Induction of silicon defences in wheat landraces is local, not systemic, and driven by mobilization of soluble silicon to damaged leaves.

In response to herbivory, many grasses, including crops such as wheat, accumulate significant levels of silicon (Si) as an antiherbivore defence. Damage-induced increases in Si can be localized in damaged leaves or be more systemic, but the mechanisms leading to these differences in Si distribution remain untested. Ten genetically diverse wheat landraces (Triticum aestivum) were used to assess genotypic variation in Si induction in response to mechanical damage and how this was affected by exogenous Si supply. Total and soluble Si levels were measured in damaged and undamaged leaves as well as in the phloem to test how Si was allocated to different parts of the plant after damage. Localized, but not systemic, induction of Si defences occurred, and was more pronounced when plants had supplemental Si. Damaged plants had significant increases in Si concentration in their damaged leaves, while the Si concentration in undamaged leaves decreased, such that there was no difference in the average Si concentration of damaged and undamaged plants. The increased Si in damaged leaves was due to the redirection of soluble Si, present in the phloem, from undamaged to damaged plant parts, potentially a more cost-effective defence mechanism for plants than increased Si uptake.

Climatic Drivers of Silicon Accumulation in a Model Grass Operate in Low- but Not High-Silicon Soils.

Grasses are hyper-accumulators of silicon (Si), which is known to alleviate diverse environmental stresses, prompting speculation that Si accumulation evolved in response to unfavourable climatic conditions, including seasonally arid environments. We conducted a common garden experiment using 57 accessions of the model grass Brachypodium distachyon, sourced from different Mediterranean locations, to test relationships between Si accumulation and 19 bioclimatic variables. Plants were grown in soil with either low or high (Si supplemented) levels of bioavailable Si. Si accumulation was negatively correlated with temperature variables (annual mean diurnal temperature range, temperature seasonality, annual temperature range) and precipitation seasonality. Si accumulation was positively correlated with precipitation variables (annual precipitation, precipitation of the driest month and quarter, and precipitation of the warmest quarter). These relationships, however, were only observed in low-Si soils and not in Si-supplemented soils. Our hypothesis that accessions of B. distachyon from seasonally arid conditions have higher Si accumulation was not supported. On the contrary, higher temperatures and lower precipitation regimes were associated with lower Si accumulation. These relationships were decoupled in high-Si soils. These exploratory results suggest that geographical origin and prevailing climatic conditions may play a role in predicting patterns of Si accumulation in grasses.

Pathways of degradation in rangelands in Northern Tanzania show their loss of resistance, but potential for recovery.

Semiarid rangelands are identified as at high risk of degradation due to anthropogenic pressure and climate change. Through tracking timelines of degradation we aimed to identify whether degradation results from a loss of resistance to environmental shocks, or loss of recovery, both of which are important prerequisites for restoration. Here we combined extensive field surveys with remote sensing data to explore whether long-term changes in grazing potential demonstrate loss of resistance (ability to maintain function despite pressure) or loss of recovery (ability to recover following shocks). To monitor degradation, we created a bare ground index: a measure of grazeable vegetation cover visible in satellite imagery, allowing for machine learning based image classification. We found that locations that ended up the most degraded tended to decline in condition more during years of widespread degradation but maintained their recovery potential. These results suggest that resilience in rangelands is lost through declines in resistance, rather than loss of recovery potential. We show that the long-term rate of degradation correlates negatively with rainfall and positively with human population and livestock density, and conclude that sensitive land and grazing management could enable restoration of degraded landscapes, given their retained ability to recover.

The Ability of Silicon Fertilisation to Alleviate Salinity Stress in Rice is Critically Dependent on Cultivar.

Silicon (Si) fertiliser can improve rice (Oryza sativa) tolerance to salinity. The rate of Si uptake and its associated benefits are known to differ between plant genotypes, but, to date, little research has been done on how the benefits, and hence the economic feasibility, of Si fertilisation varies between cultivars. In this study, a range of rice cultivars was grown both hydroponically and in soil, at different levels of Si and NaCl, to determine cultivar variation in the response to Si. There was significant variation in the effect of Si, such that Si alleviated salt-induced growth inhibition in some cultivars, while others were unaffected, or even negatively impacted. Thus, when assessing the benefits of Si supplementation in alleviating salt stress, it is essential to collect cultivar-specific data, including yield, since changes in biomass were not always correlated with those seen for yield. Root Si content was found to be more important than shoot Si in protecting rice against salinity stress, with a root Si level of 0.5-0.9% determined as having maximum stress alleviation by Si. A cost-benefit analysis indicated that Si fertilisation is beneficial in mild stress, high-yield conditions but is not cost-effective in low-yield production systems.

