Leafminer attack accelerates the development of soil‐dwelling conspecific pupae via plant‐mediated changes in belowground volatiles

Abstract

Summary Herbivore population dynamics are strongly influenced by the interactions established through their shared host. Such plant‐mediated interactions can occur between different herbivore species and different life developmental stages of the same herbivore. However, whether these interactions occur between leaf‐feeding herbivores and their soil‐dwelling pupae is unknown. We studied whether tomato (Solanum lycopersicum) leaf herbivory by the American serpentine leafminer Liriomyza trifolii affects the performance of conspecific pupae exposed to the soil headspace of the plant. To gain mechanistic insights, we performed insect bioassays with the jasmonate‐deficient tomato mutant def‐1 and its wild‐type, along with phytohormones, gene expression and root volatiles analyses. Belowground volatiles accelerated leafminer metamorphosis when wild‐type plants were attacked aboveground by conspecifics. The opposite pattern was observed for def‐1 plants, in which aboveground herbivory slowed metamorphosis. Leafminer attack induced jasmonate and abscisic acid accumulation and modulated volatile production in tomato roots in a def‐1‐dependent manner. Our results demonstrate that aboveground herbivory triggers changes in root defence signalling and expression, which can directly or indirectly via changes in soil or microbial volatiles, alter pupal development time. This finding expands the repertoire of plant–herbivore interactions to herbivory‐induced modulation of metamorphosis, with potential consequences for plant and herbivore community dynamics.

The benzoxazinoid breakdown product 5-Methoxy-2-Nitrophenol has a dual function in maize defense against herbivory

“…Two distinct methods were employed to determine (relative) amounts of 5M2NP in maize tissues. SPME-GC-MS, as outlined in Escobar-Bravo et al (2022b), was used as the standard method. Samples were aliquoted from ground frozen homogenized plant material (roots: 90-110 mg, leaves: 10-20 mg) prior to analysis.…”

“…Samples were aliquoted from ground frozen homogenized plant material (roots: 90-110 mg, leaves: 10-20 mg) prior to analysis. Note that this method involves incubating individual samples at 50°C for 40 min to collect VOCs (Escobar-Bravo et al, 2022b). 5M2NP identification was based on similarity to NIST14 MS Library matches (NIST, Gaithersburg, MD, USA), plus comparisons with mass spectra and retention times of commercially available methoxy-nitrophenols (Supporting Information Fig.…”

High-resolution kinetics of herbivore-induced plant volatile transfer reveal clocked response patterns in neighboring plants

“…A new set of plants was used for each time point. Analysis of foliar terpene pools was conducted using slightly modified, previously described, methods [44]. In brief, ca.…”

Belowground insect herbivory induces systemic volatile emissions that strengthen neighbouring plant resistance aboveground

“…Changes in systemic HIPV emissions can alter plant interactions with other members of their ecological communities (Barber et al, 2015; Huang et al, 2017). For example, aboveground herbivory induces systemic HIPV emissions from roots, which modify belowground insect herbivore foraging (Robert et al, 2012) and development (Escobar‐Bravo et al, 2022). Relatedly, belowground herbivory can modulate systemic HIPV emissions from leaves that affect the foraging behaviours of aboveground herbivores (Sun et al, 2019) and natural enemies (Soler et al, 2007).…”