Nanosilica supplementation in tomato increases oviposition on stems and caterpillar mortality in the tomato pinworm

Abstract

Silicon-induced responses play a key role in plant defense against herbivory, though the underlying mechanisms remain underexplored. In this study, we examined how mesoporous silica nanoparticles (MSNs) affect tomato (Solanum lycopersicum) defense against an invasive and highly destructive lepidopteran herbivore, the tomato pinworm (TPW), Phthorimaea absoluta. In tomato plants supplemented with MSN, prior exposure to TPW oviposition shifted subsequent egg-laying from a preference for leaves to an even distribution between stems and leaves. This shift was not observed in nonsilicon-supplemented plants. Prolonged oviposition triggered pigmentation in the basal cells of type I glandular trichomes on the stems of silicon-supplemented plants. Chemical analysis by coupled gas chromatography-mass spectrometry revealed that the pigmented trichome was rich in soluble sugars (sucrose and l-arabinose) and waxes, dominated by the saturated hydrocarbon tetracosane. Bioassays with the crude extract of the pigmented trichome and a three-component sugar–wax blend replicated the oviposition and caterpillar response observed with the pigmented trichome, while individual components produced variable effects. While l-arabinose alone replicated the oviposition effects of the three-component sugar–wax blend, sucrose increased oviposition and caterpillar feeding and survival, while l-arabinose and tetracosane caused the highest caterpillar mortality. Additionally, these treatments altered caterpillar gut microbiota composition and influenced frass volatiles, which attracted the TPW natural enemies, Nesidiocoris tenuis (predator) and Neochrysocharis formosa (parasitoid). Our findings suggest that silicon supplementation increases tomato defense against TPW through oviposition-induced responses, which promotes recruitment of natural enemies.

SIGNIFICANCE : Plants utilize physical and biochemical defenses to protect themselves from herbivores, yet the role of nonnutritional components like mesoporous silica nanoparticles (MSNs) in plant–herbivore interactions is not well understood. In this study, we explored silicon-mediated defenses in tomato plants against the tomato pinworm (TPW), a major agricultural pest. Supplementation with MSNs enhanced biochemical defenses in tomato trichomes, a key site of plant–herbivore interaction. TPW females are attracted to MSN-enriched trichomes for egg-laying on stems, but caterpillars that hatch and consume the trichomes experience high mortality, reducing pest survival and minimizing plant damage. Additionally, silicon supplementation indirectly strengthens plant defenses by altering volatile organic compound (VOC) emissions in caterpillar frass, which attract the TPW natural enemies Nesidiocoris tenuis (predator) and Neochrysocharis formosa (parasitoid). These results suggest that MSN supplementation could be an effective crop protection strategy, enhancing plant resilience and promoting the recruitment of natural enemies.