Silicon fertilisation affects morphological and immune defences of an insect pest and enhances plant compensatory growth

Herbivorous insects have evolved various anti-predator defences, including morphological, behavioural, and immune defences, which can make biocontrol of herbivorous pests challenging. Silicon (Si) accumulation in plants is a potent physical defence against mandibulate insects. However, it remains uncertain how Si affects the anti-predator defences of insect herbivores and plant defences following herbivory. We grew the model grass, Brachypodium distachyon, hydroponically with (+Si) or without (–Si) Si and investigated the plant-mediated effects of Si on the anti-predator defences of the cotton bollworm, Helicoverpa armigera, integrating morphological (i.e. integument resistance and thickness), behavioural, and immune defences. We also examined the effects of Si on plant compensatory growth and leaf trichome production. Larval growth, leaf consumption, and integument resistance were lower when feeding on +Si plants compared to when feeding on –Si plants. Larval integument thickness, defensive behaviours, haemocyte density, and lysozyme-like activity in the haemolymph were unaffected by Si. Larvae fed on +Si plants had higher haemolymph phenoloxidase (PO) and total-PO activities than larvae fed on –Si plants, although this did not enhance the melanisation response of larvae. Furthermore, Si supplies increased plant compensation for herbivory and constitutive trichome production, whereas herbivory induced trichome production only on –Si plants. We provide the first evidence for plant-mediated effects of Si on anti-predator defences of an insect herbivore. We suggest that the lower integument resistance of larvae when feeding on Si-supplemented plants could contribute to their vulnerability to natural enemies and that high PO activity may impose fitness costs (e.g. delayed development)

Elevated atmospheric CO2 triggers compensatory feeding by root herbivores on a C3 but not a C4 grass

Predicted increases in atmospheric carbon dioxide (CO2) concentrations often reduce nutritional quality for herbivores by increasing the C:N ratio of plant tissue. This frequently triggers compensatory feeding by aboveground herbivores, whereby they consume more shoot material in an attempt to meet their nutritional needs. Little, however, is known about how root herbivores respond to such changes. Grasslands are particularly vulnerable to root herbivores, which can collectively exceed the mass of mammals grazing aboveground. Here we provide novel evidence for compensatory feeding by a grass root herbivore, Sericesthis nigrolineata, under elevated atmospheric CO2 (600 mmol mol21) on a C3 (Microlaena stipoides) but not a C4 (Cymbopogon refractus) grass species. At ambient CO2 (400 mmol mol21) M. stipoides roots were 44% higher in nitrogen (N) and 7% lower in carbon (C) concentrations than C. refractus, with insects performing better on M. stipoides. Elevated CO2 decreased N and increased C:N in M. stipoides roots, but had no impact on C. refractus roots. Root-feeders displayed compensatory feeding on M. stipoides at elevated CO2, consuming 118% more tissue than at ambient atmospheric CO2. Despite this, root feeder biomass remained depressed by 24%. These results suggest that compensatory feeding under elevated atmospheric CO2 may make some grass species particularly vulnerable to attack, potentially leading to future shifts in the community composition of grasslands

Increased insect herbivore performance under elevated CO2 is associated with lower plant defence signalling and minimal declines in nutritional quality

Changes in insect herbivore performance under elevated atmosphere carbon dioxide concentrations e[CO2] are often driven by changes in the nutritional and defensive chemistry of their host plants. Studies addressing how the prolific pest cotton bollworm (Helicoverpa armigera) responds to e[CO2] show that performance usually declines, often associated with lower nutritional (e.g. nitrogen (N) concentrations) quality of host plants under e[CO2]. We investigated the impacts of e[CO2] on nutritional quality and anti-herbivore (jasmonate) defensive signalling in lucerne (Medicago sativa) when challenged by H. armigera. While foliar N decreased under e[CO2], other aspects of nutritional quality (soluble protein, amino acids, foliar C:N) were largely unaffected, potentially due to increased root nodulation under e[CO2]. In contrast, e[CO2] greatly reduced jasmonate signalling in M. sativa following H. armigera attack; jasmonic acid concentrations were ca. 56% lower in attacked plants grown under e[CO2]. Concurrent with this, relative growth rates of H. armigera were ca. 66% higher when feeding on e[CO2]-grown plants. In contrast with previous reports, which we meta-analytically summarise, we provide the first evidence that H. armigera performance can increase under e[CO2]. This may occur in plants, such as M. sativa, where e[CO2] has limited impacts on nutritional quality yet reduces jasmonate defence signalling. Note: An Author Correction to this article was published on 07 December 2020. The PDF available here includes the correction appended to the original

Aphid feeding induces phytohormonal cross-talk without affecting silicon defense against subsequent chewing herbivores

