Silicon is often regarded as a plant nutritional 'non-entity'. A suite of factors associated with Si have been recently identified, relating to plant chemistry, physiology, gene regulation and interactions with other organisms. Research to date has typically focused on the impact of Si application upon plant stress responses. However, the fundamental, underlying mechanisms that account for the manifold effects of Si in plant biology remain undefined. Here, the known effects of Si in higher plants relating to alleviation of both abiotic and biotic stress are briefly reviewed and the potential importance of Si in plant primary metabolism is discussed, highlighting the need for a unifying research framework targeting common underlying mechanisms. The traditional approach of discipline-specific work on single stressors in individual plant species is currently inadequate. Thus, a holistic and comparative approach is proposed to assess the mode of action of Si between plant trait types (e.g. C3, C4 and CAM; Si accumulators and non-accumulators) and between biotic and abiotic stressors (pathogens, herbivores, drought, salt), considering potential pathways (i.e. primary metabolic processes) highlighted by recent empirical evidence. Utilizing genomic, transcriptomic, proteomic and metabolomic approaches in such comparative studies will pave the way for unification of the field and a deeper understanding of the role of Si in plants.
Phenolic compounds play a role in plant defense against herbivores. For some herbivorous insects, particularly root herbivores, host plants with high phenolic concentrations promote insect performance and tissue consumption. This positive relationship between some insects and phenolics, however, could reflect a negative correlation with other plant defenses acting against insects. Silicon is an important element for plant growth and defense, particularly in grasses, as many grass species take up large amounts of silicon. Negative impact of a high silicon diet on insect herbivore performance has been reported aboveground, but is unreported for belowground herbivores. It has been hypothesized that some silicon accumulating plants exhibit a trade-off between carbon-based defense compounds, such as phenolics, and silicon-based defenses. Here, we investigated the impact of silicon concentrations and total phenolic concentrations in sugarcane roots on the performance of the root-feeding greyback canegrub (Dermolepida albohirtum). Canegrub performance was positively correlated with root phenolics, but negatively correlated with root silicon. We found a negative relationship in the roots between total phenolics and silicon concentrations. This suggests the positive impact of phenolic compounds on some insects may be the effect of lower concentrations of silicon compounds in plant tissue. This is the first demonstration of plant silicon negatively affecting a belowground herbivore.
Herbivorous insect pests living in the soil represent a significant challenge to food security given their persistence, the acute damage they cause to plants and the difficulties associated with managing their populations. Ecological research effort into rhizosphere interactions has increased dramatically in the last decade and we are beginning to understand, in particular, the ecology of how plants defend themselves against soil-dwelling pests. In this review, we synthesise information about four key ecological mechanisms occurring in the rhizosphere or surrounding soil that confer plant protection against root herbivores. We focus on root tolerance, root resistance via direct physical and chemical defences, particularly via acquisition of siliconbased plant defences, integration of plant mutualists (microbes and entomopathogenic nematodes, EPNs) and the influence of soil history and feedbacks. Their suitability as management tools, current limitations for their application, and the opportunities for development are evaluated. We identify opportunities for synergy between these aspects of rhizosphere ecology, such as mycorrhizal fungi negatively affecting pests at the root-interface but also increasing plant uptake of silicon, which is also known to reduce herbivory. Finally, we set out research priorities for developing potential novel management strategies. Re: Revision of our review APSOIL-D-16-00199 Dear Prof van Gestel, Many thanks for your email advising us that our paper may be considered for publication pending major revisions. Please find enclosed our revised article New frontiers in belowground ecology for plant protection from root-feeding insects. As you will see this paper has been substantially rewritten and developed. Full details of these changes are in our response to reviewers. We are thankful to both reviewers for constructive comments and suggestions. We are grateful for the extension you provided and very sorry that we were late returning this revision to you. Please don't hesitate to contact me if I can provide further information.
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 anti-herbivore 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.
/0000-0002-5117-687X, Johnson, Scott N., Ryalls, James M. W. et al. (4 more authors) (2017) Silicon-induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance. Functional Ecology.
Summary Predicted increases in atmospheric concentrations of CO2 may alter the susceptibility of many plants to insect herbivores due to changes in plant nutrition and defences. Silicon plays a critical role in plant defence against herbivores, so increasing such silicon‐based defences in plants may help remediate situations where plants become more susceptible to herbivores. Sugar cane (Saccharum spp. hybrid) was subjected to fully factorial treatment combinations of ambient (aCO2) or elevated (eCO2) atmospheric CO2 concentrations; ambient silicon or silicon supplementation; insect‐free or subject to root herbivory by greyback canegrub (Dermolepida albohirtum). A glasshouse study was used to determine how these factors affected rates of photosynthesis, growth, chemistry (concentrations of silicon, carbon, nitrogen and non‐structural carbohydrates). Changes in canegrub mass were determined in the glasshouse pot study, together with more detailed assessment of how eCO2 and silicon supplementation affected performance and feeding behaviour (relative growth rate and relative consumption) in a 24‐h feeding efficiency assay. Elevated CO2 and silicon supplementation increased rates of photosynthesis (+32% and 14%, respectively) and sugar cane biomass (+45% and 69%, respectively). Silicon supplementation increased silicon concentrations in both leaves and roots by 54% and 75%, respectively. eCO2 caused root C : N to increase by 12%. Canegrub performance and consumption increased under eCO2; relative growth rate (RGR) increased by 116% and consumed 57% more root material (suggestive of compensatory feeding). Silicon application reversed these effects, with large decreases in mass change, RGR and root consumption (65% less root mass consumed). Synthesis and applications. Our results suggest future atmospheric carbon dioxide concentrations could lead to increased crop damage by a below‐ground herbivore. Increasing bioavailable silicon in soil stimulated silicon‐based defences which dramatically decreased herbivory and herbivore performance. Our findings suggest future pest management strategies could benefit from characterising deficiencies in bioavailable silicon in agricultural soils and targeted application of silicon fertilisers. Moreover, future breeding programmes should exploit variation in silicon uptake between cultivars to enhance silicon uptake in new crop varieties. Silicon‐based plant defence proved to be highly beneficial for remediating the negative effects of atmospheric change on sugar cane susceptibility to herbivory and could be applicable in other crops.
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