Diptera-specific Daedalus controls Zucchini endonucleolysis in piRNA biogenesis independent of exonucleases

Abstract

PIWI-interacting RNAs (piRNAs) protect germline genomes and maintain fertility by repressing transposons. Daedalus and Gasz act together as a mitochondrial scaffold for Armitage, a necessary factor for Zucchini-dependent piRNA processing. However, the mechanism underlying this function remains unclear. Here, we find that the requirements of Daedalus and Gasz in this process are different: Daedalus physically interacts with Armitage, whereas Gasz supports Daedalus to maintain its function. Daedalus binds to Armitage through two distinct regions, an extended coiled-coil identified in this study, and a sterile α motif (SAM). The former tethers Armitage to mitochondria, while the latter controls Zucchini endonucleolysis to define the length of piRNAs in an exonuclease-independent manner. piRNAs produced in the absence of Daedalus SAM do not exhibit full transposon silencing functionality. Daedalus is Diptera specific. Evolutionarily more complex species, such as mice, rely on exonucleases after Zuc processing to specify the length of piRNAs.