A conserved zinc-finger gene BmZFO721 regulates meiosis and female fertility in silkworm, Bombyx mori.

Abstract

Accurate meiotic progression during oogenesis is fundamental to oocyte maturation and female fertility in sexually reproducing organisms. In lepidopteran insects, however, the upstream regulators governing female meiotic progression, particularly ovary-specific functional genes, remain largely uncharacterized, and their in vivo roles in oocyte development are poorly understood. Here, we identified a gene encoding an ovary-specific C2H2-type zinc-finger protein (ZFP), designated BmZFO721 (Bombyx mori Zinc-Finger Ovary gene 721). Phylogenetic and genomic synteny analyses reveal that BmZFO721 is highly conserved across lepidopteran insects, and hybridization chain reaction staining demonstrates its specific expression in germ cells (nurse cells and oocytes) within ovarioles, with no detectable signal in somatic follicle cells or the germarium. CRISPR/Cas9-mediated knockout of BmZFO721 severely disrupts oogenesis, impairing synaptonemal complex (SC) assembly and chromosomal condensation. The synapsis deficiency triggers meiotic checkpoint activation and subsequent germ cell apoptosis, which eliminates aberrant oocytes and ultimately results in complete female sterility. In addition, transcriptomic analysis further suggests that the oogenic defects in mutants are associated with dysregulation of genes involved in DNA metabolism, chromatin structural organization, and nucleosome dynamics. Collectively, our findings demonstrate that BmZFO721 functions as a crucial regulator of meiotic progression and germ cell survival, revealing unique regulatory strategies in lepidopteran oogenesis.