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Trans-generational epigenetic regulation of C. elegans primordial germ cells

Hirofumi Furuhashi14, Teruaki Takasaki2, Andreas Rechtsteiner2, Tengguo Li1, Hiroshi Kimura3, Paula M Checchi15, Susan Strome2 and William G Kelly1*

Author Affiliations

1 Biology Department, Emory University, Atlanta, GA 30322, USA

2 Department of MCD Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA

3 Graduate School for Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka 565-0871, Japan

4 Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan

5 Department of Molecular & Cellular Biology, UC Davis, Davis, CA 95616, USA

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Epigenetics & Chromatin 2010, 3:15  doi:10.1186/1756-8935-3-15

Published: 12 August 2010

Abstract

Background

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. 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.

Results

We 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.

Conclusions

Our 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.