Leafminer attack induces plant-mediated facilitation of conspecific pupae in the soil

Abstract

O_LIHerbivore population dynamics are strongly influenced by the interactions established through their shared host. Such plant-mediated interactions can occur between different herbivore species and between different life developmental stages of the same herbivore. Yet, whether these interactions occur between leaf-feeding herbivores and their soil-dwelling pupae is unknown. C_LIO_LIWe studied whether tomato (Solanum lycopersicum) leaf-herbivory by the American serpentine leafminer Lyriomiza trifolii affects the performance of conspecific pupae in the soil adjacent to the plant. To gain mechanistic insights, we performed insect bioassays with the jasmonate-deficient tomato mutant def-1 and its wild type, along with the analysis of phytohormones, gene expression and root volatiles. C_LIO_LILeafminer metamorphosis in the soil was accelerated when wild type plants were attacked aboveground by conspecifics, but the opposite was observed in def-1. Changes in pupal developmental rate were mediated by belowground volatiles. Accordingly, leafminer herbivory differentially modulated jasmonate and abscisic acid signaling and the accumulation of specific volatiles in the roots of wild type versus def-1 plants C_LIO_LIOur results demonstrate that aboveground herbivores can facilitate their soil-dwelling pupae by inducing def-1-dependent systemic responses. This study expands the repertoire of plant-herbivore interactions to herbivory-induced modulation of metamorphosis, with potentially important consequences for plant and herbivore community dynamics. C_LI