Abstract
BackgroundThe processes through which the germline maintains its continuity across generations has long been the focus of biological research. Recent studies have suggested that germline continuity can involve epigenetic regulation, including regulation of histone modifications. However, it is not clear how histone modifications generated in one generation can influence the transcription program and development of germ cells of the next.ResultsWe show that the histone H3K36 methyltransferase maternal effect sterile (MES)-4 is an epigenetic modifier that prevents aberrant transcription activity in Caenorhabditis elegans primordial germ cells (PGCs). In mes-4 mutant PGCs, RNA Pol II activation is abnormally regulated and the PGCs degenerate. Genetic and genomewide analyses of MES-4-mediated H3K36 methylation suggest that MES-4 activity can operate independently of ongoing transcription, and may be predominantly responsible for maintenance methylation of H3K36 in germline-expressed loci.ConclusionsOur data suggest a model in which MES-4 helps to maintain an 'epigenetic memory' of transcription that occurred in germ cells of previous generations, and that MES-4 and its epigenetic product are essential for normal germ cell development.
Highlights
The processes through which the germline maintains its continuity across generations has long been the focus of biological research
RNA interference (RNAi) knockdown of tlk-1 did not consistently ablate the H5 epitope in primordial germ cells (PGCs), significant loss of H5 staining was observed in some somatic nuclei (Figure 2C). tlk-1(RNAi) embryos exhibited numerous other phenotypes, including cytokinetic defects [18], and we did observe some embryos lacking PGC H5 staining, so we cannot exclude some indirect effects on H5 staining in tlk-1(RNAi) embryos
Note that the H5 signal was fully depleted in the PGCs of ama-1 RNAi embryos, indicating that in PGCs the H5 epitope that was resistant to cdk-9 and tlk-1 single RNAi is associated with AMA-1
Summary
The processes through which the germline maintains its continuity across generations has long been the focus of biological research. Recent studies have suggested that germline continuity can involve epigenetic regulation, including regulation of histone modifications. It is not clear how histone modifications generated in one generation can influence the transcription program and development of germ cells of the next. An additional round of epigenetic reprogramming occurs upon establishment of the embryonic germline in many species [1]. The purpose of these events are not clear, but they are thought to be important for resetting an epigenetic ‘ground state’ that is compatible with developmental pluripotency in the zygote, and with maintaining or establishing totipotency in the germline.
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