Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (Plutella xylostella) to evaluate changes in fitness, and additionally examined the effects on a predatory lacewing (Chrysoperla carnea). Silencing glucosinolate sulfatase genes resulted in the systemic accumulation of toxic isothiocyanates in P. xylostella larvae, impairing larval development and adult reproduction. The predatory lacewing C. carnea, however, efficiently degraded ingested isothiocyanates via a general conjugation pathway, with no negative effects on survival, reproduction, or even prey preference. These results illustrate how plant defenses and their detoxification strongly influence herbivore fitness but might only subtly affect a third trophic level.

Plant chemical defences impact not only herbivores, but also organisms in higher trophic levels that prey on or parasitize herbivores. While herbivorous insects can often detoxify plant chemicals ingested from suitable host plants, how such detoxification affects endoparasitoids that use these herbivores as hosts is largely unknown. Here, we used transformed plants to experimentally manipulate the major detoxification reaction used by Plutella xylostella (diamondback moth) to deactivate the glucosinolate defences of its Brassicaceae host plants. We then assessed the developmental, metabolic, immune, and reproductive consequences of this genetic manipulation on the herbivore as well as its hymenopteran endoparasitoid Diadegma semiclausum. Inhibition of P. xylostella glucosinolate metabolism by plant‐mediated RNA interference increased the accumulation of the principal glucosinolate activation products, the toxic isothiocyanates, in the herbivore, with negative effects on its growth. Although the endoparasitoid manipulated the excretion of toxins by its insect host to its own advantage, the inhibition of herbivore glucosinolate detoxification slowed endoparasitoid development, impaired its reproduction, and suppressed the expression of genes of a parasitoid‐symbiotic polydnavirus that aids parasitism. Therefore, the detoxification of plant glucosinolates by an herbivore lowers its toxicity as a host and benefits the parasitoid D. semiclausum at multiple levels.

Beauveria bassiana is a soil fungus that parasitizes a large number of arthropod species, including numerous crop pests, causing white muscardine disease and is therefore used as a biological insecticide. However, some insects, such as the cabbage aphid (Brevicoryne brassicae), defend themselves chemically by sequestering dietary pro-toxins (glucosinolates) from their Brassicales host plants. Glucosinolates are accumulated by cabbage aphids and activated to form toxic isothiocyanates when under attack. While isothiocyanate formation protects aphids against most attackers, B. bassiana is still able to infect the cabbage aphid under natural conditions. We therefore investigated how this fungus is able to circumvent the chemical defense system of the cabbage aphid. Here, we describe how B. bassiana infection activates the cabbage aphid defense system, but the resulting toxins are metabolized by B. bassiana via the mercapturic acid pathway, of which the first step is catalyzed by glutathione-S-transferases of low substrate specificity. This detoxification pathway enhances B. bassiana growth when isothiocyanates are present in natural concentrations, and so appears to be an important factor in fungal parasitization of these chemically defended aphids.

The cabbage aphidBrevicoryne brassicaeis a notorious agricultural pest that specializes on plants of the Brassicaceae family, which are chemically defended by glucosinolates. By sequestering glucosinolates from its host plants and producing its own activating enzyme (myrosinase), this aphid employs a self-defense system against enemies paralleling that in plants. However, we know little about the metabolic fate of individual glucosinolates during aphid sequestration and activation and about the biochemical effects of this defense on aphid enemies. Here, we probed these questions focusing onB. brassicaeand a predatory lacewing,Chrysoperla carnea. We found that distinct glucosinolates were accumulated byB. brassicaeat different rates, with aliphatic glucosinolates being taken up more quickly than indolic ones.B. brassicaemyrosinase enzymatic activities toward different glucosinolates were strongly correlated to their rates of accumulation in vivo. Surprisingly, after simulated predation, the production of toxic isothiocyanate products (ITCs) was quantitatively outweighed by less toxic products such as nitriles and ITC-conjugates. Nevertheless, the defensive cocktails significantly impairedC. carneadevelopment.Tissue-specific quantification of glucosinolate metabolites revealed that the lacewings employ both conjugation and mobilization to reduce the toxicity of aliphatic ITCs, but these strategies were only partially effective. These results clarify the metabolic fates of glucosinolates after sequestration by an aphid herbivore and further in a higher trophic level, as well as the consequences for predator survival and development, and might be instructive for integrative pest management approaches targeting the cabbage aphid.

Brassicales plants defend themselves with glucosinolates that, upon herbivory, are hydrolyzed into toxic isothiocyanates (ITCs) and other derivatives. The side chain diversity of glucosinolates results in a range of structurally distinct products, but how this chemical variation affects herbivores and their detoxification responses remains incompletely understood. Here, we show the effects of ITC hydrolysis products with various side chains on Spodoptera littoralis larvae and their detoxification system. ITCs inhibit larval growth to varying degrees, depending on the chemical nature of their side chain. The larvae metabolize ITCs by conjugating them to glutathione in the mercapturic acid pathway and to lysine forming an amine conjugate. Over half of the 34 S. littoralis glutathione-S-transferases (GSTs), tested as His-tagged derivatives, actively conjugate ITCs, with most catalyzing reactions with multiple substrates. Larval performance on various ITC-containing diets correlates positively with GST activity, highlighting this detoxification system’s role in supporting growth on glucosinolate-containing plants. The propensity of multiple GSTs to react with an individual ITC and the wide expression of GST-encoding genes across larval organs likely promote the ability of this generalist herbivore to thrive on glucosinolate-defended Brassicales plants. These findings provide insight into herbivore adaptation and may inform future research on plant–insect interactions.

After consumption by herbivores, plant antimicrobial defense compounds may enhance herbivore immunity to pathogenic microbes. In conifer-bark beetle interactions, beetles ingest large quantities of phloem tissue containing high concentrations of antimicrobial phenolic glucosides, such as stilbenes and flavonoids. It is not known, however, if these compounds increase bark beetle resistance to pathogens. We showed that Eurasian spruce bark beetles ( Ips typographus ) attacking Norway spruce ( Picea abies ) hydrolyze phenolic glucosides to their corresponding aglucones increasing their antifungal activity. However, the entomopathogen Beauveria bassiana , a natural fungal parasite of these beetles, detoxifies stilbene and flavonoid aglucones by forming methylglucoside derivatives. A two-step pathway involving a UDP-glycosyltransferase and an O -methyltransferase produces phenolic O -methylglucosides that are no longer toxic to B. bassiana and are stable to β-glucosidase action. Compared to wild-type strains of B. bassiana , mutant strains knocked out in the genes of this pathway exhibited decreased methylglucoside formation, slower growth on medium containing phenolic compounds, and reduced virulence toward bark beetles. Hence, methylglucosylation of plant-derived phenolics is a detoxification process that significantly increases the ability of B. bassiana to parasitize host insects consuming plant tissue high in phenolics, such as conifer phloem. This is one of the few examples of an entomopathogen that is able to resist the plant-derived defenses of an insect host.