thought to function in biotic stress resistance in two ways, first by forming mechanical barriers and second by acting as a modulator for host responses (Ma and Yamaji, 2006). Using a hydroponic nutrient solution, it has been shown that cucumber (Cucumis sativus) plants grown in a Si-containing medium have increased leaf rigidity, roughness, and dry weight, and enhanced resistance to downy mildew fungus (Adatia and Besford, 1986). Amending soil with Si fertilizers results in increased content in rice tissues, which in turn increases resistance to infection by brown spot and blast (Magnaporthe grisea) (Datnoff et al., 1992). Microscopic examination of the adaxial leaf surface indicates that increased Si content reduces appressorial penetration of the rice blast fungus into the epidermis (Hayasaka et al. 2008). Fungal infection is also prevented by Si-mediated formation of papillae and deposition of callose in wheat (Bélanger et al., 2003). Similarly, rose plants showed Si-induced resistance against powdery mildew due to the formation of papillae and fluorescent epidermal cells, which are interpreted as an indication of the hypersensitive response (Shetty et al., 2012). Deposition of callose and accumulation of H2O2 was also observed at the sites of infection. Leaf sheaths of rice plants supplied with Si show higher puncture resistance compared to plants without supplementation; for example, Si deposition in the sheaths results in increased resistance to infection by Rhizoctonia solani (Schurt et al., 2012). Silicon strengthens the cell wall by associating with the lignin component, and this strengthening helps in blast disease resistance in rice (Kim et al., 2002). A pioneer study by Chérif et al. (1992) demonstrated that Si leads to increased fungal resistance in cucumber as the result of deposition of phenolic material in the infected tissues and in primary and secondary cell walls, which damages the fungal hyphae. This study helped to reveal the role of Si other than as a purely mechanical barrier. Similarly, Si-induced deposition of a dense, amorphous material in rice leaves has been found to be associated with enhanced resistance against blast infection that can be attributed to both physical and cytochemical factors (Rodrigues et al., 2003). Cucumber plants grown with Si supplementation show antifungal activity against Pythium infection in the roots as a result of stimulation of chitinase activity followed by activation of peroxidases, polyphenol oxidases, and glycosidically bound phenolics (Chérif et al., 1994). Accumulation of phytoalexins induced by Si has been found to be responsible for increased resistance to powdery mildew in cucumber (Fawe et al., 1998). Wheat plants supplemented with Si show increased defence against Blumeria graminis f. sp. tritici as the result of releasing glycosylated phenolics, which affect the haustoria (Bélanger et al., 2003). Studies such as these changed the idea that resistance developed by Si is merely the result of formation of physical barriers. Another example is the restriction of blast infection in susceptible rice cultivars by Si supplementation, which results in increased accumulation of glucanase, peroxidase, and pathogenesis-related protein 1 (PR-1; Rodrigues et al., 2005). Sun et al. (2010) also found that Si induces host resistance mechanisms to blast in rice by enhancing the activities of catalase and peroxidase, and it also leads to lipid degradation and accumulation of H2O2. Rose plants supplemented with Si show resistance to powdery mildew as a result of a several-fold increase in content of the antifungal phenolic compounds chlorogenic acid and rutin (Shetty et al., 2011). Thus, Si plays an active role in mounting resistance against biotic stresses in plants. The role of Si in biotic stress has been further confirmed by studies of the rice mutant lsi1, which shows lower accumulation of Si in leaves compared to the wild-type. When inoculated with blast fungus, symptoms rapidly become apparent in the mutant, whereas the wild-type shows resistance (Ueno et al., 2007), which clearly suggests that the inability to take up Si is responsible for the susceptibility to the disease. Silicon accumulated in epidermal cells acts as a mechanical barrier that protects plants from herbivores, either directly or passively. Silicon treatment in sugarcane hardens the external rind and reduces penetration and stalk damage caused by larvae of the borer insect Eldana saccharina (Kvedaras and Keeping, 2007). The reduced ability to penetrate the stalk increases larval mortality as they are exposed to harsh environmental conditions for longer. Silicon is known to enhance physiological and biochemical processes in plants and as a consequence increase physiological resistance to herbivores. Despite being considered as a non-accumulator, even small amount of Si deposition in leaves of collard (Brassica oleracea) hardens them, thereby affecting the nutrition and performance of larvae of Plutella xylostella (Teixeira et al., 2017). The presence of Si at relatively high