Bicaudal-C plays a critical role in regulating oogenesis in the lepidopteran insect Bombyx mori

Oogenesis is an intricate cellular specialization process that requires the precise expression of multiple genes. However, the functional genes and mechanisms contributing to lepidopteran oogenesis remain incompletely understood. In silkworm, the eggless mutant (smⁿ) has a typical oogenesis disorder phenotype. In smⁿ females, oocyte development is delayed, causing follicle degeneration and the absence of mature eggs in virgin ovarioles. Here, we revealed that BmBic-C, an ortholog of Drosophila melanogaster Bicaudal-C (Bic-C), is responsible for smⁿ. BmBic-C expression was significantly downregulated in smⁿ, likely due to an Organdy transposon insertion upstream of BmBic-C. CRISPR/Cas9-mediated knockout of BmBic-C results in a no-egg phenotype consistent with smⁿ. BmBic-C deficiency reduces the absorption efficiency of vitellogenin, a key factor in egg development. A comparative proteomic analysis between the ΔBmBic-C and control strains revealed 633 differentially expressed proteins (DEPs). Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses of the DEPs suggested that BmBic-C might contribute to ovarian cell development and survival through signal transduction, autophagy, and other pathways. Moreover, BmBic-C dysfunction triggers the apoptosis cascade, highlighting the essential role of BmBic-C in regulating ovarian homeostasis and cell fate. Phylogenetic and selection pressure analyses revealed that Bic-C is highly conserved across lepidopteran species and has undergone purifying selection throughout evolution, suggesting that Bic-C is a key component in organism survival and reproductive regulation. This study provides novel insights into oogenesis and lays a foundation for precision lepidopteran pest control against species-specific genomic/coding variable regions.