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Functional proteomics identified a PICS complex required for piRNA maturation and chromosome segregation

ABSTRACT: Piwi-interacting RNAs (piRNAs) play significant roles in suppressing transposons and nonself nucleic acids, maintaining genome integrity, and defending against viral infections, and are essential for fertility in a variety of organisms. In C. elegans, most piRNA precursors are transcribed by RNA polymerase II in the nucleus and are subjected to a number of processing and maturation steps. However, the biogenesis of piRNAs is still not fully understood. We used functional proteomics to study piRNA biogenesis in C. elegans and identified a piRNA processing and chromosome segregation (PICS) complex. The PICS complex contains two known piRNA biogenesis factors, TOFU-6 and PID-1, and three new proteins PICS-1, TOST-1, and ERH-2, which exhibit dynamic localization among different subcellular compartments. In the germlines of gravid animals, the PICS complex contains TOFU-6/PICS-1/ERH-2/PID-1, is largely concentrated at the perinuclear granule zone and engages in piRNA processing. During early embryogenesis, the TOFU-6/PICS-1/ERH-2/TOST-1 complex accumulates in the nucleus and plays essential roles in chromosome segregation and cell division. Interestingly, the functions of these factors in mediating chromosome segregation are independent of piRNA production. Therefore, we speculate that differential compositions of PICS factors may help cells coordinate distinct cellular processes.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE130371 | GEO | 2019/05/19

REPOSITORIES: GEO

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Project description:Small non-coding RNAs that associate with Piwi proteins, called piRNAs, serve as guides for repression of diverse transposable elements in germ cells of Metazoa. In Drosophila, the genomic regions that give rise to piRNAs, the so-called piRNA clusters, are transcribed to generate long precursor molecules that are processed into mature piRNAs. How genomic regions that give rise to piRNA precursor transcripts are differentiated from the rest of the genome and how these transcripts are specifically channeled into the piRNA biogenesis pathway are not known. We found that trans-generationally inherited piRNAs provide the critical trigger for piRNA production from homologous genomic regions in the next generation by two different mechanisms. First, inherited piRNAs enhance processing of homologous transcripts into mature piRNAs by initiating the ping-pong cycle in the cytoplasm. Second, inherited piRNAs induce installment of the H3K9me3 mark on genomic piRNA cluster sequences. The HP1 homolog Rhino binds to the H3K9me3 mark through its chromodomain and is enriched over piRNA clusters. Rhino recruits the piRNA biogenesis factor Cutoff to piRNA clusters and is required for efficient transcription of piRNA precursors. We propose that trans-generationally inherited piRNAs act as an epigenetic memory for identification of substrates for piRNA biogenesis on two levels, by inducing a permissive chromatin environment for piRNA precursor synthesis and by enhancing processing of these precursors. sequencing of argonaute-bound and total small RNAs from ovaries of different fly crosses: maternal deposition (MD) crosses, in which piRNAs from the P1152 locus are transmitted into the next generation through the mother. No maternak deposition (NMD) crosses, which are reciprocal to the MD crosses. Subsequently, no piRNAs from the P1152 locus are transmitted into the next generation. The strain P-1152, that carries insertion of P{lArB} construct in telomeric sequences of X chromosome (site 1A) is described in (Roche and Rio 1998). The strain BC69 that has insertion of P{A92} construct at a euchromatic location on chromosome 2L (site 35B10-35C1) is described in (Lemaitre et al. 1993).Both stocks were a generous gift from S. Ronsseray.

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Functional proteomics identified a PICS complex required for piRNA maturation and chromosome segregation

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