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.

Plant silicon application alters leaf alkaloid concentrations and impacts parasitoids more adversely than their aphid hosts.

Grasses accumulate large amounts of silicon (Si) which acts as a highly effective physical defence against insect herbivory, however recent evidence shows that Si supplementation also modifies plant secondary metabolite concetrations. Changes in plant secondary metabolites concentrations can have cascading effects on higher trophic levels, such as parasitoids, as they are dependent on the host herbivore for growth and development. However, relatively little is known about how Si application affects higher trophic levels. We examined the effects of Si addition on alkaloid content in leaves of Phalaris aquatica (Poaceae) and the effect on interactions between an aphid (Rhopalosiphum padi) and its parasitoid (Aphidius colemani). Si supplementation had no effect on aphid abundance or parasitism rate. Adult aphids, aphid mummies (parasitised aphids) and the emergent parasitoids were, however, significantly smaller on Si+ plants. Parasitoid traits (size and emergence) were correlated with aphid mummy size. Si addition reduced parasitoid emergence rate and size due to reduced host mummy size, in addition, significantly fewer females emerged from mummies on Si+ plants. Aphid infestation significantly altered alkaloids concentrations, reducing gramine by 80% while increasing tryptamine by 91% in Si- plants. Si addition reduced aphid-induced tryptamine concentrations by 64% and increased 5-MeO-tryptamine by over 800% in control and 142% in aphid infested plants. Our results show that while Si addition has modest impacts on the herbivore, it significantly alters secondary metabolites and has stronger effects on the higher trophic level through changes in the quality of the parasitised host.

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.

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

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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.

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.

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.

Silicon is an inducible and effective herbivore defence against Helicoverpa punctigera (Lepidoptera: Noctuidae) in soybean.

The role of silicon (Si) in alleviating the effects of biotic and abiotic stresses, including defence against insect herbivores, in plants is widely reported. Si defence against insect herbivores is overwhelmingly studied in grasses (especially the cereals), many of which are hyper-accumulators of Si. Despite being neglected, legumes such as soybean (Glycine max) have the capacity to control Si accumulation and benefit from increased Si supply. We tested how Si supplementation via potassium, sodium or calcium silicate affected a soybean pest, the native budworm Helicoverpa punctigera Wallengren (Lepidoptera: Noctuidae). Herbivory reduced leaf biomass similarly in Si-supplemented (+Si) and non-supplemented (-Si) plants (c. 29 and 23%, respectively) relative to herbivore-free plants. Both Si supplementation and herbivory increased leaf Si concentrations. In relative terms, herbivores induced Si uptake by c. 19% in both +Si and -Si plants. All Si treatments reduced H. punctigera relative growth rates (RGR) to a similar extent for potassium (-41%), sodium (-49%) and calcium (-48%) silicate. Moreover, there was a strong negative correlation between Si accumulation in leaves and herbivore RGR. To our knowledge, this is only the second report of Si-based herbivore defence in soybean; the rapid increase in leaf Si following herbivory being indicative of an induced defence. Taken together with the other benefits of Si supplementation of legumes, Si could prove an effective herbivore defence in legumes as well as grasses.

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.

Alkaloid diversity in the leaves of Australian Flindersia (Rutaceae) species driven by adaptation to aridity.

The genus Flindersia (Rutaceae) comprises 17 species of mostly Australian endemic trees. Although most species are restricted to rainforests, four have evolved to grow in semi-arid and arid environments. In this study, the leaf alkaloid diversity of rainforest and semi-arid/arid zone adapted Australian Flindersia were compared by LC/MS-MS and NMR spectroscopy. Contrary to expectations, Flindersia alkaloid diversity was strongly correlated with environmental aridity, where species predominating in drier regions produced more alkaloids than their wet rainforest congenerics. Rainforest species were also more chemically similar to each other than were the four semi-arid/arid zone species. There was a significant relationship between the presence of alkaloid structural classes and phylogenetic distance, suggesting that alkaloid profiles are influenced by both genetic and environmental factors. The results suggest that the radiation of Flindersia species out of the rainforest and into drier environments has promoted the evolution of unique alkaloid diversity. Plants growing in arid and semi-arid regions of Australia may represent an untapped source of undescribed specialised metabolites.