Sequence-dependent but not sequence-specific piRNA adhesion traps mRNAs to the germ plasm

• Published in: Nature (London) 2016-03, Vol.531 (7594), p.390-394
• Main Authors: Vourekas, Anastassios, Alexiou, Panagiotis, Vrettos, Nicholas, Maragkakis, Manolis, Mourelatos, Zissimos
• Format: Article
• Language: English
• Subjects: 631/136/2434; 631/337/384/2054; 631/337/505; Analysis; Animals; Argonaute Proteins - metabolism; Base Pairing; Binding Sites; Cytoplasm - genetics; Cytoplasm - metabolism; Diffusion; DNA Transposable Elements - genetics; Drosophila melanogaster - cytology; Drosophila melanogaster - genetics; Drosophila melanogaster - metabolism; Drosophila Proteins - metabolism; Embryos; Female; Humanities and Social Sciences; Insects; letter; Male; Membrane Transport Proteins - metabolism; Messenger RNA; multidisciplinary; Offspring; Oocytes - cytology; Oocytes - metabolism; Oogenesis; Peptide Initiation Factors - metabolism; Proteins; Ribonucleic acid; Ribonucleoproteins - metabolism; RNA; RNA Interference; RNA sequencing; RNA Transport; RNA, Messenger - chemistry; RNA, Messenger - genetics; RNA, Messenger - metabolism; RNA, Small Interfering - chemistry; RNA, Small Interfering - genetics; RNA, Small Interfering - metabolism; Science; Transcriptome - genetics; Transposons
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature17150

Maternal mRNAs are tethered within the Drosophila germ plasm via base-pairing interactions between mRNAs and piRNPs containing the Aub Piwi protein; the preference for certain mRNAs to be tethered appears to be related to their longer length, which provides more potential piRNP-binding sites, and the results suggest a new role for piRNAs in germ-cell specification independent of their role in transposon silencing. Germ-cell specification by piRNAs Complexes consisting of Piwi proteins and piwi-interacting RNAs (piRNAs) suppress the activity of transposable elements in germ cells. Maternal piRNPs are transmitted to the oocyte germ plasm, as are mRNAs that specify primordial germ cell formation. Zissimos Mourelatos and colleagues have now defined how these maternal mRNAs are tethered within the germ plasm, via base-pairing interactions between mRNAs and piRNPs containing the Aubergine (Aub) Piwi protein. The preference for certain mRNAs to be tethered appears to be related to their greater length, which provides more potential piRNP binding sites. This work defines a new role for piRNAs in germ cell specification independent of their role in transposon suppression. The conserved Piwi family of proteins and piwi-interacting RNAs (piRNAs) have a central role in genomic stability, which is inextricably linked to germ-cell formation, by forming Piwi ribonucleoproteins (piRNPs) that silence transposable elements 1 . In Drosophila melanogaster and other animals, primordial germ-cell specification in the developing embryo is driven by maternal messenger RNAs and proteins that assemble into specialized messenger ribonucleoproteins (mRNPs) localized in the germ (pole) plasm at the posterior of the oocyte 2 , 3 . Maternal piRNPs, especially those loaded on the Piwi protein Aubergine (Aub), are transmitted to the germ plasm to initiate transposon silencing in the offspring germ line 4 , 5 , 6 , 7 . The transport of mRNAs to the oocyte by midoogenesis is an active, microtubule-dependent process 8 ; mRNAs necessary for primordial germ-cell formation are enriched in the germ plasm at late oogenesis via a diffusion and entrapment mechanism, the molecular identity of which remains unknown 8 , 9 . Aub is a central component of germ granule RNPs, which house mRNAs in the germ plasm 10 , 11 , 12 , and interactions between Aub and Tudor are essential for the formation of germ granules 13 , 14 , 15 , 16 . Here we show that Aub-loaded piRNAs use partial base-pairing characteristi