The Role of Silicon in Higher Plants under Salinity and Drought Stress

1Although appreciated by biologists for >150 years, the benefits of silicon (Si) to plants, particularly under stress, have been studied intensively only in recent decades. This is largely due to silicon’s “non-essential" designation by early plant nutritionists (e.g.,;; see also;, for historical overview). Indeed, Si is not considered “essential" for higher plants, as they can fulfil their life cycles without it. Nevertheless, Si is considered to be “quasi-essential", due to the far-reaching benefits it confers on plants, including enhanced growth, yield and crop quality, photosynthesis, N2 fixation, particularly in response to abiotic and biotic stresses such as infectious disease, herbivory, gravity, metal toxicity, high and low temperature, UV radiation, nutrient deficiency and excess, drought, and salinity (for review, see,,;;;,;;; ).

2However, despite much recent research, the mechanisms underlying these effects are not well understood, although important new insights into the membrane transport of Si (,; cf. ), and the alleviatory role of Si in biotic stress have been gained. Mechanistic understanding of the role of Si in abiotic stress resistance, however, is relatively limited, but important avenues of research in salinity and drought contexts are emerging (for review, see;; ). Salinity stress affects over 800 million hectares globally – up to a third of all agricultural land and nearly half of all irrigated land, which produces roughly a third of the world’s food. Drought stress, which shares many features with salinity stress, is even more pervasive and damaging to agricultural production, particularly in arid and semi-arid regions, which account for approximately 30% of the world’s land area. Both problems are predicted to be aggravated by anthropogenic climate change.

3In this mini-review, we focus on current understanding (and gaps therein) of the mechanisms underlying silicon-induced alleviation of salinity and drought stress in higher plants, and will also discuss the feasibility of Si amendments in arid or saline agricultural fields. Where possible, we distinguish apoplast effects (i.e., suberization, lignification, and silicification of the extracellular matrix; transpirational bypass flow of solutes and water), from those of the symplast (i.e., transmembrane transport of solutes and water; gene expression; oxidative stress; metabolism), and consider where mechanistic overlaps exist.

4Silicon is well documented to strengthen cell walls and provide mechanical support for monocots and pteridophytes (much less is known about dicots), by enhancing suberization, lignification, and silicification (for a recent review, see ). Improved structural stability has been attributed to the binding of Si with cell-wall hemicellulose, which is clearly beneficial under water deficit. In addition, biosilicification in plants, involving the polymerization of silicic acid within the apoplast, leads to the formation of an amorphous silica barrier, which can help alleviate both biotic and abiotic stresses, hindering pathogen infection and the penetration of potential toxicants such as aluminum (Al), manganese (Mn), cadmium (Cd), zinc (Zn), and sodium (Na), into the symplast and/or transpiration stream. In roots of salt-sensitive and -tolerant wheat, for example, Si increased cell-wall binding of Na+ in the root while decreasing its transport to the shoot (;; see also below); however, direct evidence of Na+ complexation by Si, which may underlie this potentially important salt-tolerance mechanism, is lacking.

5Silicon has also been shown to promote Casparian band development in the root endodermis and exodermis. For example, in rice, Si treatment resulted in enhanced suberization, and lignification of sclerenchyma, in these tissues (; cf. ), which coincided with reduced radial oxygen loss and oxidation power in the mature root. Si also triggered the transcription of genes related to lignin and suberin synthesis (; see below). These components can form barriers to apoplastic Na+ transport in roots, correlating with higher salt tolerance in rice. In particular, Si deposition in the endodermis is proposed to restrict Na+ transport along a “transpirational bypass” route from root to shoot in rice, as we shall now discuss.

6Limiting shoot Na+ and Cl- accumulation is critical to salt tolerance in many species, as it may prevent leaf metabolic disorders, ion imbalances, and the desiccation of leaf tissue via osmotic stress. This is particularly important in rice, where, in addition to normal transpiration, involving xylem loading via the symplast, there is a pronounced transpirational bypass flow, i.e., a bypassing of the symplast in regions where endodermal barriers are underdeveloped or absent (root tips, or zones of lateral root emergence;;;; see also;;;; ). Si provision has been shown to reduce root-to-shoot translocation of both Na+ and Cl- in salt-stressed rice, despite increasing transpiration and stomatal conductance, indicating that Si does not act to reduce sodium translocation by reducing transpiration per se, but rather by blocking bypass flow (;; Figure 1, inset). The proposal that Si deposition in endodermal and exodermal Casparian bands forms physical barriers to Na+ and Cl- translocation is supported by X-ray localization patterns of Si deposition, and the greatly reduced translocation, with Si treatment, of the apoplastic dye trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS) (;; see also ). Whether this mechanism is peculiar to rice, or is taxonomically widespread, awaits investigation in other species.

