Proteasome β3 subunit (PSMB3) controls female reproduction by promoting ecdysteroidogenesis during sexual maturation in Bactrocera dorsalis

Abstract

Steroid hormone 20-hydroxyecdysone (20E) plays critical roles in reproductive development in dipterans and several other insect species. Ecdysteroidogenesis in the glands of larval or nymphal insects and other arthropods has been extensively studied, but that in the adult gonads remains largely unknown. Here we identified a proteasome β3 subunit (PSMB3) from a highly invasive pest Bactrocera dorsalis, and found that this gene was crucial for ecdysone production during female reproduction. PSMB3 was enriched in the ovary, and it was upregulated during sexual maturation. RNAi-mediated depletion of PSMB3 resulted in retarded ovarian development and decreased fecundity. Additionally, knockdown of PSMB3 reduced 20E titer in hemolymph of B. dorsalis. Molecularly, RNA sequencing and qPCR validation revealed that PSMB3 depletion suppressed the expression of 20E biosynthetic genes in the ovary and 20E responsive genes in the ovary and fat body. Furthermore, exogenous 20E rescued the inhibition of the ovarian development caused by PSMB3 depletion. Taken together, this study provides new insights into the adult reproductive development-related biological processes controlled by PSMB3, and proposed a potential eco-friendly control strategy against this notorious agricultural pest.