Abstract

Wood-feeding insects encounter challenging diets containing low protein quantities, recalcitrant carbohydrate sources, and plant defensive compounds. The Asian longhorned beetle (Anoplophora glabripennis) is a wood-feeding insect that attacks and kills a diversity of hardwood tree species. We compared gene expression of midguts collected from larvae feeding in a preferred tree, sugar maple, to those consuming a nutrient-rich artificial diet, to identify genes putatively involved in host plant utilization. Anoplophora glabripennis larvae exhibited differential expression of ~3600 genes in response to different diets. Genes with predicted capacity for plant and microbial carbohydrate usage, detoxification, nutrient recycling, and immune-related genes relevant for facilitating interactions with microbial symbionts were upregulated in wood-feeding larvae compared to larvae feeding in artificial diet. Upregulation of genes involved in protein degradation and synthesis was also observed, suggesting that proteins incur more rapid turnover in insects consuming wood. Additionally, wood-feeding individuals exhibited elevated expression of several mitochondrial cytochrome C oxidase genes, suggesting increased aerobic respiration compared to diet-fed larvae. These results indicate that A. glabripennis modulates digestive and basal gene expression when larvae are feeding in a nutrient-poor, yet suitable host plant compared to a tractable and nutrient-rich diet that is free of plant defensive compounds.

Highlights

  • Wood-feeding insects encounter challenging diets containing low protein quantities, recalcitrant carbohydrate sources, and plant defensive compounds

  • The heterogeneous nature of the sugar maple wood in terms of polysaccharide composition and nutritional quality was reflected in our findings in that several of the genes with variable expression levels between the two groups of midguts collected from sugar maple-reared insects had putative roles in digestion and nutrient acquisition, which included carboxylesterase (AGLA013185), aldehyde dehydrogenase (AGLA009921), nucleoside transporter (AGLA007856), sugar transporter (AGLA00783), subtilase serine proteinase (AGLA004564), glucose hydrolase (GH) 79 (AGLA003075), trypsin (AGLA002776), and aldo-keto reductase (AGLA000966)

  • We identified marked differences in midgut gene expression in A. glabripennis midgut larvae in their digestive and basal metabolic processes between larvae fed in wood or on artificial diet

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Summary

Introduction

Wood-feeding insects encounter challenging diets containing low protein quantities, recalcitrant carbohydrate sources, and plant defensive compounds. We compared gene expression of midguts collected from larvae feeding in a preferred tree, sugar maple, to those consuming a nutrient-rich artificial diet, to identify genes putatively involved in host plant utilization. Woodfeeding individuals exhibited elevated expression of several mitochondrial cytochrome C oxidase genes, suggesting increased aerobic respiration compared to diet-fed larvae. These results indicate that A. glabripennis modulates digestive and basal gene expression when larvae are feeding in a nutrientpoor, yet suitable host plant compared to a tractable and nutrient-rich diet that is free of plant defensive compounds. Xylophagous (wood-feeding) insects have adapted multiple, complementary mechanisms to contend with these challenges Among these adaptations are host selection behaviors, associations with microbial symbionts, and intrinsic digestive and detoxification capabilities. Microbes can metabolize various classes of tree phytochemical defensive compounds to alleviate toxicity to their herbivore hosts[22,23,24,25]

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