levels in various grass species impedes herbivory by Schistocerca gregaria and Spodoptera exempta (Massey et al., 2006), although no effect is seen on the phloem-feeding Sitobion avenae. Silicon supplementation in rice increases its concentration in the stem and this enhances resistance to the brown planthopper by reducing successful probing and phloem-sap ingestion, with the result that the pest shows reduced preference for settling on the plants (Yang et al., 2017). Mechanical barriers formed by Si in rice also help to resist the leaf folder Cnaphalocrocis medinalis, which is known to cause heavy damage (Han et al., 2015). Relatively high concentrations of Si in grasses cause wear of the mandibles within the first instar of S. exempta, resulting in reduced growth and nitrogen absorption by the larvae (Massey and Hartley, 2009). Similarly, increased Si concentration in Bromus catharticus increases the frequency of phytoliths, thereby helping resistance to the grasshopper Oxya grandis as a result of mandible wear (Mir et al., 2019). Abiotic stress Drought stress Silicon enhances tolerance to various abiotic stresses including drought, salinity, heavy metal toxicity, chilling, freezing, high-temperatures, high radiation, and waterlogging (Ma, 2004; Liang et al., 2015). Despite an abundance of information about the role of Si in alleviating abiotic stress, knowledge of its specific mechanisms of action is lacking. The deposition of a layer of Si below the cuticle reduces transpiration during water deficit and thus provides tolerance against drought stress (Ma et al., 2001). Drought conditions intensify the production of reactive oxygen species (ROS), which have deleterious effects on physiological and biochemical processes in plants (Cruz de Carvalho, 2008). Silicon enhances the activities of the ROS-scavenging enzymes catalase, superoxide dismutase, and glutathione reductase in wheat under drought stress whilst the oxidative stress is decreased (Gong et al., 2005). Silicon also aids in osmotic adjustment by enhancing the accumulation of proline and glycine betaine during drought conditions (Ahmad and Haddad, 2011), and it prevents membrane damage in sunflower by increasing the relative water content (Gunes et al., 2008). Silicon helps to maintain photosynthetic rates in cucumber under drought by reducing stomatal conductance, improving the water holding capacity, stabilizing the transpiration rate, and reducing chlorophyll decomposition (Ma et al., 2004). Silicon improves water uptake and hydraulic conductance during drought stress in sorghum (Sonobe et al., 2009). Silicon deposition in the leaves of Poa pratensis aids in maintaining them in an erect position, which improves photosynthesis through increased light penetration in the canopy and reduced transpiration (Saud et al., 2014), a change in morphology that can be important in alleviating drought stress. It has been demonstrated that sorghum plants treated with Si show enhanced accumulation of polyamines together with a decline in content of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid, which results in delayed leaf senescence and an increase in the root to shoot ratio (Yin et al., 2014). Thus, Si enhances drought tolerance in plants by modulating a number of different physiological processes. Salinity stress Deposition of Si in the root endodermis and exodermis hampers apoplastic flow during salinity stress and reduces the uptake of sodium ions (Na+), thereby helping to avoid their deleterious effects (Yeo et al., 1999; Gong et al., 2006). Silicon supply also enhances the formation of the Casparian strip during salinity stress (Fleck et al., 2015), and the resulting blocking of apoplastic flow may be important in imparting tolerance. Treatment with Si during salinity stress improves dry matter production and chlorophyll content in wheat (Tuna et al., 2008), whilst in maize it enhances the sequestration of Na+ into leaf vacuoles, thereby preventing its excessive accumulation in the chloroplasts (Bosnic et al., 2018). Similar to drought stress, Si nutrition has been found to increase the activity of antioxidant enzymes such as catalase, ascorbate peroxidase, and guaiacol peroxidase during salinity stress in a cucumber cultivar displaying salinity tolerance (Khoshgoftarmanesh et al., 2014). Silicon supplementation confers salinity tolerance in mung bean plants by enhancing the accumulation of K+ and Ca+ ions, and the osmoprotectants proline and glycine betaine (Ahmad et al., 2019), whilst in pepper it increases the expression of adenylosuccinate synthase and E3 ubiquitin ligase, which aid in biomass accumulation, floral development, and senescence (Manivannan et al., 2016). Expression of Rubisco and oxygen-evolving enhancer proteins are also increased. Heavy metal stress Williams and Vlamis (1957) found that Si alleviates manganese toxicity in barley by causing it to be evenly distributed across the leaves, rather than accumulating to toxic levels in localized zones. In cucumber subjected to excess copper, Si supply increases both its