Elevated atmospheric CO2 changes defence allocation in wheat but herbivore resistance persists.

Predicting how plants allocate to different anti-herbivore defences in response to elevated carbon dioxide (CO2) concentrations is important for understanding future patterns of crop susceptibility to herbivory. Theories of defence allocation, especially in the context of environmental change, largely overlook the role of silicon (Si), despite it being the major anti-herbivore defence in the Poaceae. We demonstrated that elevated levels of atmospheric CO2 (e[CO2]) promoted plant growth by 33% and caused wheat (Triticum aestivum) to switch from Si (-19%) to phenolic (+44%) defences. Despite the lower levels of Si under e[CO2], resistance to the global pest Helicoverpa armigera persisted; relative growth rates (RGRs) were reduced by at least 33% on Si-supplied plants, irrespective of CO2 levels. RGR was negatively correlated with leaf Si concentrations. Mandible wear was c. 30% higher when feeding on Si-supplemented plants compared to those feeding on plants with no Si supply. We conclude that higher carbon availability under e[CO2] reduces silicification and causes wheat to increase concentrations of phenolics. However, Si supply, at all levels, suppressed the growth of H. armigera under both CO2 regimes, suggesting that shifts in defence allocation under future climate change may not compromise herbivore resistance in wheat.

Short-term exposure to silicon rapidly enhances plant resistance to herbivory.

Silicon (Si) can adversely affect insect herbivores, particularly in plants that evolved the ability to accumulate large quantities of Si. Very rapid herbivore-induced accumulation of Si has recently been demonstrated, but the level of protection against herbivory this affords plants remains unknown. Brachypodium distachyon, a model Si hyperaccumulating grass, was exposed to the chewing herbivore, Helicoverpa armigera, and grown under three conditions: supplied Si over 34 d (+Si), not supplied Si (-Si), or supplied Si once herbivory began (-Si → +Si). We evaluated the effectiveness of each Si treatment at reducing herbivore performance and measured Si-based defenses and phenolics (another form of defense often reduced by Si). Although Si concentrations remained lower, within 72 h of exposure to Si, -Si → +Si plants were as resistant to herbivory as +Si plants. Both +Si and -Si → +Si treatments reduced herbivore damage and growth, and increased mandible wear compared to -Si. After 6 h, herbivory increased filled Si cell density in -Si → +Si plants, and within 24 h, -Si → +Si plants reached similar filled Si cell densities to +Si plants, although decreased phenolics only occurred in +Si plants. We demonstrate that plants with short-term Si exposure can rapidly accumulate Si-based antiherbivore defenses as effectively as plants with long-term exposure.

The Effect of Silicon on Osmotic and Drought Stress Tolerance in Wheat Landraces.

Drought stress reduces annual global wheat yields by 20%. Silicon (Si) fertilisation has been proposed to improve plant drought stress tolerance. However, it is currently unknown if and how Si affects different wheat landraces, especially with respect to their innate Si accumulation properties. In this study, significant and consistent differences in Si accumulation between landraces were identified, allowing for the classification of high Si accumulators and low Si accumulators. Landraces from the two accumulation groups were then used to investigate the effect of Si during osmotic and drought stress. Si was found to improve growth marginally in high Si accumulators during osmotic stress. However, no significant effect of Si on growth during drought stress was found. It was further found that osmotic stress decreased Si accumulation for all landraces whereas drought increased it. Overall, these results suggest that the beneficial effect of Si commonly reported in similar studies is not universal and that the application of Si fertiliser as a solution to agricultural drought stress requires detailed understanding of genotype-specific responses to Si.

Targeted plant defense: silicon conserves hormonal defense signaling impacting chewing but not fluid-feeding herbivores.

