The making of aggregation: terpene pheromone biosynthesis in the multicolored Asian lady beetle, Harmonia axyridis (Pallas)

Females of the invasive, cosmopolitan lady beetle, Harmonia axyridis (Pallas), emit a sex/aggregation pheromone consisting of a mixture of volatile terpenes including (E)-β-caryophyllene as the primary constituent. The biosynthetic origins of the terpene metabolites composing this pheromone are poorly understood. Previously, insects were thought to lack the ability to synthesize terpene metabolites de novo. However, recent characterizations of isoprenyl diphosphate synthase (IDS)-like proteins in several insect species (including some belonging to the order Coleoptera) have revealed the presence of IDS-like proteins with terpene synthase (TPS) function that evolved independently and perhaps more recently than bona fide TPSs found in microbes and plants. To investigate the biosynthetic origins of Harmonia axyridis terpene pheromone components, we cloned and functionally characterized a family of H. axyridis IDS-like genes/proteins, revealing at least two proteins that catalyze the formation of terpenes including the pheromone constituents (E)-β-caryophyllene and α-humulene. Phylogenetic and genomic analysis of the H. axyridis TPS genes suggest an emergence from duplicated genes with conserved IDS function. Results from these experiments expand our knowledge on the recruitment of ancestral primary metabolic genes/proteins in the evolution of terpene pheromone metabolism in beetles and other insect lineages.