deposition in the cell walls in the roots and its chelation by plastocyanin and acconitate in the leaves, thus helping to maintain cytosolic copper concentrations at relatively low levels (Bosnic et al., 2019). Silicon treatment decreases the transport of cadmium from roots to shoot in wheat, and decreases its uptake into leaf protoplasts (Greger et al., 2016). Heavy metal uptake in rice is also hampered by the blockage of the apoplastic pathway by substantial deposition of Si in the endodermal region, thus resulting in a reduction in their translocation (Shi et al., 2005). Silicon-mediated enhancement of the Casparian strip and suberin lamellae may also further reduce uptake of toxic heavy metals in plants. Silicon can also function to reduce the uptake of heavy metals from the soil. Heavy metal uptake is favoured by low pH and hence it can be reduced by increasing the pH (Bolan et al., 2003), which can be achieved by addition of Si, leading to immobilization of the metals (Bhat et al., 2019). Silicon also reduces the phytoavailibity of heavy metals by forming silicate complexes with them, resulting in changes in speciation and conversions from toxic to non-toxic forms (Emamverdian et al., 2018). Flavanoid-phenolics and organic acid chelation of heavy metals are other Si-induced heavy metal stress mitigation mechanisms. Secretion of an organic acid with chelating ability aids in detoxifying aluminum in higher plants (Ma, 2000). Silicon treatment enhances exudation of aluminum-chelating phenols from the root tips in an aluminum-tolerant maize variety (Kidd et al., 2001). Accumulation of heavy metals in plants triggers ROS production, which induces oxidative stress (Jalmi et al., 2018), and Si supply enhances the activities of antioxidant enzymes such as superoxide dismutase, catalase, and ascorbate peroxidase whilst reducing levels of malondialdehyde and H2O2 in rice and Brassica chinensis when they are stressed with zinc and cadmium, respectively (Song et al., 2009, 2011). Application of Si and nitric oxide to wheat decreases cadmium accumulation and reduces toxicity by up-regulation of the antioxidant defence system (Singh et al., 2020). Morphology, composition, and distribution of phytoliths The term phytolith was introduced by Ruprecht (1866) and is mainly used to indicate siliceous deposits. Many other terms are also used, including opaline silica, biogenic silica, and plant opal, and they essentially distinguish plant-derived silica from inorganic silica. Silica deposition occurs in different types of plant cells including silicified cells, micro-hairs, macro-hairs, long cells, and short cells. Phytoliths derived from different cells differ morphologically. The morphology of silica mainly depends on two factors, namely the type of cell in which it is formed and its precise location within the plant tissue; however, there are exceptions where the shape of the phytolith is not in accordance with the cell type. Phytoliths may be regularly shaped (i.e. spherical, globular, cylindrical, hexagonal, and cubical) or irregularly shaped (i.e. dumbbell, saddle, bowl, boat-shaped, bulliform, and polylobate). Phytoliths remain in the environment after plant death and the decay of organic matter, and their accumulation and persistence as microfossils can assist in archaeological studies that examine the agricultural origins of crop plants around the world (Ball et al., 2016). Morphological characterization is the only approach that can be efficiently used for such studies, as phytoliths exist as a distinct entity rather than as a fragment of any plant tissue. Phytoliths are not always exclusively composed of Si, and the chemical composition varies according to species, climatic conditions, pH, temperature, and soil composition (Kameník et al., 2013; Nawaz et al., 2019). The cellular environment in which development of the phytolith takes place may also have a profound effect on its composition; for example, phytoliths from the carbohydrate matrix in the cell wall differ from phytoliths deposited in the cell lumen in terms of their organic content (Hodson, 2016). The elemental composition of phytoliths can also be affected by the presence of pollutants in the soil, such as those caused by the mining industry (Buján, 2013). The elemental composition of phytoliths can vary between species grown in the same soil and environment (Hart, 2001). A survey by Carnelli et al. (2002) suggested that aluminum deposition in phytoliths was specific to woody species, but Hodson and Sangster (2002) determined that this might not be the case and instead it could be dependent on the pH of the substrate. The composition of phytoliths is also known to vary from organ to organ within the same plant (Hodson et al., 2008). Phytoliths are formed in almost all parts of plants, including the roots, shoots, stems, and leaves, and a single species can produce different types of phytoliths (Golokhvast et al., 2014). Hence, phytoliths can be a tool to identify plant species and to place them within the taxonomic hierarchy (Metcalfe, 