Plants deploy an arsenal of chemical and physical defenses against arthropod herbivores, but it may be most cost efficient to produce these only when attacked. Herbivory activates complex signaling pathways involving several phytohormones, including jasmonic acid (JA), which regulate production of defensive compounds. The Poaceae also have the capacity to take up large amounts of silicon (Si), which accumulates in plant tissues. Si accumulation has antiherbivore properties, but it is poorly understood how Si defenses relate to defense hormone signaling. Here we show that Si enrichment causes the model grass Brachypodium distachyon to show lower levels of JA induction when attacked by chewing herbivores. Triggering this hormone even at lower concentrations, however, prompts Si uptake and physical defenses (e.g., leaf hairs), which negatively impact chewing herbivores. Removal of leaf hairs restored performance. Crucially, activation of such Si-based defense is herbivore-specific and occurred only in response to chewing and not fluid-feeding (aphid) herbivores. This aligned with our meta-analysis of 88 studies that showed Si defenses were more effective against chewing herbivores than fluid feeders. Our results suggest integration between herbivore defenses in a model Si-accumulating plant, which potentially allows it to avoid unnecessary activation of other costly defenses.

Silicon deposition on guard cells increases stomatal sensitivity as mediated by K+ efflux and consequently reduces stomatal conductance.

Silicon (Si) has been widely reported to improve plant resistance to water stress via various mechanisms including cuticular Si deposition to reduce leaf transpiration. However, there is limited understanding of the effects of Si on stomatal physiology, including the underlying mechanisms and implications for resistance to water stress. We grew tall fescue (Festuca arundinacea Schreb. cv. Fortuna) hydroponically, with or without Si, and treated half of the plants with 20% polyethylene glycol to impose physiological drought (osmotic stress). Scanning electron microscopy in conjunction with X-ray mapping found that Si was deposited on stomatal guard cells and as a sub-cuticular layer in Si-treated plants. Plants grown in Si had a 28% reduction in stomatal conductance and a 23% reduction in cuticular conductance. When abscisic acid was applied exogenously to epidermal leaf peels to promote stomatal closure, Si plants had 19% lower stomatal aperture compared to control plants (i.e. increased stomatal sensitivity) and an increased efflux of guard cell K+ ions. However, the changes in stomatal physiology with Si were not substantial enough to improve water stress resistance, as shown by a lack of significant effect of Si on water potential, growth, photosynthesis and water-use efficiency. Our findings suggest a novel underlying mechanism for reduced stomatal conductance with Si application; specifically, that Si deposition on stomatal guard cells promotes greater stomatal sensitivity as mediated by guard cell K+ efflux.

Silicon Defence in Plants: Does Herbivore Identity Matter?

Silicon accumulation is a key defence against herbivorous pests, but may have wider detrimental impacts if plants become unpalatable for livestock. We argue that some herbivores are better adapted to silicon-rich diets than others; herbivore anatomy and physiology, and the nature of silicon deposition, are crucial to understanding these differences.

Is Silicon a Panacea for Alleviating Drought and Salt Stress in Crops?

Salinity affects around 20% of all arable land while an even larger area suffers from recurrent drought. Together these stresses suppress global crop production by as much as 50% and their impacts are predicted to be exacerbated by climate change. Infrastructure and management practices can mitigate these detrimental impacts, but are costly. Crop breeding for improved tolerance has had some success but is progressing slowly and is not keeping pace with climate change. In contrast, Silicon (Si) is known to improve plant tolerance to a range of stresses and could provide a sustainable, rapid and cost-effective mitigation method. The exact mechanisms are still under debate but it appears Si can relieve salt stress via accumulation in the root apoplast where it reduces "bypass flow of ions to the shoot. Si-dependent drought relief has been linked to lowered root hydraulic conductance and reduction of water loss through transpiration. However, many alternative mechanisms may play a role such as altered gene expression and increased accumulation of compatible solutes. Oxidative damage that occurs under stress conditions can be reduced by Si through increased antioxidative enzymes while Si-improved photosynthesis has also been reported. Si fertilizer can be produced relatively cheaply and to assess its economic viability to improve crop stress tolerance we present a cost-benefit analysis. It suggests that Si fertilization may be beneficial in many agronomic settings but may be beyond the means of smallholder farmers in developing countries. Si application may also have disadvantages, such as increased soil pH, less efficient conversion of crops into biofuel and reduced digestibility of animal fodder. These issues may hamper uptake of Si fertilization as a routine agronomic practice. Here, we critically evaluate recent literature, quantifying the most significant physiological changes associated with Si in plants under drought and salinity stress. Analyses show that metrics associated with photosynthesis, water balance and oxidative stress all improve when Si is present during plant exposure to salinity and drought. We further conclude that most of these changes can be explained by apoplastic roles of Si while there is as yet little evidence to support biochemical roles of this element.

