Armitage determines Piwi−piRISC processing from precursor formation and quality control to inter‐organelle translocation

Abstract

Piwi and piRNA form the piRNA-induced silencing complex (piRISC) to repress transposons. In the current model, Armitage (Armi) brings the Piwi-piRISC precursor (pre-piRISC) to mitochondria, where Zucchini-dependent piRISC maturation occurs. Here, we show that Armi is necessary for Piwi-pre-piRISC formation at Yb bodies and that Armi triggers the exit of Piwi-pre-piRISC from Yb bodies and the translocation to mitochondria. Piwi-pre-piRISC resist leaving Yb bodies until Armi binds Piwi-pre-piRISC through the piRNA precursors. The lack of the Armi N-terminus also blocks the Piwi-pre-piRISC exit from Yb bodies. Thus, Armi determines Piwi-piRISC processing, in a multilayered manner, from precursor formation and quality control to inter-organelle translocation for maturation.

Assembly and Function of Gonad-Specific Non-Membranous Organelles in Drosophila piRNA Biogenesis

“…This action does not require Piwi [63]. However, Armi remains localized to Yb bodies in the absence of Piwi, indicating that the departure of Armi from Yb bodies requires Piwi [96]. Armi has the intrinsic ability to bind RNAs promiscuously.…”

“…For the proportion of Zuc that is located far from Yb bodies to function in piRNA processing, RNA substrates would need to travel across the cytosol from Yb bodies to mitochondria. Recent studies show that the intermediates dynamically move from Yb bodies to mitochondria in association with Piwi and Armi [67,96]. In the complex, Piwi interacts with the 5 -phosphate group of the intermediates [96].…”

“…Recent studies show that the intermediates dynamically move from Yb bodies to mitochondria in association with Piwi and Armi [67,96]. In the complex, Piwi interacts with the 5 -phosphate group of the intermediates [96]. Armi also binds the RNAs but this interaction depends on Piwi [67].…”

“…Additional knockdown of Gasz causes Armi to be stuck in Yb bodies [67,96]. Piwi behaves similarly, but to a lesser extent, and cannot stay longer on Gasz through Armi at the surface of mitochondria when Zuc function is abrogated [96]. The functions of Daed and Mino in OSCs remain elusive.…”

“…Upon completion of piRNA processing, Piwi-piRISCs are promptly imported to the nucleus in an Impα/β dependent manner [106]. The nuclear import of Piwi is strictly regulated by Piwi-piRNA association, and apo-Piwi is not imported to the nucleus [61][62][63][65][66][67][68]96,107].…”