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

Abstract

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. convergent evolution | host plant specialization P hytophagous insects are confronted with an arsenal of constitutive and inducible chemical plant defenses (1). To avoid deleterious effects from plant toxins, herbivores require appropriate biochemical adaptations allowing them to deal with these metabolites, for example, by developing insensitive target sites or by enzymatic detoxification. Many specialized insects are able to sequester plant defense compounds and exploit them for their own protection against natural enemies and/or as semiochemicals in interspecific communication (2, 3).The glucosinolate-myrosinase system characteristic of plants in the order Brassicales is one of the best-studied activated plant defense systems (4-6), and several different strategies for avoiding glucosinolate toxicity have been described in specialized insect herbivores of the orders Lepidoptera, Hemiptera, and Hymenoptera (7). Glucosinolates are a structurally diverse group of β-thioglucoside-N-hydroxysulfates that are classified according to their precursor amino acid as aliphatic, aromatic, or indolic glucosinolates (6,8). Plant myrosinases, ascorbate-dependent β-thioglucosidases (EC 3.2.1.147) belonging to glycoside hydrolase family 1 (GH1), are stored separately from the glucosinolates and only come into contact with their substrate when the spatial compartmentalization is destroyed, for example, by herbivore feeding (6). The profile of hydrolysis products then depends on glucosinolate structure, cellular conditio...

Novel family of terpene synthases evolved from trans -isoprenyl diphosphate synthases in a flea beetle

“…We searched for candidate genes encoding TPS enzymes in a P. striolata transcriptome database (27) based on amino acid sequence similarity, but no sequences homologous to known plant, fungal, or bacterial TPS were found. However, nine transcripts were predicted to encode trans-IDS enzymes (i.e., GPPS or FPPS).…”

Acylated Quinic Acids Are the Main Salicortin Metabolites in the Lepidopteran Specialist Herbivore Cerura vinula

“…As the insects' nutritional spectrum is limited to plants of the Salicaceae family (Salix and Populus species), they are regarded as specialist herbivores (Ali and Agrawal 2012;Hintze-Podufal 1970). Numerous metabolic studies (recent examples: Beran et al 2014;Joussen et al 2012;Shelomi et al 2016) have addressed the question whether a specialist herbivore uses a distinct mechanism to cope with the defense of its host plant. In the present publication, we used a double-track strategy: the careful structural identification of metabolic products arising from the diet of the specialist herbivore resulted in an assumption about how the main chemical defense compounds were transformed during digestion.…”

Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore

“…Several specialist species have been shown to selectively sequester at the level of glucosinolate group. For example, the crucifer flea beetle Phyllotreta striolata and the sawfly Athalia rosae both exhibit a preference for host plant glucosinolates belonging to the aliphatic group over indoles (Abdalsamee and Müller 2012;Beran et al 2014). Our study reports a similar result.…”