Functional Analysis of Lactase Phlorizin Hydrolase in Insect–Plant Coevolution Based on Deglycosylation

During coevolution, plants produce numerous toxic secondary metabolites to protect themselves. However, most plants still serve as food for insects to meet their nutritional needs. The evolutionary processes that enable herbivorous insects to resist plant defenses remain largely complex and difficult to predict. In this study, lactase phlorizin hydrolase (LPH) was identified for the first time in <i>Aphis gossypii</i>. Bioinformatics analysis showed that the LPH protein belongs to the glycoside hydrolase 1 (GH1) family. The qPCR showed that the transcript level of <i>LPH</i> in cotton aphids treated with the expression dsAgCYP6CY3 cotton lines was significantly reduced by 39.9% at 48 h compared to the nontransgenic cotton, and the hydrolytic activities of LPH on lactose and phlorizin were significantly reduced by 28.7% and 20.1%, respectively. In vitro enzyme activity experiments demonstrated that LPH could hydrolyze lactose and four phenolic glycosides. In addition, RNA interference (RNAi) and insect performance assays showed that silencing <i>LPH</i> affected the growth of the larvae, resulting in the death of the larvae exposed to phenolic glycosides. These results reveal an evolutionary scenario whereby herbivores use deglycosylation to develop resistance to plant defenses and this can be exploited for plant protection.