PIWI proteins are essential for early Drosophila embryogenesis

Abstract

PIWI proteins, a subfamily of the ARGONAUTE/PIWI protein family, have been implicated in transcriptional and posttranscriptional gene regulation and transposon silencing mediated by small non-coding RNAs, especially piRNAs. Although these proteins are known to be required for germline development, their somatic function remains elusive. Here, we examine the maternal function of all three PIWI proteins in Drosophila; Piwi, Aubergine (Aub) and Argonaute3 (Ago3) during early embryogenesis. In syncytial embryos, Piwi displays an embryonic stage-dependent localization pattern. Piwi is localized in the cytoplasm during mitotic cycles 1-10. Between cycles 11 and 14, Piwi remains in the cytoplasm during mitosis but moves into the somatic nucleus during interphase. Beyond cycle 14, it stays in the nucleus. Aub and Ago3 are diffusely cytoplasmic from cycle 1-14. Embryos maternally depleted of any one of the three PIWI proteins display severe mitotic defects, including abnormal chromosome and nuclear morphology, cell cycle arrest, asynchronous nuclear division and aberrant nuclear migration. Furthermore, all three PIWI proteins are required for the assembly of mitotic machinery and progression through mitosis. Embryos depleted of maternal PIWI proteins also exhibit chromatin organization abnormalities. These observations indicate that maternal Piwi, Aub and Ago3 play a critical role in the maintenance of chromatin structure and cell cycle progression during early embryogenesis, with compromised chromatin integrity as a possible cause of the observed mitotic defects. Our study demonstrates the essential function of PIWI proteins in the first phase of somatic development.

The developmental proteome of Drosophila melanogaster

“…4D; Supplemental Table S8). These include well-known examples such as Oskar (Osk), String (Stg), Piwi, Aubergine (Aub), Extra sexcombs (Esc), Dorsal (Dl), Mothers against dpp (Mad), and Swallow (Swa) (Chao et al 1991;Edgar and Datar 1996;Luschnig et al 2004;Simmons et al 2010;Mani et al 2014). However, also yet undescribed candidates like CG11674, CG5568, CG17018, CG15047, Zpg, GammaTub37C, and Tosca found in this set represent interesting candidates with a putative role in oogenesis and early embryogenesis.…”

Dynamic RNA–protein interactions underlie the zebrafish maternal-to-zygotic transition

“…Indeed, it has been shown that the depletion of maternal-effect genes, Zar1 and Zar1l, causes embryonic arrest in early mouse embryos (Wu et al 2003;Hu et al 2010). Moreover, lack of maternal Piwi protein in fly embryos causes developmental defects, such as abnormal chromosome morphology and cell cycle arrest (Mani et al 2014). One possibility is that these mRBPs (e.g., ZAR1 and Piwi) escaped detection in other mRNA interactome capture experiments.…”

PIWI proteins and PIWI-interacting RNAs in the soma

“…28). A recent publication has shown that all Drosophila PIWIs are expressed during early embryogenesis and that depletion of maternal Drosophila PIWIs results in profound chromosomal and mitotic defects, thus establishing a crucial function for PIWIs in the earliest stage of somatic development 29 . Together with the work on basal eukaryotes, studies in Drosophila highlight the existence and function of PIWIs in somatic tissues.…”