Aphid estrogen-related receptor controls glycolytic gene expression and fecundity

Aphids, the major insect pests of agricultural crops, reproduce sexually and asexually depending upon environmental factors such as the photoperiod and temperature. Nuclear receptors, a unique family of ligand-dependent transcription factors, control insect development and growth including morphogenesis, molting, and metamorphosis. However, the structural features and biological functions of the aphid estrogen-related receptor (ERR) are largely unknown. Here, we cloned full-length cDNA encoding the ERR in the green peach aphid, Myzus persicae, (Sulzer) (Hemiptera: Aphididae) (MpERR) and demonstrated that the MpERR modulated glycolytic gene expression and aphid fecundity. The phylogenetic analysis revealed that the MpERR originated in a unique evolutionary lineage distinct from those of hemipteran insects. Moreover, the AF-2 domain of the MpERR conferred nuclear localization and transcriptional activity. The overexpression of the MpERR significantly upregulated the gene expression of rate-limiting enzymes involved in glycolysis such as phosphofructokinase and pyruvate kinase by directly binding to ERR-response elements in their promoters. Moreover, ERR-deficient viviparous female aphids showed decreased glycolytic gene expression and produced fewer offspring. These results suggest that the aphid ERR plays a pivotal role in glycolytic transcriptional control and fecundity.