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Many insects are able to feed on crucifers despite the presence of a potent activated defense system known as the mustard oil bomb. In damaged tissue, mustard oil glucosides (glucosinolates) are hydrolyzed by the enzyme myrosinase to form toxic mustard oils (isothiocyanates). Here, we analyzed how the the cabbage stem flea beetle Psylliodes chrysocephala, a key pest of oilseed rape, copes with this chemical defense. First, we found that P. chrysocephala prevents the activation of ingested glucosinolates by two different strategies, a) by sequestering glucosinolates and b) by converting glucosinolates to desulfo-glucosinolates. Our next aim was to identify the sulfatase enzyme(s) responsible for the detoxification of glucosinolates in P. chrysocephala. Nine arylsulfatase-like genes were identified in the transcriptome of P. chrysocephala, and five of them showed glucosinolate sulfatase activity upon heterologous expression in Sf9 cells. By using RNAi, we confirmed that PcGSS1 and PcGSS2 are active towards benzenic and indolic glucosinolates in P. chrysocephala adults in vivo. However, in feeding experiments, the proportion of sequestered and desulfated glucosinolates ranged from 26 to 35% which suggests that these strategies alone are likely not sufficient to overcome the chemical plant defense. Indeed, P. chrysocephala additionally conjugates isothiocyanates to glutathione and metabolizes them via the conserved mercapturic acid pathway. In summary, the cabbage stem flea beetle avoids isothiocyanate formation by specialized strategies (sequestration and desulfation), but also relies on a conserved detoxification pathway to prevent toxicity of isothiocyanates.
