Phyllotreta striolata flea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

Significance Associations of plants and herbivores are regarded as the result of coevolution, which has produced an astonishing diversity of plant defenses and corresponding insect counteradaptations. We focus on the leaf beetle Phyllotreta striolata, which is adapted to the glucosinolate-myrosinase system present in its cruciferous host plants. We show that P. striolata adults not only selectively sequester intact glucosinolates from their host plants but also express their own myrosinase, a member of the β-glucosidase family capable of hydrolyzing glucosinolates to form toxic degradation products. Our results reveal the convergent evolution of a glucosinolate-myrosinase system in P. striolata that enables this herbivore to use glucosinolate hydrolysis products for its own purposes. The ability of a specialized herbivore to overcome the chemical defense of a particular plant taxon not only makes it accessible as a food source but may also provide metabolites to be exploited for communication or chemical defense. Phyllotreta flea beetles are adapted to crucifer plants (Brassicales) that are defended by the glucosinolate-myrosinase system, the so-called “mustard-oil bomb.” Tissue damage caused by insect feeding brings glucosinolates into contact with the plant enzyme myrosinase, which hydrolyzes them to form toxic compounds, such as isothiocyanates. However, we previously observed that Phyllotreta striolata beetles themselves produce volatile glucosinolate hydrolysis products. Here, we show that P. striolata adults selectively accumulate glucosinolates from their food plants to up to 1.75% of their body weight and express their own myrosinase. By combining proteomics and transcriptomics, a gene responsible for myrosinase activity in P. striolata was identified. The major substrates of the heterologously expressed myrosinase were aliphatic glucosinolates, which were hydrolyzed with at least fourfold higher efficiency than aromatic and indolic glucosinolates, and β-O-glucosides. The identified beetle myrosinase belongs to the glycoside hydrolase family 1 and has up to 76% sequence similarity to other β-glucosidases. Phylogenetic analyses suggest species-specific diversification of this gene family in insects and an independent evolution of the beetle myrosinase from other insect β-glucosidases.