1960). Epidermal phytoliths are mainly utilized for identification of grasses at the subfamily and tribe levels. Some types are common in all tribe members of a family, but some short-cell phytoliths are mainly specific for a particular tribe and can be used as indicators of individual subfamilies, tribes, and genera (Piperno and Pearsall, 1998). Different subfamilies of Poaceae have been characterized on the basis of the type of phytoliths present. For example, bilobate and saddle-shaped phytoliths are a characteristic feature for the Panicoideae and Chloridoideae subfamilies, respectively (Shakoor and Bhat, 2014). Maize contains phytoliths of both the festucoid and panicoid type and they have anatomical and morphological characters that are similar to the Andropogoneae and Panacea, so accordingly the species was placed in the subfamily Panicoideae (Prat, 1948). The evolutionary path of the specific chemical composition of phytoliths and its relevance to Si-derived benefits to plants are not yet understood. Biogeocycling of phytoliths Transport and recycling of Si within earth systems forms a biogeochemical cycle that is also known as the silica cycle. Bartoli (1983) was first to suggest a role for phytoliths in the biogeochemical cycle of Si. Preliminary studies suggested that the amount of soluble silica in water and soil is chiefly controlled by the dissolution of quartz (Rimstidt, 1997). Alexandre et al. (1997) studied the silica cycle in rainforests and found that phytoliths restore the silica in soil and are responsible for the soil silica dynamics. Meunier et al. (2001) also highlighted the importance of phytoliths as a Si reservoir in soil. Meunier et al. (2001) confirmed the importance of phytoliths in the silica cycle with the finding that a 15-cm deep layer of biogenic silica was formed by forest fires in bamboo stands. It has been observed that phytoliths are major contributors to soluble silica as compared to the organic matrix during plant decomposition (Fraysse et al., 2006). Polymerization of silicon Monosilicic acid is known to undergo polymerization once its concentration exceeds 2 mM (Ma and Yamaji, 2006). Its concentration in soil is much lower than this, and hence polymerization is restricted to within plants. In wheat and rice, the concentration of Si in the xylem sap can reach up to 8 mM and 6 mM, respectively. Although monosilicic acid is the major form, this excess concentration is transient and it is rapidly transported to the leaf tissue, where polymerization takes place (Casey et al., 2004; Mitani et al., 2005). Silicon polymerization consists of the condensation of [Si(OH)4] to Si-O-Si, which takes place in three steps: nuclei formation by monomer polymerization, growth of polymer particles, and formation of branched-chains by linkage of the particles, which leads to formation of a gel (Iler, 1979). Polymerization of silicon takes place by oxolation involving an SN2 nucleophilic substitution, with the rate increasing with increasing pH. The oxidation process proceeds with the concentrating of silanol units and H2O being released. Inanaga and Okasaka (1995) demonstrated that cell wall extracts from rice shoots contain Si-binding compounds. Cellulose assists in the formation of ordered octahedral Si aggregates, with unordered aggregates being formed in its absence (Perry and Lu, 1992). Protein-containing biomolecules are known to aid polymerization of monosilicic acid and have been studied in protein extracts from plants that accumulate silicon such as Phalaris, Equisetum, and Phragmites (Harrison, 1996; Perry and Keeling-Tucker, 2003). These extracts are found to be rich in proline, aspartic acid, and glutamic acid. Belton et al. (2004) studied the effects of 11 amino acids and glycine and lysine homopeptides on silicification, and found interactions between negatively charged Si and amino acids with positively charged side-chains. Increase in the length of the L-lysine homopeptide increased monomer formation and aggregation of Si. Coradin and Livage (2001) demonstrated that peptides and the amino acids serine, proline, lysine, and aspartic acid interact with silicate and aid in its polymerization to polysilicates, with the effects of the peptides being the more prominent. Differences in amino acid properties such as the isoelectric point and hydrophobicity affect the surface area of the polymers (Belton et al., 2004). In cucumber, proline-rich protein 1 (PRP1), a systemic acquired resistance protein with high numbers of lysine and arginine residues at the C-terminal end, is known to function in the polymerization of monosilicic acid at the site of fungal infection (Kauss et al., 2003), and the polymerization activity of PRP1 is attributable to its high density of positive charges. Kumar et al. (2020) identified the siliplant1 (Slp1) protein in sorghum, which has seven repeat units rich in proline, lysine, and glutamic acid, and functions to precipitate in silica cells. Slp1 interacts with silica by binding through the lysine amino group. Vesicles release Slp1 into the