Abstract

Polyphagous insect herbivores possess diverse mechanisms to overcome challenges of feeding in multiple plant species including, but not limited to, transcriptional plasticity and associations with obligate or facultative symbionts. The Asian longhorned beetle (Anoplophora glabripennis) is a polyphagous wood-feeder capable of developing on over 100 tree species and, like other polyphages, its genome contains amplifications of digestive and detoxification genes. This insect also possesses a diverse gut microbial community, which has the metabolic potential to augment digestive physiology. While the genomic repertoires of A. glabripennis and its microbial community have been studied previously, comparatively less is known about how the gut transcriptome and community change in response to feeding in different hosts. In this study, we show that feeding in two suitable hosts (Acer spp. and Populus nigra) altered the expression levels of multicopy genes linked to digestion and detoxification. However, feeding in a host with documented resistance (Populus tomentosa) induced changes in the transcriptome and community beyond what was observed in insects reared in P. nigra, including the downregulation of numerous β-glucosidases, odorant binding proteins, and juvenile hormone binding proteins, the upregulation of several cuticular genes, and the loss of one major bacterial family from the gut community.

Highlights

  • Polyphagous insect herbivores must contend with the challenges of feeding on host plants with varying nutrient and allelochemical compositions

  • The composition of the gut bacterial and fungal communities can vary between individuals at the operational taxonomic unit (OTU) level[26], the taxonomic makeup and metabolic potential of the microbial community are similar across populations and a fungal member in the Fusarium solani species complex (FSSC) is consistently associated with this insect[22,27,28,29,30]

  • Polyphagous insects rely on transcriptional plasticity and, in some cases, facultative and/or obligate symbionts to overcome the challenges of feeding in multiple hosts

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Summary

Introduction

Polyphagous insect herbivores must contend with the challenges of feeding on host plants with varying nutrient and allelochemical compositions. Behavioral, transcriptional, and physiological plasticity are integrated mechanisms used by polyphages to overcome these challenges Evidence for this plasticity is apparent in the genomes and transcriptomes of many of these insects, which often contain large expansions of genes linked to digestion, detoxification, and stress responses whose expression can be modulated to respond to different plant hosts[1,2,3]. The composition of the gut bacterial and fungal communities can vary between individuals at the operational taxonomic unit (OTU) level[26], the taxonomic makeup and metabolic potential of the microbial community are similar across populations and a fungal member in the Fusarium solani species complex (FSSC) is consistently associated with this insect[22,27,28,29,30]. This study examined host plant induced changes to the A. glabripennis gut microbial community and transcriptome profiles in suitable host species belonging to two different genera and a host that is resistant in the field

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