Prior feeding by insect herbivores frequently affects plant quality for herbivores that subsequently feed on the plant. Facilitation occurs when one herbivore improves plant quality for other herbivores, including when the former compromises plant defenses. Silicon (Si) is an important defense in grasses that increases following activation of the jasmonic acid (JA) pathway. Given that aphids often stimulate the salicylic acid (SA) pathway, we hypothesized that this could reduce Si defense because of the well documented antagonistic cross-talk between SA and JA. We tested this in the model grass Brachypodium distachyon with and without Si (+Si and −Si, respectively); half of the plants were exposed to aphids (Rhopalosiphum padi) and half remained aphid-free. Aphid-free and aphid-exposed plants were then fed to chewing herbivores (Helicoverpa armigera). Aphids triggered higher SA concentrations which suppressed JA concentrations but this did not affect foliar Si. Chewing herbivores triggered higher JA concentrations and induced Si uptake, regardless of previous feeding by aphids. Chewer growth rates were not impacted by prior aphid herbivory but were reduced by 75% when feeding on +Si plants. We concluded that aphids caused phytohormonal cross-talk but this was overridden by chewing herbivory that also induced Si uptake

Field application of silicon alleviates drought stress and improves water use efficiency in wheat

Detrimental impacts of drought on crop yield have tripled in the last 50 years with climate models predicting that the frequency of such droughts will intensify in the future. Silicon (Si) accumulation, especially in Poaceae crops such as wheat (Triticum aestivum L.), may alleviate the adverse impacts of drought. We have very limited information, however, about whether Si supplementation could alleviate the impacts of drought under field conditions and no studies have specifically manipulated rainfall. Using field–based rain exclusion shelters, we determined whether Si supplementation (equivalent to 39, 78 and 117 kg ha-1) affected T. aestivum growth, elemental chemistry [Si, carbon (C) and nitrogen (N)], physiology (rates of photosynthesis, transpiration, stomatal conductance, and water use efficiency) and yield (grain production) under ambient and drought (50% of ambient) rainfall scenarios. Averaged across Si treatments, drought reduced shoot mass by 21% and grain production by 18%. Si supplementation increased shoot mass by up to 43% and 73% in ambient and drought water treatments, respectively, and restored grain production in droughted plants to levels comparable with plants supplied with ambient rainfall. Si supplementation increased leaf-level water use efficiency by 32–74%, depending on Si supplementation rates. Water supply and Si supplementation did not alter concentrations of C and N, but Si supplementation increased shoot C content by 39% and 83% under ambient and drought conditions, respectively. This equates to an increase from 6.4 to 8.9 tonnes C ha-1 and from 4.03 to 7.35 tonnes C ha-1 under ambient and drought conditions, respectively. We conclude that Si supplementation ameliorated the negative impacts of drought on T. aestivum growth and grain yield, potentially through its beneficial impacts on water use efficiency. Moreover, the beneficial impacts of Si on plant growth and C storage may render Si supplementation a useful tool for both drought mitigation and C sequestration

Silicon accumulation suppresses arbuscular mycorrhizal fungal colonisation in the model grass Brachypodium distachyon

Purpose Silicon (Si) accumulation by grasses alleviates diverse biotic and abiotic stresses. Despite this important functional role, we have limited understanding of how root microbial symbionts, such as arbuscular mycorrhizal (AM) fungi, affect Si uptake and even less about how Si supply and accumulation affect AM fungal colonisation. Our objective was to determine the nature of this two–way interaction in the model grass, Brachypodium distachyon. Methods We grew B. distachyon with five levels of Si supplementation using wild-type plants and a mutant (Bdlsi1-1) that has little capacity for Si uptake. Half of the plants were colonised by AM fungi; half were free of AM fungi. We measured Si accumulation, AM fungal colonisation, leaf carbon (C), nitrogen (N) and phosphorus (P) concentrations. Results AM fungi did not affect Si accumulation, although small increases occurred when root mass was included as a covariate. Si supplemented soil promoted plant growth and P uptake. Si accumulation suppressed colonisation by AM fungi and C concentrations in wild type but not in Bdlsi1-1 plants. Si concentrations were negatively correlated with C and N concentrations, with correlations being stronger in wild-type plants than Bdlsi1-1 plants. Conclusions Our results indicate that Si accumulation in the plant, rather than Si availability in the soil, underpinned reduced AMF colonisation. We propose that Si accumulation is unlikely to be impacted by AM fungi in plants with inherently high Si accumulation, but Si accumulation may suppress AM fungal colonisation in such plants

Silicon alters leaf surface morphology and suppresses insect herbivory in a model grass species

