Contrasting diets reveal the metabolic plasticity of the tree-killing beetle, Anoplophora glabripennis (Cerambycidae: Lamiinae)

Authors: MASON, CHARLES - Pennsylvania State University; Scully, Erin; Geib, Scott; HOOVER, KELLI - Pennsylvania State University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/2/2016
Publication Date: 9/22/2016
Publication URL: http://handle.nal.usda.gov/10113/63266
Citation: Mason, C.J., Scully, E.D., Geib, S.M., Hoover, K. 2016. Contrasting diets reveal the metabolic plasticity of the tree-killing beetle, Anoplophora glabripennis (Cerambycidae: Lamiinae). Scientific Reports. 6: 33813. doi:10.1038/srep33813.

Interpretive Summary: Feeding on wood presents numerous digestive and nutritional challenges for insects such as the Asian longhorned beetle (ALB), an invasive pest capable of colonizing over 40 tree deciduous species in the United States. Comparison of gene expression of ALB larvae feeding on sugar maple trees, a preferred host tree, and those feeding on a nutrient-rich artificial diet identified genes that enable this insect to digest plant cell walls and other components of wood, obtain essential nutrients, and detoxify plant defensive compounds. Highly expressed genes in ALB feeding in sugar maple included those involved in digesting the main components of plant cell walls (cellulose, xylan, pectin, xyloglucan), metabolizing sucrose (the main sugar product of photosynthesis), and converting 5- and 6- carbon sugars into energy. Additionally, several pathways involved in stress response, detoxification, and producing antioxidants were highly expressed and could be fundamental in allowing ALB to overcome host plant defenses and mitigating damage to tissues. Pathways involved in protein degradation and biosynthesis were also highly expressed, which likely provide a means to quickly replace proteins and digestive enzymes damaged by plant defensive compounds. Genes interacting with beneficial gut microbes were also highly expressed indicating potential roles for microbes in facilitating survival in wood, such as synthesizing essential nutrients and facilitating the digestion of wood. The inventory of genes expressed while this insect feeds in a preferred host begins to lay the foundation for identifying genes that allow ALB and other wood-feeding insects to overcome digestive and nutritional challenges associated with feeding in wood and that contribute to the invasive nature of this insect. These findings will enable us to develop novel gene targets to disrupt digestive, detoxification, and nutrient acquiring processes to control ALB and other wood-feeding pests.

Technical Abstract: Wood-feeding insects encounter challenging diets with low quantities of protein, recalcitrant sources of carbohydrates, and high levels of defensive compounds. These insects have multiple, complementary mechanisms to contend with these digestive challenges. The Asian longhorned beetle (Anoplophora glabripennis) is a polyphagous wood-feeding insect capable of attacking and killing a wide range of hardwood tree species. We compared global gene expression of midguts collected from larvae feeding in sugar maple, a preferred host tree, to those feeding on a nutrient-rich artificial diet, to identify genes putatively involved in digestion of wood and host plant utilization. Differential expression of ~3600 genes in the midguts of A. glabripennis larvae feeding on the two diets reflected marked differences in responses to dietary substrate. Genes with the predicted capacity for plant and microbial carbohydrate usage, detoxification, and nutrient recycling were upregulated in wood-fed larvae. Additionally, immune-related genes relevant for facilitating interactions with microbial symbionts were more highly expressed in wood-feeding larvae. Upregulation of several genes involved in protein degradation and synthesis was also noted, suggesting that proteins incur more rapid turnover in insects consuming wood. Elevated expression levels for several mitochondrial cytochrome C oxidase genes were also observed, suggesting elevated aerobic respiration rates are occurring in wood-feeding individuals. Collectively, these results indicate that A. glabripennis modulates gene expression profiles when larvae are fed in a nutrient-poor, yet suitable host plant compared with a more tractable and nutrient-rich diet that is free of defensive compounds.