The Role of Silicon in Antiherbivore Phytohormonal Signalling.

The role of plant silicon (Si) in the alleviation of abiotic and biotic stress is now widely recognised and researched. Amongst the biotic stresses, Si is known to increase resistance to herbivores through biomechanical and chemical mechanisms, although the latter are indirect and remain poorly characterised. Chemical defences are principally regulated by several antiherbivore phytohormones. The jasmonic acid (JA) signalling pathway is particularly important and has been linked to Si supplementation, albeit with some contradictory findings. In this Perspectives article, we summarise existing knowledge of how Si affects JA in the context of herbivory and present a conceptual model for the interactions between Si and JA signalling in wounded plants. Further, we use novel information from the model grass Brachypodium distachyon to underpin aspects of this model. We show that Si reduces JA concentrations in plants subjected to chemical induction (methyl jasmonate) and herbivory (Helicoverpa armigera) by 34% and 32%, respectively. Moreover, +Si plants had 13% more leaf macrohairs than -Si plants. From this study and previous work, our model proposes that Si acts as a physical stimulus in the plant, which causes a small, transient increase in JA. When +Si plants are subsequently attacked by herbivores, they potentially show a faster induction of JA due to this priming. +Si plants that have already invested in biomechanical defences (e.g. macrohairs), however, have less utility for JA-induced defences and show lower levels of JA induction overall.

Simulated Herbivory: The Key to Disentangling Plant Defence Responses.

Plants are subjected to a multitude of stimuli during insect herbivory, resulting in a complex and cumulative defence response. Breaking down the components of herbivory into specific stimuli and identifying the mechanisms of defence associated with them has thus far been challenging. Advances in our understanding of responses to inconspicuous stimuli, such as those induced by microbial symbionts in herbivore secretions and mechanical stimulation caused by insects, have illuminated the intricacies of herbivory. Here, we provide a synthesis of the interacting impacts of herbivory on plants and the consequential complexities associated with uncoupling defence responses. We propose that simulated herbivory should be used to complement true herbivory to decipher the mechanisms of insect herbivore-induced plant defence responses.

Population-level manipulations of field vole densities induce subsequent changes in plant quality but no impacts on vole demography.

Grazing-induced changes in plant quality have been suggested to drive the negative delayed density dependence exhibited by many herbivore species, but little field evidence exists to support this hypothesis. We tested a key premise of the hypothesis that reciprocal feedback between vole grazing pressure and the induction of anti-herbivore silicon defenses in grasses drives observed population cycles in a large-scale field experiment in northern England. We repeatedly reduced population densities of field voles (Microtus agrestis) on replicated 1-ha grassland plots at Kielder Forest, northern England, over a period of 1 year. Subsequently, we tested for the impact of past density on vole life history traits in spring, and whether these effects were driven by induced silicon defenses in the voles' major over-winter food, the grass Deschampsia caespitosa. After several months of density manipulation, leaf silicon concentrations diverged and averaged 22% lower on sites where vole density had been reduced, but this difference did not persist beyond the period of the density manipulations. There were no significant effects of our density manipulations on vole body mass, spring population growth rate, or mean date for the onset of spring reproduction the following year. These findings show that grazing by field voles does induce increased silicon defenses in grasses at a landscape scale. However, at the vole densities encountered, levels of plant damage appear to be below those needed to induce changes in silicon levels large and persistent enough to affect vole performance, confirming the threshold effects we have previously observed in laboratory-based studies. Our findings do not support the plant quality hypothesis for observed vole population cycles in northern England, at least over the range of vole densities that now prevail here.

Benefits from Below: Silicon Supplementation Maintains Legume Productivity under Predicted Climate Change Scenarios.