Grasses accumulate large amounts of silicon (Si) which is deposited in trichomes, specialised silica cells and cell walls. This may increase leaf toughness and reduce cell rupture, palatability and digestion. Few studies have measured leaf mechanical traits in response to Si, thus the effect of Si on herbivores can be difficult to disentangle from Si-induced changes in leaf surface morphology. We assessed the effects of Si on Brachypodium distachyon mechanical traits (specific leaf area (SLA), thickness, leaf dry matter content (LDMC), relative electrolyte leakage (REL)) and leaf surface morphology (macrohairs, prickle, silica and epidermal cells) and determined the effects of Si on the growth of two generalist insect herbivores (Helicoverpa armigera and Acheta domesticus). Si had no effect on leaf mechanical traits; however, Si changed leaf surface morphology: silica and prickle cells were on average 127% and 36% larger in Si supplemented plants, respectively. Prickle cell density was significantly reduced by Si, while macrohair density remained unchanged. Caterpillars were more negatively affected by Si compared to crickets, possibly due to the latter having a thicker and thus more protective gut lining. Our data show that Si acts as a direct defence against leaf-chewing insects by changing the morphology of specialised defence structures without altering leaf mechanical traits

Uptake of silicon in barley under contrasting drought regimes

Purpose: Silicon (Si) accumulation in plant tissues plays a vital role in alleviating biotic and abiotic stresses, including drought. Temperate regions are predicted to experience reductions in the quantity and frequency of rainfall events, potentially impacting plant Si uptake via the transpiration stream. Despite the importance for predicting plant responses to Si amendments, the effects of changes in rainfall patterns on Si uptake in cereals have not been characterised. Methods: Five watering regimes were applied based on predicted precipitation scenarios, varying the quantity of water delivered (ambient, 40% or 60% reduction) and watering frequency (40% reduction in quantity, applied 50% or 25% of ambient frequency), and the effects on growth and leaf Si concentrations of a barley landrace and cultivar were determined. Results: Reductions in the quantity of water reduced plant growth and yield, whereas reducing the watering frequency had little impact on growth, and in some cases partially ameliorated the negative effects of drought. Reductions in quantity of water lowered leaf Si concentrations in both the cultivar and landrace, although this effect was alleviated under the drought/deluge watering regime. The landrace had greater leaf Si concentration than the cultivar regardless of watering regime, and under ambient watering deposited Si in all cells between trichomes, whereas the cultivar exhibited gaps in Si deposition. Conclusion: The impact of future reductions in rainfall on barley productivity will depend upon how the water is delivered, with drought/deluge events likely to have smaller effects on yield and on Si uptake than continuous drought

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

Elevated atmospheric CO2 suppresses silicon accumulation and exacerbates endophyte reductions in plant phosphorus

Many temperate grasses are both hyper-accumulators of silicon (Si) and hosts of Epichloë fungal endophytes, functional traits which may alleviate environmental stresses such as herbivore attack. Si accumulation and endophyte infection may operate synergistically, but this has not been tested in a field setting, nor in the context of changing environmental conditions. Predicted increases in atmospheric CO2 concentrations can affect both Si accumulation and endophyte function, but these have not been studied in combination. We investigated how elevated atmospheric CO2 (eCO2), Si supplementation, endophyte-presence and insect herbivory impacted plant growth, stoichiometry (C, N, P and Si), leaf gas exchange (rates of photosynthesis, stomatal conductance, transpiration rates) and endophyte production of anti-herbivore defences (alkaloids) of an important pasture grass (tall fescue; Lolium arundinaceum) in the field. eCO2 and Si supplementation increased shoot biomass (+52% and +31%, respectively), whereas herbivory reduced shoot biomass by at least 35% and induced Si accumulation by 24%. Shoot Si concentrations, in contrast, decreased by 17%–21% under eCO2. Si supplementation and herbivory reduced shoot C concentrations. eCO2 reduced shoot N concentrations which led to increased shoot C:N ratios. Overall, shoot P concentrations were 26% lower in endophytic plants compared to non-endophytic plants, potentially due to decreased mass flow (i.e. observed reductions in stomatal conductance and transpiration). Alkaloid production was not discernibly affected by any experimental treatment. The negative impacts of endophytes on P uptake were particularly strong under eCO2. We show that eCO2 and insect herbivory reduce and promote Si accumulation, respectively, incorporating some field conditions for the first time. This indicates that these drivers operate in a more realistic ecological context than previously demonstrated. Reduced uptake of P in endophytic plants may adversely affect plant productivity in the future, particularly if increased demand for P due to improved plant growth under eCO2 cannot be met. Read the free Plain Language Summary for this article on the Journal blog. © 2023 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society