The Evolution of Glycoside Hydrolase Family 1 in Insects Related to Their Adaptation to Plant Utilization

SIMPLE SUMMARY: β-glucosidase is a crucial enzyme in the adaptation of insects to plant cell wall digestion and plant metabolite detoxication. However, the evolution of this enzyme remains unclear. Here, we fill this gap by investigating the evolution of insect glycoside hydrolase family GH1, accounting for the majority of members of β-glucosidase. We found the GH1 gene family to be present in all insect species with large gene numbers in insects directly feeding on plant cell wall components. Furthermore, the large gene numbers were associated with a complex evolutionary history, including tandem duplication and neofunctionalization. These results highlight the evolutionary traits of an important insect enzyme and provide further insights into our understanding of the evolution of insect–plant interactions. ABSTRACT: Insects closely interact with plants with multiple genes involved in their interactions. β-glucosidase, constituted mainly by glycoside hydrolase family 1 (GH1), is a crucial enzyme in insects to digest plant cell walls and defend against natural enemies with sequestered plant metabolites. To gain more insights into the role of this enzyme in plant–insect interactions, we analyzed the evolutionary history of the GH1 gene family with publicly available insect genomes. We found that GH1 is widely present in insects, while the gene numbers are significantly higher in insect herbivores directly feeding on plant cell walls than in other insects. After reconciling the insect GH1 gene tree with a species tree, we found that the patterns of duplication and loss of GH1 genes differ among insect orders, which may be associated with the evolution of their ecology. Furthermore, the majority of insects’ GH1 genes were tandem-duplicated and subsequently went through neofunctionalization. This study shows the evolutionary history of an important gene family GH1 in insects and facilitates our understanding of the evolution of insect–plant interactions.