7Effects of Si on transpiration depend on species and environmental conditions. While Si increased transpiration in both drought and salt-stressed rice (; see above), Si decreased transpiration in non-stressed rice. Similar observations were found in drought-stressed wheat and sorghum, while, by contrast, Si reduced transpiration in drought-stressed maize, and had no effect in cucumber. Such variability suggests divergent strategies among species, as they balance rates of water uptake and those of leaf-level water loss. The mechanisms underlying these strategies and responses to Si require much more discovery and analysis.

8Salt- and drought-stressed plants have reduced water uptake and content, both of which can be alleviated by Si provision, which leads to improved water status and water-use efficiency in many species. In sorghum, for example, Si increased root and whole-plant hydraulic conductance, transpiration, stomatal conductance, and leaf water content under osmotic stress. The increase in root hydraulic conductance coincided with a 2- to 4-fold increased expression of plasma-membrane intrinsic protein (PIP) aquaporins, and increased PIP-mediated water transport was suggested by inhibition of the water flux by mercury (Hg2+) (,; see also ). The use of Hg2+ as an aquaporin inhibitor should be taken with caution, however, as it can also inhibit influx of K+, which can affect water transport due to the important osmotic role of K+. Regardless, the mechanisms by which Si nutrition affects aquaporin expression and activity have yet to be resolved.

9It is interesting that Si transport is also mediated by aquaporins, specifically members of the Nod26-like major intrinsic protein (NIP) III subgroup. The expression pattern of Lsi1, a NIP homolog encoding a Si influx transporter, shows varying responses to Si nutrition in different species. For example, its expression in response to Si provision is downregulated in rice and soybean, unaffected in maize, barley, and wheat, and upregulated in cucumber (; and references therein). Interestingly, under salinity stress, OsLsi1 expression was upregulated in roots of both a salt-sensitive and -tolerant variety of rice (1.82- and 2.12-fold, respectively; ). The authors proposed that this may result in greater Si uptake in the salt-tolerant variety compared to the salt-sensitive one, with enhanced Si deposition in the transpirational bypass route, and thus restricted shoot Na+ translocation. Given that rice OsLsi1 expression shows opposing responses to Si supply and salinity stress separately, it would be interesting to see how expression responds to co-application in this important, salt-sensitive, and highly water-demanding species.

10Besides affecting hydraulic conductance and water transport by modulating aquaporin expression/activity, Si can affect water transport by adjusting the osmotic potential of cells through increased osmolyte accumulation (e.g., proline, soluble sugars, inorganic ions, etc.;;;; ). Increased root hydraulic conductance may also be attributed to Si-induced reductions in oxidative stress and membrane damage (; see below).

11The reduction of Na+ influx from the external solution into the cytosol, and the increase of Na+ efflux in the opposite direction (or from cytosol to vacuole) have been proposed to be major salt-tolerance mechanisms; both work toward lowering cytosolic Na+ pools. In addition, homeostatic maintenance of intracellular K+ pools under salt stress is critical to maintain proper cell function. Si may alleviate salinity stress by influencing these aspects of Na+ and K+ transport and accumulation (for review, see; ). In salt-stressed barley, activities of root plasma membrane H+-ATPase, and tonoplast H+-ATPase and H+-PPase, are stimulated under Si supply. These changes in cellular H+ pumps have been proposed to enhance Na+ efflux via the Na+-H+ exchangers HvSOS1 and HvNHX1 (in the plasma membrane and tonoplast, respectively), and K+ influx via K+-H+ symporters such as HvHAK1, as they are secondarily active fluxes driven by electrochemical H+ gradients. However, proton-pump stimulation may be indirect, as H+-ATPase activity was unaffected by Si in plasma membrane vesicles from leaves of salt-stressed barley. Moreover, we have found no evidence for an effect of Si on putatively SOS1-mediated Na+ efflux in our own laboratory, in roots of intact rice seedlings under salinity stress (Figure 1, main panel; see also ). Nevertheless, this is an interesting potential mechanism of Si-mediated salt tolerance that requires further investigation by various means, including measurements of Na+ fluxes in root tips, where recent physiological evidence of Na+-H+ antiport activity has been demonstrated, as well as in planta K+ fluxes.

12Silicon can stimulate synthesis and accumulation of polyamines (PA) such as putrescine, spermidine, and spermine, in salt-stressed plants, and this has also been proposed to help mediate salt tolerance (;;; see also below). PA production may function in this way via regulating K+ and Na+ transport, improving antioxidant ability, and modifying osmotic potential. Patch-clamp analysis in root epidermal and cortical protoplasts from salt-stressed barley showed that PAs blocked inward and outward Na+ and K+ currents via non-selective cation channels (NSCCs; ), suggesting that this may prevent toxic intracellular accumulation of Na+; however, it is important to note that in planta evidence of NSCC-mediated fluxes is currently lacking, and such claims should be interpreted cautiously.

