RNase κ promotes robust piRNA production by generating 2′,3′-cyclic phosphate-containing precursors

Megumi Shigematsu, Takuya Kawamura, Keisuke Morichika, Natsuko Izumi, Takashi Kiuchi, Shozo Honda, Venetia Pliatsika, Ryuma Matsubara, Isidore Rigoutsos, Susumu Katsuma, Yukihide Tomari and Yohei Kirino ()
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Megumi Shigematsu: Thomas Jefferson University
Takuya Kawamura: Thomas Jefferson University
Keisuke Morichika: Thomas Jefferson University
Natsuko Izumi: The University of Tokyo
Takashi Kiuchi: The University of Tokyo
Shozo Honda: Thomas Jefferson University
Venetia Pliatsika: Thomas Jefferson University
Ryuma Matsubara: Thomas Jefferson University
Isidore Rigoutsos: Thomas Jefferson University
Susumu Katsuma: The University of Tokyo
Yukihide Tomari: The University of Tokyo
Yohei Kirino: Thomas Jefferson University

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract 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.

Date: 2021
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DOI: 10.1038/s41467-021-24681-w

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