BmLid has histone lysine demethylase activity and regulates oogenesis in the silkworm, Bombyx mori

Lepidoptera, a major threat to global agriculture, possesses robust reproductive strategies, making understanding reproduction crucial for developing sterile insect techniques (SIT). The silkworm (Bombyx mori), a model lepidopteran, exhibits polytrophic meroistic oogenesis involving trophocyte-mediated nutrient transport and vitellogenin receptor (VgR)-dependent yolk protein uptake. However, epigenetic regulation of these processes remains unclear. This study investigates the role of BmLid, a histone demethylase, in silkworm oogenesis. Using CRISPR/Cas9, we generated BmLid knockout mutants (ΔBmLid) and confirmed gene disruption via sequencing and western blotting. ΔBmLid females exhibited developmental defects and complete sterility, despite unaffected mating behavior or sperm migration. The H3K4me2/me3 and H3K9me2/me3 levels were significantly increased in ΔBmLid ovaries, indicating BmLid has broad demethylase activity in vivo, too. Transcriptomic analysis showed significant downregulation of VgR, critical for vitellogenin transport, alongside dysregulation of cell junction and apoptosis pathways. These defects disrupted follicular epithelium integrity and yolk protein deposition, mirroring similar phenotypes observed in VgR mutants. Our findings demonstrate that BmLid regulates oogenesis by modulating histone methylation to control VgR expression, cell adhesion, and cell apoptosis, thereby ensuring vitellogenesis. This study highlights epigenetic mechanisms underlying lepidopteran reproduction and identifies BmLid as a potential target for SIT-based pest management strategies.