Siliceous and non-nutritious: nitrogen limitation increases anti-herbivore silicon defenses in a model grass

Silicon (Si) accumulation alleviates a diverse array of environmental
stresses in many plants, including conferring physical resistance against
insect herbivores. It has been hypothesised that grasses, in particular,
utilise ‘low metabolic cost’ Si for structural and defensive roles under
nutrient limitation. While carbon (C) concentrations often negatively
correlate with Si concentrations, the relationship between nitrogen (N)
status and Si is more variable. Moreover, the impacts of N limitation on
constitutive physical Si defences (e.g. silica and prickle cells) against
herbivores are unknown. We determined how N limitation affected Si
deposition in the model grass Brachypodium distachyon and how changes in
these constitutive defences impacted insect herbivore (Helicoverpa
armigera) growth rates. We used scanning electron microscopy (SEM) and
energy dispersive X-ray spectrometry in conjunction with X-ray mapping
(XRM) to quantify physical structures on leaves and determine Si
deposition patterns. We also determined how N limitation and Si supply
impacted the jasmonic acid (JA) pathway, the master-regulator of induced
defences against arthropod herbivores. N limitation reduced shoot growth
by over 40%, but increased root mass (+21%), leaf Si concentrations (+50%)
and the density of silica (+28%) and flattened prickle (+76%) cells. EDS
and XRM established that Si was being deposited in these structures,
together with hooked prickle cells and macro-hairs. Herbivore relative
growth rates (RGR) were more than 115% lower in Si supplied plants
compared to plants without Si supply and negatively correlated with leaf
Si concentration and silica cell density. RGR was further reduced by N
limitation and positively correlated with leaf N concentrations. Increases
in JA concentrations following induction of the JA pathway were at least
doubled by N limitation. Si accumulation and deposition were
highly regulated by N availability, with N limitation promoting both
constitutive Si physical defences and induction of the JA defensive
pathway, in line with the resource availability hypothesis. These results
indicate that grasses use ‘low cost Si’ when resources are limited and
suggests that plant productivity may benefit from optimising conventional
fertilisers and Si fertilisation.