Rapid incorporation of glucosinolates as a strategy used by a herbivore to prevent activation by myrosinases.

Various plants have a binary defence system that consists of a substrate and a glucosidase, which is activated upon tissue disruption thereby forming reactive hydrolysis products. Insects feeding on such plants have to overcome this binary defence system or prevent the activation. In this study, we investigated the strategy used by a herbivore to deal with such binary defence. We studied, how the larvae of the sawfly Athalia rosae (Hymenoptera: Tenthredinidae) circumvent the activation of glucosinolates by myrosinase enzymes, which are found in their Brassicaceae host plants. Myrosinase activities were low in the front part of the larval gut but activities increased over the gut passage. In contrast, the glucosinolates were only highly concentrated in the first gut part and were rapidly incorporated into the haemolymph before the food reached the second half of the gut. Thus, the uptake and concentration of glucosinolates, i.e., sequestration, must occur in the front part of the gut. Using Matrix Assisted Laser Desorption Ionization-Mass Spectrometry Imaging (MALDI-MSI), we could demonstrate that the incorporated glucosinolate sinalbin circulates in the haemolymph where it accumulates around the Malpighian tubules. This study highlights the pivotal role of the gut of an adapted herbivore as a regulatory functional organ to cope with plant toxins. MALDI-MSI turned out as a highly useful technique to visualise glucosinolates in a herbivore, which has to deal with plants exhibiting a binary defence system, and may be applied to follow the fate of plant metabolites in other insect species in the future.

Effects of indole glucosinolates on performance and sequestration by the sawfly Athalia rosae and consequences of feeding on the plant defense system.

In this study, the performance and sequestration specificity of the sawfly Athalia rosae L. (Hymenoptera: Tenthredinidae) reared on two wild Brassica oleracea L. (Brassicaceae) populations (KIM and WIN), which express indole glucosinolates (GSs) in very high concentrations, were investigated. The local and systemic plant responses to larval feeding also were analyzed. Indole GSs predominated in KIM plants, whereas aliphatic GSs prevailed in the WIN population, which had several times higher total GS concentrations than KIM plants. Plants of the KIM population had lower specific leaf areas, and higher carbon/nitrogen ratios than WIN plants. The insects reared on WIN plants performed better for most traits than insects reared on the KIM population. The larvae preferentially sequestered aliphatic GSs but when feeding on KIM plants, indole GSs were also concentrated in the hemolymph. In response to feeding by A. rosae larvae, indole GSs were induced locally and systemically, whereas aliphatic GSs were reduced only in systemic leaves of the WIN population. Soluble myrosinase activities were constitutively higher in WIN than in KIM plants, and feeding damage led to a significant reduction of this glucosinolate-degrading enzyme in WIN plants only. The data suggest that the sawfly is well adapted to high concentrations of aliphatic GSs, which are sequestered by the larvae. In contrast, the larvae may be less adapted to plants dominated by indole GSs. Selective induction of indole GSs by the plants in response to larval feeding may be adaptive as accumulation of indole GSs may lower the performance of the larvae.