13Lipid peroxidation by reactive oxygen species (ROS) is another major mechanism of salt toxicity in higher plants. Si has been shown to decrease the concentration of malondialdehyde (MDA), the end-product of lipid peroxidation, in salt-stressed barley, maize, and grapevine rootstock, and thus may help to maintain membrane integrity and decrease permeability. Si has also been shown to increase the activity of key antioxidant defense enzymes superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), as well as glutathione reductase (GR) activities and the glutathione (GSH) concentration in salt-stressed plants. showed that MDA concentrations were positively correlated with Na+ uptake in salt-stressed cucumber but negatively correlated with Ca2+ and K+ uptake, and with Si supply. How Si mediates this response is unclear, but the explanation that, under Si supply, stabilized membranes lead to symplastic [Na+] reductions, and [K+] and [Ca2+] increases, is more parsimonious than one invoking altered ion transporters such as NSCCs (see above).

14Silicon is the second most abundant soil element after oxygen, comprising ∼29% of the Earth’s crust. This is mostly as insoluble crystalline aluminosilicates, which are not plant-available. Soluble, bioavailable Si, by contrast (i.e., monosilicic/orthosilicic acid; H4SiO4), normally ranges between 0.1 and 0.6 mM in soils. H4SiO4 is weakly acidic (pKa1 = 9.84, pKa2 = 13.2), and thus is largely undissociated in most soils. The traditional view, that bioavailable Si derives from solvation of primary and secondary minerals and buffered by the adsorption and desorption of silicate onto sesquioxides, has been supplanted by the idea that phytogenic cycling of Si (uptake by plants, silica formation mainly in leaves, and return to the soil as plant litter) is the main determinant of bioavailable soil Si in natural ecosystems (; see also; ). Si pools in agricultural soils are often low due to the regular removal of Si-rich litter during harvest, a practice which may be altering terrestrial and global Si cycling.

15Use of Si fertilizers began in the 1950s in Japan and is now widespread, the most common sources being industrial slags, as well as plant straw, typically from rice. These applications have been effective in enhancing the yield and quality of many agricultural crops, including both monocots such as rice, wheat, maize, barley, millet, sorghum, and sugarcane, and dicots such as cotton and soybean (; and references therein).

16It has been claimed that Si primarily benefits stressed plants, with minor effects on unstressed plants. For example, Si addition showed little alteration of the transcriptome of unstressed Arabidopsis, wheat, and rice (; cf.; ), and the proteome of rice. However, such changes do not necessarily indicate the lack of a beneficial role. In long-term studies, Si was shown to increase crop yields, even in unstressed rice; this was attributed to lower transpiration by spikelets. Si was also shown to increase yields of rice growing under non-stressed conditions by altering source-sink relationships and increasing photosynthesis, mesophyll conductance, N-use efficiency, and mobilization of photoassimilates and amino acids from vegetative tissues to grains. The authors suggested that Si may act as a signaling factor redirecting the primary metabolism of plants, although the mechanism by which this is achieved is not known; this is an exciting and promising new avenue of Si research.

17Lastly, a new prospect of Si research involves “seed priming,” whereby exposing seeds to Si for only a few hours fortifies plants against future stress events. Currently, the priming literature is focused on biotic stress resistance, and relatively few studies have investigated effects on performance under abiotic stress; however, several interesting and promising findings have emerged. For example, wheat seeds treated with Si for 6–8 h showed significant increases in germination rate, vegetative growth, and crop yield under salinity and osmotic stresses, compared to non-primed seeds. Similarly, maize plants grown from seeds treated for 12 h in Si showed increased growth, leaf relative water content, and levels of photosynthetic pigments, soluble sugars, soluble proteins, total free amino acids, potassium, and activities of SOD, CAT, and POD enzymes, compared to plants that were not primed. Moreover, Si-primed seedlings showed decreased proline, MDA, and Na+ contents. Although the underlying mechanisms are unknown, and much more investigation is required, seed priming appears to be a promising and cost-effective procedure to confer resistance to major stresses such as drought and salinity.

18Plant silicon research has made great strides since the designation of Si as “non-essential.” While this element is still generally excluded from most plant growth-media formulations, it is now widely accepted to benefit many plant species, including many agriculturally prominent crops. While these benefits may be particularly pronounced under stresses such as drought and salinity, growing evidence indicates that Si may also improve growth under relatively benign conditions. Today, the multiple threats faced by our species, including rapid human population growth, changing climate, and increasing salinity, add urgency to the investigation of crop improvement by Si.

19DC wrote the manuscript, with input and editing from DB, WH, and HK.

20The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.