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Sex determination is a hierarchically-regulated process with high diversity in different organisms including insects. The W chromosome-derived  Fem  piRNA has been identified as the primary sex determination factor in the lepidopteran insect,  Bombyx mori , revealing a distinctive piRNA-mediated sex determination pathway. However, the comprehensive mechanism of silkworm sex determination is still poorly understood. We show here that the silkworm PIWI protein BmSiwi, but not BmAgo3, is essential for silkworm sex determination. CRISPR/Cas9-mediated depletion of  BmSiwi  results in developmental arrest in oogenesis and partial female sexual reversal, while  BmAgo3  depletion only affects oogenesis. We identify three histone methyltransferases (HMTs) that are significantly down-regulated in  BmSiwi  mutant moths. Disruption one of these,  BmAsh2 , causes dysregulation of piRNAs and transposable elements ( TEs ), supporting a role for it in the piRNA signaling pathway. More importantly, we find that  BmAsh2  mutagenesis results in oogenesis arrest and partial female-to-male sexual reversal as well as dysregulation of the sex determination genes,  Bmdsx  and  BmMasc . Mutagenesis of other two HMTs,  BmSETD2  and  BmEggless , does not affect piRNA-mediated sex determination. Histological analysis and immunoprecipitation results support a functional interaction between the BmAsh2 and BmSiwi proteins. Our data provide the first evidence that the HMT, BmAsh2, plays key roles in silkworm piRNA-mediated sex determination.

Bombyx mori histone methyltransferase BmAsh2 is essential for silkworm piRNA-mediated sex determination