Many studies demonstrate that elevated atmospheric carbon dioxide concentrations (eCO2) can promote root nodulation and biological nitrogen fixation (BNF) in legumes such as lucerne (Medicago sativa). But when elevated temperature (eT) conditions are applied in tandem with eCO2, a more realistic scenario for future climate change, the positive effects of eCO2 on nodulation and BNF in M. sativa are often much reduced. Silicon (Si) supplementation of M. sativa has also been reported to promote root nodulation and BNF, so could potentially restore the positive effects of eCO2 under eT. Increased nitrogen availability, however, could also increase host suitability for aphid pests, potentially negating any benefit. We applied eCO2 (+240 ppm) and eT (+4°C), separately and in combination, to M. sativa growing in Si supplemented (Si+) and un-supplemented soil (Si-) to determine whether Si moderated the effects of eCO2 and eT. Plants were either inoculated with the aphid Acyrthosiphon pisum or insect-free. In Si- soils, eCO2 stimulated plant growth by 67% and nodulation by 42%, respectively, whereas eT reduced these parameters by 26 and 48%, respectively. Aphids broadly mirrored these effects on Si- plants, increasing colonization rates under eCO2 and performing much worse (reduced abundance and colonization) under eT when compared to ambient conditions, confirming our hypothesized link between root nodulation, plant growth, and pest performance. Examined across all CO2 and temperature regimes, Si supplementation promoted plant growth (+93%), and root nodulation (+50%). A. pisum abundance declined sharply under eT conditions and was largely unaffected by Si supplementation. In conclusion, supplementing M. sativa with Si had consistent positive effects on plant growth and nodulation under different CO2 and temperature scenarios. These findings offer potential for using Si supplementation to maintain legume productivity under predicted climate change scenarios without making legumes more susceptible to insect pests.

Elevated carbon dioxide and warming impact silicon and phenolic-based defences differently in native and exotic grasses.

Global climate change may increase invasions of exotic plant species by directly promoting the success of invasive/exotic species or by reducing the competitive abilities of native species. Changes in plant chemistry, leading to altered susceptibility to stress, could mediate these effects. Grasses are hyper-accumulators of silicon, which play a crucial function in the alleviation of diverse biotic and abiotic stresses. It is unknown how predicted increases in atmospheric carbon dioxide (CO2 ) and air temperature affect silicon accumulation in grasses, especially in relation to primary and secondary metabolites. We tested how elevated CO2 (eCO2 ) (+240 ppm) and temperature (eT) (+4°C) affected chemical composition (silicon, phenolics, carbon and nitrogen) and plant growth in eight grass species, either native or exotic to Australia. eCO2 increased phenolic concentrations by 11%, but caused silicon accumulation to decline by 12%. Moreover, declines in silicon occurred mainly in native species (-19%), but remained largely unchanged in exotic species. Conversely, eT increased silicon accumulation in native species (+19%) but decreased silicon accumulation in exotic species (-10%). Silicon and phenolic concentrations were negatively correlated with each other, potentially reflecting a defensive trade-off. Moreover, both defences were negatively correlated with plant mass, compatible with a growth-defence trade-off. Grasses responded in a species-specific manner, suggesting that the relative susceptibility of different species may differ under future climates compared to current species rankings of resource quality. For example, the native Microlaena stipoides was less well defended under eCO2 in terms of both phenolics and silicon, and thus could suffer greater vulnerability to herbivores. To our knowledge, this is the first demonstration of the impacts of eCO2 and eT on silicon accumulation in grasses. We speculate that the greater plasticity in silicon uptake shown by Australian native grasses may be partly a consequence of evolving in a low nutrient and seasonally arid environment.

Evidence for Active Uptake and Deposition of Si-based Defenses in Tall Fescue.

