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.

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.

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.

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.

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.

Roots under attack: contrasting plant responses to below- and aboveground insect herbivory.

The distinctive ecology of root herbivores, the complexity and diversity of root-microbe interactions, and the physical nature of the soil matrix mean that plant responses to root herbivory extrapolate poorly from our understanding of responses to aboveground herbivores. For example, root attack induces different changes in phytohormones to those in damaged leaves, including a lower but more potent burst of jasmonates in several plant species. Root secondary metabolite responses also differ markedly, although patterns between roots and shoots are harder to discern. Root defences must therefore be investigated in their own ecophysiological and evolutionary context, specifically one which incorporates root microbial symbionts and antagonists, if we are to better understand the battle between plants and their hidden herbivores.

Infection by a foliar endophyte elicits novel arabidopside-based plant defence reactions in its host, Cirsium arvense.

Endophytic fungi live asymptomatically within plants. They are usually regarded as nonpathogenic or even mutualistic, but whether plants respond antagonistically to their presence remains unclear, particularly in the little-studied associations between endophytes and nongraminoid herbaceous plants. We investigated the effects of the endophyte Chaetomium cochlioides on leaf chemistry in Cirsium arvense. Plants were sprayed with spores; leaf material from both subsequent new growth and the sprayed leaves was analysed 2 wk later. Infection frequency was 91% and 63% for sprayed and new growth, respectively, indicating that C. cochlioides rapidly infects new foliage. Metabolomic analyses revealed marked changes in leaf chemistry with infection, especially in new growth. Changes in several novel oxylipin metabolites were detected, including arabidopsides reported here for the first time in a plant species other than Arabidopsis thaliana, and a jasmonate-containing galactolipid. The production of these metabolites in response to endophyte presence, particularly in newly infected foliage, suggests that endophytes elicit similar chemical responses in plants to those usually produced following wounding, herbivory and pathogen invasion. Whether endophytes benefit their hosts may depend on a complex series of chemically mediated interactions between the plant, the endophyte, other microbial colonists and natural enemies.

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.

Rapid and accurate analyses of silicon and phosphorus in plants using a portable X-ray fluorescence spectrometer.

The elemental analysis of plant material is a frequently employed tool across biological disciplines, yet accurate, convenient and economical methods for the determination of some important elements are currently lacking. For instance, digestion-based techniques are often hazardous and time-consuming and, particularly in the case of silicon (Si), can suffer from low accuracy due to incomplete solubilization and potential volatilization, whilst other methods may require large, expensive and specialised equipment. Here, we present a rapid, safe and accurate procedure for the simultaneous, nonconsumptive analysis of Si and phosphorus (P) in as little as 0.1 g dried and ground plant material using a portable X-ray fluorescence spectrometer (P-XRF). We used certified reference materials from different plant species to test the analytical performance of P-XRF and show that the analysis suffers from very little bias and that the repeatability precision of the measurements is as good as or better than that of other methods. Using this technique we were able to process and analyse 200 ground samples a day, so P-XRF could provide a particularly valuable tool for plant biologists requiring the simultaneous nonconsumptive analysis of multiple elements, including those known to be difficult to measure such as Si, in large numbers of samples.

Aboveground-belowground herbivore interactions: a meta-analysis.

Research investigating interactions between aboveground (AG) and below-ground (BG) herbivores has been central to characterizing AG-BG linkages in terrestrial ecosystems, with many of these interactions forming the basis of complex food webs spanning the two subsystems. Despite the growing literature on the effects of AG and BG herbivores on each other, underlying patterns have been difficult to identify due to a high degree of context dependency. In this study, we present the first quantitative meta-analysis of AG and BG herbivore interactions. Previous global predictions, specifically that BG herbivores normally promoted AG herbivore performance and AG herbivores normally reduced BG herbivore performance, were not supported. Instead, the meta-analysis identified four factors that determined the outcome of AG-BG interactions. (1) Sequence of herbivore arrival on host plants was important, with BG herbivores promoting AG herbivore performance only when introduced to the plant simultaneously, whereas AG herbivores had negative effects on BG herbivores only when introduced first. (2) AG herbivores negatively affected BG herbivore survival but tended to increase population growth rates. (3) AG herbivores negatively affected BG herbivore performance on annual plants, but not on perennials, and these effects were observed more consistently in laboratory than field studies. (4) The type of herbivore was also important, with BG insect herbivores belonging to the order Diptera (i.e., true flies) having the strongest negative effects on AG herbivores. Coleoptera (i.e., beetles) species were the most widely investigated BG herbivores and had positive impacts on AG Homoptera (e.g., aphids), but negative effects on AG Hymenoptera (e.g., sawflies). The strongest negative outcomes for BG herbivores were seen when the AG herbivore was a Coleoptera species. We found no evidence for publication bias in AG-BG herbivore interaction literature and conclude that several biological and experimental factors are important for predicting the outcome of AG-BG herbivore interactions. The sequence of herbivore arrival on the host plant was among the most influential.

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.

Interactive effects of plant-available soil silicon and herbivory on competition between two grass species.

BACKGROUND AND AIMS: The herbivore defence system of true grasses (Poaceae) is predominantly based on silicon that is taken up from the soil and deposited in the leaves in the form of abrasive phytoliths. Silicon uptake mechanisms can be both passive and active, with the latter suggesting that there is an energetic cost to silicon uptake. This study assessed the effects of plant-available soil silicon and herbivory on the competitive interactions between the grasses Poa annua, a species that has previously been reported to accumulate only small amounts of silicon, and Lolium perenne, a high silicon accumulator. METHODS: Plants were grown in mono- and mixed cultures under greenhouse conditions. Plant-available soil silicon levels were manipulated by adding silicon to the soil in the form of sodium silicate. Subsets of mixed culture pots were exposed to above-ground herbivory by desert locusts (Schistocerca gregaria). KEY RESULTS: In the absence of herbivory, silicon addition increased biomass of P. annua but decreased biomass of L. perenne. Silicon addition increased foliar silicon concentrations of both grass species >4-fold. Under low soil-silicon availability the herbivores removed more leaf biomass from L. perenne than from P. annua, whereas under high silicon availability the reverse was true. Consequently, herbivory shifted the competitive balance between the two grass species, with the outcome depending on the availability of soil silicon. CONCLUSIONS: It is concluded that a complex interplay between herbivore abundance, growth-defence trade-offs and the availability of soil silicon in the grasses' local environment affects the outcome of inter-specific competition, and so has the potential to impact on plant community structure.

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.

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.

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.

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.

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.