The selective sequestration of glucosinolates by the cabbage aphid severely impacts a predatory lacewing

The cabbage aphid Brevicoryne brassicae is 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 on B. brassicae and a predatory lacewing, Chrysoperla carnea. We found that distinct glucosinolates were accumulated by B. brassicae at different rates, with aliphatic glucosinolates being taken up more quickly than indolic ones. B. brassicae myrosinase 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 impaired C. carnea development. 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.