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Author Notes:

Corresponding author: Eleanor M. Maine, Department of Biology, Syracuse University, Syracuse, New York, United States of America. Email: emmaine@syr.edu.

Conceived and designed the experiments: XS WGK EMM.

Performed the experiments: XS XX AF EMM.

Analyzed the data: XS XX AF WGK EMM.

Contributed reagents/materials/analysis tools: WGK EMM.

Wrote the paper: XS EMM.

We are indebted to Jill Spoerke for early phenotypic and genetic analysis of the ego mutations; we thank Anette Hoye for assistance with mapping om55 and om56 and Nicole Jacobs for assistance in the initial characterization of ekl-1 ego-1 and ego-1 drh-3 males.

We thank: John Belote, Chris Rocheleau, Meera Sundaram, and Michael Cosgrove for many helpful discussions during the course of this work; Mike Cosgrove for comments on the manuscript; C. David Allis, Craig Mello, Shohei Mitani, Anne Villeneuve, Judith Yanowitz, Monique Zetka, and Monica Collaiacovo for providing reagents, protocols, or strains.

Some strains used in this study were obtained from the Caenorhabditis Genetics Center.

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

The authors have declared that no competing interests exist.

Subjects:

Research Funding:

This work was supported by funds from the National Science Foundation (MCB-0615657) and Syracuse University to EMM, and by funds from the National Institutes of Health (RO1 GM063102) to WGK.

The Caenorhabditis Genetics Center, from which some nematode strains used in this study were obtained, is supported by funding from the NIH Center for Research Resources.

Regulation of Heterochromatin Assembly on Unpaired Chromosomes during Caenorhabditis elegans Meiosis by Components of a Small RNA-Mediated Pathway

Journal Title:

PLoS Genetics

Volume:

Volume 5, Number 8

Publisher:

, Pages e1000624-e1000624

Type of Work:

Article | Final Publisher PDF

Abstract:

Many organisms have a mechanism for down regulating the expression of non-synapsed chromosomes and chromosomal regions during meiosis. This phenomenon is thought to function in genome defense. During early meiosis in Caenorhabditis elegans, unpaired chromosomes (e.g., the male X chromosome) become enriched for a modification associated with heterochromatin and transcriptional repression, dimethylation of histone H3 on lysine 9 (H3K9me2). This enrichment requires activity of the cellular RNA-directed RNA polymerase, EGO-1. Here we use genetic mutation, RNA interference, immunofluorescence microscopy, fluorescence in situ hybridization, and molecular cloning methods to identify and analyze three additional regulators of meiotic H3K9me2 distribution: CSR-1 (a Piwi/PAZ/Argonaute protein), EKL-1 (a Tudor domain protein), and DRH-3 (a DEAH/D-box helicase). In csr-1, ekl-1, and drh-3 mutant males, we observed a reduction in H3K9me2 accumulation on the unpaired X chromosome and an increase in H3K9me2 accumulation on paired autosomes relative to controls. We observed a similar shift in H3K9me2 pattern in hermaphrodites that carry unpaired chromosomes. Based on several assays, we conclude that ectopic H3K9me2 accumulates on paired and synapsed chromosomes in these mutants. We propose alternative models for how a small RNA-mediated pathway may regulate H3K9me2 accumulation during meiosis. We also describe the germline phenotypes of csr-1, ekl-1, and drh-3 mutants. Our genetic data suggest that these factors, together with EGO-1, participate in a regulatory network to promote diverse aspects of development.

Copyright information:

© 2009 She et al.

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