Trichome acylsugar defenses are equally effective against leaf-mining and free-living insects

Trichomes, epidermal projections, are crucial components of plant defense systems. Whether these epidermal defenses are effective against leafminers, which infest the internal mesophyll layers, remains unclear. Using the devastating invasive tomato pest, Phthorimaea absoluta (tomato leafminer), and the trichome-rich wild tomato, Solanum pennellii, we demonstrate that trichome-produced acylsugars effectively inhibit the growth of endophagous P. absoluta larvae feeding inside leaves. High-spatial-resolution leaf- and frass-metabolite analysis by matrix-assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) and stimulated Raman scattering microscopy revealed that trichome-synthesized acylsugars are translocated into the mesophyll tissues when larvae infest leaves. We identified an ATP-binding cassette (ABC) transporter, SpABCB5, as the mediator of this translocation and as an essential component of defense against leafminers. These data reveal that epidermal trichomes not only defend against free-living (ectophagous) herbivores through direct contact or rapid deposition of chemical defenses onto leaf surfaces but also defend against endophagous leafminers by rapidly depositing chemical defenses into internal tissues. By delivering mines against leafminers, trichomes offer new avenues for breeding crops with resistance to leafminers.