paramural space where it precipitates silicic acid. Other biomolecules have also been studied for their roles in biosilicification. For example, Belton et al. (2005a, 2005b) found that putrescine homologs positively affect condensation and aggregation, whilst analogs of spermine and spermidine positively affect aggregation. The effects of spermine and spermidine are related to their chain lengths. Significance of silicon deposition in cell walls in poor-accumulator species Numerous reports have suggested that supplementation of Si has beneficial effects even in poor-accumulator species such as tomato, canola, and Arabidopsis (Fauteux et al., 2006; Romero-Aranda et al., 2006; Hashemi et al., 2010; Khandekar and Leisner, 2011). This is puzzling since most studies over the last century have correlated Si-derived benefits with high accumulation. However, experiments performed with the rice lsi1 mutant may provide an explanation. Isa et al. (2010) used the mutant to examine the role of silica bodies in rice leaves and found that plants benefited even without forming Si-filled silica cells. The physiological role played by Si deposited in the cell wall seems to be different to that of Si deposited in the silica cells and silicon bodies. The growth enhancement observed in the lsi1 mutant in the absence of a high level of Si deposition might be the result of the formation of complexes of Si with polysaccharides in the cell wall. Evaluation of isolated cell walls from rice cell suspension cultures has shown crosslinking of Si with hemicellulose polysaccharides (He et al., 2015), which also suggests that very low amounts of silicon can change the cell wall physiology, leading to different observed effects in poor accumulators. This notion is further supported by a recent study in which a biophysical evaluation of single, isolated cells was carried out. Sheng et al. (2018) performed in situ micro-testing of ammonium (NH4+) ion fluxes in conjunction with atomic force microscopy of the cell wall and single-cell proteomics, and found that Si deposition clearly altered the cell wall structure, resulting in uptake of NH4+ that was twice that of cells cultured without Si. This indicates the role of Si in providing stability to the cell wall, which leads to optimized nutrient uptake and hence enhanced the growth and development with Si supplementation. A similar mechanism might be expected in species that do not accumulate Si in the aerial tissue because they lack a functional transporter, where Si interactions in the roots could still take place. Results from studies such as this are helpful in understanding the beneficial effects of Si in poor accumulators, but we need to add to the very limited information that is currently available. Summary Silicon is found in varying quantities in different tissues and it clearly imparts benefits to plant species. Among the numerous mechanisms explaining these benefits, the most commonly observed include alterations in physiological processes, modulation of stress responses, and biochemical interactions, such as those related to cell wall stability and the compositional diversity of phytoliths. A single mechanism or mode of action cannot account for the versatile roles that Si has been shown to perform (Fig. 7), and more studies at all scales of detail are therefore required if we are to gain a better understanding of how it benefits plants. We hope that the information provided in this review on the known molecular mechanisms, patterns of deposition, and roles in biotic and abiotic stress will be helpful in guiding future studies aimed at exploiting Si for agriculture applications. Fig. 7. Open in new tabDownload slide Biotic and abiotic stress tolerance mechanisms induced by silicon. Silicon is taken up by plant in the form of silicic acid present in soil, and is subsequently transported to other tissues where it is deposited in different cells and intracellular spaces. The uptake of silicon and its deposition result in numerous benefits to the plants, as indicated. Fig. 7. Open in new tabDownload slide Biotic and abiotic stress tolerance mechanisms induced by silicon. Silicon is taken up by plant in the form of silicic acid present in soil, and is subsequently transported to other tissues where it is deposited in different cells and intracellular spaces. The uptake of silicon and its deposition result in numerous benefits to the plants, as indicated. Acknowledgements RD and HS are thankful to the Government of India Department of Biotechnology for Ramalingaswami Fellowships, and the Science and Engineering Research Board (SERB) for financial support in the form of a grant (CRG/2019/006599). 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TI - Significance of silicon uptake, transport, and deposition in plants
JF - Journal of Experimental Botany
DO - 10.1093/jxb/eraa301
DA - 2020-12-02
UR - https://www.deepdyve.com/lp/oxford-university-press/significance-of-silicon-uptake-transport-and-deposition-in-plants-aGY3lJjSYg
SP - 6703
EP - 6718
VL - 71
IS - 21
DP - DeepDyve
ER -