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

Ruo Sun,Michael Reichelt,Xingcong Jiang,Daniel Giddings Vassão,Jonathan Gershenzon

doi:10.1007/s10340-020-01319-2

Ruo Sun, Michael Reichelt + Show 3 more

Open Access

https://doi.org/10.1007/s10340-020-01319-2

Copy DOI

Abstract

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.

Highlights

Plants of the order Brassicales, such as those in the Brassicaceae and Capparaceae families, produce glucosinolates and myrosinases as an effective two-component defensive system against non-adapted herbivores and pathogens
The relative accumulation rates revealed that sequestration of aliphatic glucosinolates occurred more rapidly than that of indolic glucosinolates: the concentrations of aliphatic glucosinolates in B. brassicae exceeded those in A. thaliana within one day, while at least 2 days were required for indolic glucosinolates to reach the same concentrations as in the host plant (Fig. 1a)
These results show that different glucosinolates are accumulated at different rates during all life stages of the aphid, and the length of the side chains determines the selective accumulation of aliphatic glucosinolates

Summary

Introduction

Plants of the order Brassicales, such as those in the Brassicaceae and Capparaceae families, produce glucosinolates and myrosinases as an effective two-component defensive system against non-adapted herbivores and pathogens. Glucosinolates are glucosylated pro-toxins that are constitutively and abundantly accumulated in sulfur-rich S-cells (Koroleva and Cramer 2011), whereas the activating enyzmes, myrosinases (β-thioglucoside glucohydrolases), are present in protein-enriched idioblasts called myrosin cells (Andréasson and Jørgensen 2003; Rask et al 2000; Wittstock and Gershenzon 2002). Such a physical compartmentation avoids the self-intoxication that could result from the unintended hydrolysis of glucosinolates by myrosinases, so that mixing of hydrolytic activating enzymes and their glucosinolate substrates occurs only upon tissue damage, e.g., during attack by a herbivore. Other hydrolysis products, such as CNs, are thought to be less toxic than ITCs and can have a role in indirect defense (Burow et al 2006)

Methods

Results

Conclusion