Increased root herbivory under elevated atmospheric carbon dioxide concentrations is reversed by silicon‐based plant defences

Abstract

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.

Silicon‐induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance

“…) and invertebrate herbivores (Keeping & Meyer ; Massey, Ennos & Hartley ; Frew et al . ). Silicon negatively affects herbivores via abrasive effects on herbivore mouthparts (Massey & Hartley ; but see Kvedaras et al .…”

“…In addition to promoting plant growth, silicon deposition in plant tissues has been shown to be an effective defence against both vertebrate Wieczorek et al 2015) and invertebrate herbivores (Keeping & Meyer 2006;Massey, Ennos & Hartley 2006;Frew et al 2017). Silicon negatively affects herbivores via abrasive effects on herbivore mouthparts (Massey & Hartley 2009; but see Kvedaras et al 2009), reduced digestive efficiency (Massey, Ennos & Hartley 2006;Wieczorek et al 2015) and induction of secondary metabolites (Reynolds, Keeping & Meyer 2009), which can include metabolites involved in indirect defences (e.g.…”

Silicon application promotes rice growth and negatively affects development of Spodoptera frugiperda (J. E. Smith)

“…Positive responses resulting from Si application are attributed to Si deposition in plant epidermal cells, which promotes mechanical defence (Massey & Hartley, ). In addition, Si‐based resistance is reported to be associated with the production of defensive substances such as oxidative enzymes, phytoalexins, lignin and suberin, compounds that are intimately related to plant resistance against pathogen infection and herbivore attack both above‐ (Han et al., ; Ma & Yamaji, ) and belowground (Frew, Allsopp, Gherlenda, & Johnson, ). Finally, Si was reported to alleviate the negative abiotic effects of salinity (Liu et al., ), drought (Chen, Yao, Cai, & Chen, ) and heavy metal toxicity (Farooq, Detterbeck, Clemens, & Dietz, ) in plants.…”

Biogenic silica accumulation varies across tussock tundra plant functional type

“…Terrestrial plants take up dissolved silica (DSi) from surrounding soil solution via their roots, transport it in solution via the xylem, and deposit it as biogenic silica (BSi), an amorphous form of silica, most commonly in roots and transpiration termini (e.g. leaves) (Epstein, 1994;Frew, Allsopp, Gherlenda, & Johnson, 2016;Raven, 2003). Silica uptake by land plants, known as the terrestrial silica pump, represents a major component of the global silica cycle, equal to roughly one-third that of diatoms in the ocean (Carey & Fulweiler, 2012a).…”