Investigation of Genes Linked to Polyphagy and Xylophagy in Asian Longhorned Beetle (Anoplophora glabripennis) through Comparative Genomics and Transcriptome Profiling

The Asian longhorned beetle (ALB; Anoplophora glabripennis) is an invasive, wood-boring beetle that completes its development while feeding exclusively inside a broad range of deciduous host trees. Here, it faces a number of nutritional and digestive challenges, including the presence of highly recalcitrant lignocellulose and hemicellulose, high concentrations of plant defensive chemicals, and low abundances of protein, amino acids and essential nutrients. While microbes housed in the gut make important contributions to nutritional ecology in ALB, the genome contains numerous amplifications of various classes of glycoside hydrolases (GHs), carboxylesterases, cytochrome P450s, UDP-glucuronosyl transferases, and digestive serine proteinases in comparison to other phytophagous insects limited host ranges (e.g., Agrilus planipennis; emerald ash borer). Many of these genes were highly expressed in the larval midgut when the insect fed in a suitable host (Acer saccharum) compared to a nutrient rich artificial diet, suggesting that they are relevant for digesting plant cell walls, detoxification, and nutrient acquisition. The expression profile of these amplified gene families also changed dramatically when ALB larvae were fed in another suitable host tree (Populus nigra) suggesting that they provide ALB with the metabolic plasticity to thrive on multiple hosts. Finally, feeding in a resistant tree (Populus tomentosa) not only caused substantial disruptions to several families of digestive and detoxification, but it also reduced expression of several genes with hypothesized roles in development. Taken together, these findings provide insight into the functions of amplified gene families in and the mechanisms of host tree resistance in polyphagous insects.