Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster

Abstract

Early embryonic germ cells in C. elegans and D. melanogaster fail to express many messenger RNAs expressed in somatic cells. In contrast, we find that ribosomal RNAs are expressed in both cell types. We show that this deficiency in mRNA production correlates with the absence of a specific phosphoepitope on the carboxy-terminal domain of RNA polymerase II. In both C. elegans and Drosophila embryos, this phosphoepitope appears in somatic nuclei coincident with the onset of embryonic transcription, but remains absent from germ cells until these cells associate with the gut primordium during gastrulation. In contrast, a second distinct RNA polymerase II phosphoepitope is present continuously in both somatic and germ cells. The germ-line-specific factor PIE-1 is required to block mRNA production in the germ lineage of early C. elegans embryos (Seydoux, G., Mello, C. C., Pettitt, J., Wood, W. B., Priess, J. R. and Fire, A. (1996) Nature 382, 713–716). We show here that PIE-1 is also required for the germ-line-specific pattern of RNA polymerase II phosphorylation. These observations link inhibition of mRNA production in embryonic germ cells to a specific modification in the phosphorylation pattern of RNA polymerase II and suggest that repression of RNA polymerase II activity may be part of an evolutionarily conserved mechanism that distinguishes germ line from soma during early embryogenesis. In addition, these studies also suggest that different phosphorylated isoforms of RNA polymerase II perform distinct functions.

A global chromatin compaction pathway that represses germline gene expression during starvation

“…The presence of the pSer2 epitope corresponds to active and elongating RNAPII ( Palancade and Bensaude, 2003 ). Consistent with previous reports, we found that cells of the P lineage in early embryos lacked active RNAPII ( Seydoux and Dunn, 1997 ), whereas the pSer2 epitope was present in Z2/Z3 of all embryonic stages and was also present in new L1s ( Fig. 1 D ).…”

“…Recent work from our laboratory has examined genome activation, repression, and reactivation in the C. elegans primordial germ cells Z2 and Z3 (Z2/Z3; Butuči et al, 2015 ; Wong et al, 2018 ). Z2/Z3 are born during early embryogenesis, and soon after their birth, the PIE-1 protein is degraded ( Mello et al, 1996 ), allowing transcription to be activated for the first time in this lineage ( Seydoux and Dunn, 1997 ). Earlier studies had suggested that after a period of transcriptional activity in embryonic Z2/Z3, the genome becomes repressed again ( Furuhashi et al, 2010 ).…”

RNA Polymerase II C-Terminal Domain: Tethering Transcription to Transcript and Template

“…In a variety of organisms the specification of germ cell fate is based on transcription repression in a process that is thought to involve inhibition of CTD phosphorylation . This was first observed in C. elegans where Seydoux and colleagues showed that the levels of both Ser5P and Ser2P are reduced in germ line nuclei compared to somatic nuclei . They went on to show that PIE-1, a maternal protein that segregates with germ cells is capable of inhibiting Ser2 and Ser5 phosphorylation …”

The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

“…2D). Considering the PGCs are regarded as transcriptionally quiescent in C. elegans , 57 it is intriguing to see such a burst of expression for these eliminated genes in O. tipulae PGCs. Future studies are required to determine the function of these genes in the PGCs.…”