When resistance is futile, tolerate instead: silicon promotes plant compensatory growth when attacked by above- and belowground herbivores

Abstract

Plants have evolved numerous herbivore defences that are resistance- or tolerance-based. Resistance involves physical and chemical traits that deter and/or harm herbivores whereas tolerance minimizes fitness costs of herbivory, often via compensatory growth. The Poaceae frequently accumulate large amounts of silicon (Si), which can be used for herbivore resistance, including biomechanical and (indirectly) biochemical defences. To date, it is unclear whether Si improves tolerance of herbivory. Here we report how Si enabled a cereal ( Triticum aestivum ) to tolerate damage inflicted by above- and belowground herbivores. Leaf herbivory increased Si concentrations in the leaves by greater than 50% relative to herbivore-free plants, indicating it was an inducible defensive response. In plants without Si supplementation, leaf herbivory reduced shoot biomass by 52% and root herbivory reduced root biomass by 68%. Si supplementation, however, facilitated compensatory growth such that shoot losses were more than compensated for (+14% greater than herbivore-free plants) and root losses were minimized to −16%. Si supplementation did not improve plant resistance since Si did not enhance biomechanical resistance (i.e. force of fracture) or reduce leaf consumption and herbivore relative growth rates. We propose that Si-based defence operates in wheat via tolerance either in addition or as an alternative to resistance-based defence.

Novel evidence for systemic induction of silicon defences in cucumber following attack by a global insect herbivore

“…However, most studies on Si‐based defences have focused on grasses (Hartley et al ., 2016), as they accumulate high concentrations of Si, sometimes over 10% of their dry biomass (hyper‐accumulation) (Hodson et al ., 2005). Given that Si is not only a physical defence but also influences anti‐herbivore phytohormone signalling pathways and thereby chemical defences and enhances plant tolerance to herbivory (Johnson et al ., 2019), Si supplementation is receiving growing recognition in moderate and non‐accumulating plant species (Cooke & Leishman, 2011; Frew et al ., 2019; Johnson et al ., 2020). Only two studies, so far, have reported Si suppressing herbivore performance on cucumber.…”

“…Recent evidence suggests that JA signalling induces Si uptake when plants experience herbivore attack (Hall et al ., 2019, 2020). While a few studies have shown Si induction in plants under insect herbivory, all of them have focused on hyper‐accumulating grasses (Massey et al ., 2007; Hall et al ., 2019; Johnson et al ., 2019), except one study on soybean (Johnson et al ., 2020). As such, we have little data on the extent of Si induction by insect herbivores across different Si accumulating species and no data across plant genotypes within a species (Hartley et al ., 2016).…”

Lineage and latitudinal variation in Phragmites australis tolerance to herbivory: implications for invasion success

“…For example, phenolics are involved in lignin synthesis (Bhattacharya et al ) and silica is thought to provide similar structural support as lignin at a much lower metabolic cost (Raven ). Although silica content has been reported as a defensive compound (Massey et al , Soininen et al ), there is growing support for its role as a buffer of biotic and abiotic stress to plants (Coskun et al ) and as a promoter of tolerance to herbivory (Johnson et al ). Populations investing in structural integrity also invested in belowground biomass storage, which is widely regarded as a putative tolerance trait (Strauss and Agrawal , Tiffin , de Jong and Lin , Lurie et al ).…”

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

“…While the negative impacts of herbivory on leaf biomass were not lessened with Si supplementation over the 6 days of herbivore exposure in the current study, it remains possible that this would have occurred as more Si was accumulated. Alternatively, Si-supplemented plants may have been able to tolerate the relatively lower levels of herbivory imposed by smaller herbivores on +Si plants (Johnson et al ., 2019). Having established the potential for Si defences in soybean in the current study, longer term experiments involving measurements of flowering, yield and nitrogen fixation would be useful to determine if these defences are truly beneficial for crop protection.…”