Plant silicon defence disrupts cryptic colouration in an insect herbivore by restricting carotenoid sequestration into the haemolymph

Abstract

O_LICryptic colouration is a primary anti-predation strategy in herbivorous insects. Achieving crypsis often requires acquiring dietary carotenoids--tetraterpene pigments vital for plant colouration and photoprotection. Silicon (Si) accumulation in plants makes tissues tougher and less digestible for insects, but its effect on plant pigment levels remains unclear. It is also unknown whether feeding on silicified plants impairs insects ability to sequester carotenoids and achieve crypsis. C_LIO_LIUsing the model grass Brachypodium distachyon, we demonstrate that the cotton bollworm (Helicoverpa armigera) larvae exhibited stunted growth and reduced carotenoid sequestration, particularly lutein, into their hemolymph when feeding on Si- supplemented (+Si) plants. This reduction led to distinct body-colour morphs: larvae feeding on +Si plants developed brown colouration, contrasting sharply with the green leaves, whereas larvae feeding on Si-free (-Si) plants exhibited green cryptic colouration that blended seamlessly with the foliage. C_LIO_LIPlant leaves contained various carotenoids (neoxanthin, violaxanthin, {beta}-carotene and lutein) and chlorophylls (a and b), but larvae only sequestered {beta}-carotene and lutein into their haemolymph while excreting substantial amounts of pigments, regardless of plant Si status. Under insect-free conditions, +Si plants had lower carotenoid and chlorophyll contents than -Si plants. However, following insect herbivory, pigment levels in -Si and +Si plants equalised. Insect herbivory also increased Si accumulation in +Si plants. C_LIO_LIOur findings provide novel evidence that plant Si defences can disrupt cryptic colouration in insect herbivores by restricting carotenoid sequestration from host plant tissues. This disruption could increase insect visibility to predators, potentially elevating their risk of predation. C_LI