Silicon (Si) is taken up from the soil as monosilicic acid by plant roots, transported to leaves and deposited as phytoliths, amorphous silica (SiO2) bodies, which are a key component of anti-herbivore defense in grasses. Silicon transporters have been identified in many plant species, but the mechanisms underpinning Si transport remain poorly understood. Specifically, the extent to which Si uptake is a passive process, driven primarily by transpiration, or has both passive and active components remains disputed. Increases in foliar Si concentration following herbivory suggest plants may exercise some control over Si uptake and distribution. In order to investigate passive and active controls on Si accumulation, we examined both genetic and environmental influences on Si accumulation in the forage grass Festuca arundinacea. We studied three F. arundinacea varieties that differ in the levels of Si they accumulate. Varieties not only differed in Si concentration, but also in increases in Si accumulation in response to leaf damage. The varietal differences in Si concentration generally reflected differences in stomatal density and stomatal conductance, suggesting passive, transpiration-mediated mechanisms underpin these differences. Bagging plants after damage was employed to minimize differences in stomatal conductance between varieties and in response to damage. This treatment eliminated constitutive differences in leaf Si levels, but did not impair the damage-induced increases in Si uptake: damaged, bagged plants still had more leaf Si than undamaged, bagged plants in all three varieties. Preliminary differential gene expression analysis revealed that the active Si transporter Lsi2 was highly expressed in damaged unbagged plants compared with undamaged unbagged plants, suggesting damage-induced Si defenses are regulated at gene level. Our findings suggest that although differences in transpiration may be partially responsible for varietal differences in Si uptake, they cannot explain damage-induced increases in Si uptake and deposition, suggesting that wounding causes changes in Si uptake, distribution and deposition that likely involve active processes and changes in gene expression.

Impacts of silicon-based grass defences across trophic levels under both current and future atmospheric CO2 scenarios.

Silicon (Si) has important functional roles in plants, including resistance against herbivores. Environmental change, such as increasing atmospheric concentrations of CO2, may alter allocation to Si defences in grasses, potentially changing the feeding behaviour and performance of herbivores, which may in turn impact on higher trophic groups. Using Si-treated and untreated grasses (Phalaris aquatica) maintained under ambient (400 ppm) and elevated (640 and 800 ppm) CO2 concentrations, we show that Si reduced feeding by crickets (Acheta domesticus), resulting in smaller body mass. This, in turn, reduced predatory behaviour by praying mantids (Tenodera sinensis), which consequently performed worse. Despite elevated CO2 decreasing Si concentrations in P. aquatica, this reduction was not large enough to affect the feeding behaviour of crickets or their predator. Our results suggest that Si-based defences in plants have adverse impacts on both primary and secondary trophic taxa, and these are not likely to decline under future climate change scenarios.

DRI-Grass: A New Experimental Platform for Addressing Grassland Ecosystem Responses to Future Precipitation Scenarios in South-East Australia.

Climate models predict shifts in the amount, frequency and seasonality of rainfall. Given close links between grassland productivity and rainfall, such changes are likely to have profound effects on the functioning of grassland ecosystems and modify species interactions. Here, we introduce a unique, new experimental platform - DRI-Grass (Drought and Root Herbivore Interactions in a Grassland) - that exposes a south-eastern Australian grassland to five rainfall regimes [Ambient (AMB), increased amount (IA, +50%), reduced amount (RA, -50%), reduced frequency (RF, single rainfall event every 21 days, with total amount unchanged) and summer drought (SD, 12-14 weeks without water, December-March)], and contrasting levels of root herbivory. Incorporation of a belowground herbivore (root-feeding scarabs) addition treatment allows novel investigation of ecological responses to the twin stresses of altered rainfall and root herbivory. We quantified effects of permanently installed rain shelters on microclimate by comparison with outside plots, identifying small shelter effects on air temperature (-0.19°C day, +0.26°C night), soil water content (SWC; -8%) and photosynthetically active radiation (PAR; -16%). Shelters were associated with modest increases in net primary productivity (NPP), particularly during the cool season. Rainfall treatments generated substantial differences in SWC, with the exception of IA; the latter is likely due to a combination of higher transpiration rates associated with greater plant biomass in IA and the low water-holding capacity of the well-drained, sandy soil. Growing season NPP was strongly reduced by SD, but did not respond to the other rainfall treatments. Addition of root herbivores did not affect plant biomass and there were no interactions between herbivory and rainfall treatments in the 1st year of study. Root herbivory did, however, induce foliar silicon-based defenses in Cynodon dactylon and Eragrostis curvula. Rapid recovery of NPP following resumption of watering in SD plots indicates high functional resilience at the site, and may reflect adaptation of the vegetation to historically high variability in rainfall, both within- and between years. DRI-Grass provides a unique platform for understanding how ecological interactions will be affected by changing rainfall regimes and, specifically, how belowground herbivory modifies grassland resistance and resilience to climate extremes.