In animal germlines, PIWI proteins and the associated PIWI-interacting RNAs (piRNAs) protect genome integrity by silencing transposons. Here we report the extensive sequence and quantitative correlations between 2′,3′-cyclic phosphate-containing RNAs (cP-RNAs), identified using cP-RNA-seq, and piRNAs in the Bombyx germ cell line and mouse testes. The cP-RNAs containing 5′-phosphate (P-cP-RNAs) identified by P-cP-RNA-seq harbor highly consistent 5′-end positions as the piRNAs and are loaded onto PIWI protein, suggesting their direct utilization as piRNA precursors. We identified Bombyx RNase Kappa (BmRNase κ) as a mitochondria-associated endoribonuclease which produces cP-RNAs during piRNA biogenesis. BmRNase κ-depletion elevated transposon levels and disrupted a piRNA-mediated sex determination in Bombyx embryos, indicating the crucial roles of BmRNase κ in piRNA biogenesis and embryonic development. Our results reveal a BmRNase κ-engaged piRNA biogenesis pathway, in which the generation of cP-RNAs promotes robust piRNA production.
Shigematsu, Megumi; Kawamura, Takuya; Morichika, Keisuke; Izumi, Natsuko; Kiuchi, Takashi; Honda, Shozo; Pliatsika, Venetia; Matsubara, Ryuma; Rigoutsos, Isidore; Katsuma, Susumu; Tomari, Yukihide; and Kirino, Yohei, "RNase κ promotes robust piRNA production by generating 2',3'-cyclic phosphate-containing precursors" (2021). Computational Medicine Center Faculty Papers. Paper 37.
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