Broad chromosomal domains of histone modification patterns in C. elegans
- Tao Liu1,10,
- Andreas Rechtsteiner2,10,
- Thea A. Egelhofer2,10,
- Anne Vielle3,10,
- Isabel Latorre3,
- Ming-Sin Cheung3,
- Sevinc Ercan4,
- Kohta Ikegami4,
- Morten Jensen4,
- Paulina Kolasinska-Zwierz3,
- Heidi Rosenbaum5,
- Hyunjin Shin1,
- Scott Taing1,
- Teruaki Takasaki2,
- A. Leonardo Iniguez5,
- Arshad Desai6,
- Abby F. Dernburg7,8,
- Hiroshi Kimura9,
- Jason D. Lieb4,
- Julie Ahringer3,11,
- Susan Strome2,11 and
- X. Shirley Liu1,11
- 1 Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts 02115, USA;
- 2 Department of Molecular, Cell and Developmental Biology, University of California Santa Cruz, Santa Cruz, California 95064, USA;
- 3 The Gurdon Institute and Department of Genetics, University of Cambridge, Cambridge CB2 1QN, United Kingdom;
- 4 Department of Biology, Carolina Center for Genome Sciences and Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA;
- 5 Roche NimbleGen, Inc., Madison, Wisconsin 53719, USA;
- 6 Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California San Diego, La Jolla, California 92037, USA;
- 7 HHMI, Department of Molecular and Cell Biology, and California Institute for Quantitative Biosciences, University of California Berkeley, Berkeley, California 94720, USA;
- 8 Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA;
- 9 Graduate School for Frontier Biosciences, Osaka University, Osaka 565-0871, Japan
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↵10 These authors contributed equally to this work.
Abstract
Chromatin immunoprecipitation identifies specific interactions between genomic DNA and proteins, advancing our understanding of gene-level and chromosome-level regulation. Based on chromatin immunoprecipitation experiments using validated antibodies, we define the genome-wide distributions of 19 histone modifications, one histone variant, and eight chromatin-associated proteins in Caenorhabditis elegans embryos and L3 larvae. Cluster analysis identified five groups of chromatin marks with shared features: Two groups correlate with gene repression, two with gene activation, and one with the X chromosome. The X chromosome displays numerous unique properties, including enrichment of monomethylated H4K20 and H3K27, which correlate with the different repressive mechanisms that operate in somatic tissues and germ cells, respectively. The data also revealed striking differences in chromatin composition between the autosomes and between chromosome arms and centers. Chromosomes I and III are globally enriched for marks of active genes, consistent with containing more highly expressed genes, compared to chromosomes II, IV, and especially V. Consistent with the absence of cytological heterochromatin and the holocentric nature of C. elegans chromosomes, markers of heterochromatin such as H3K9 methylation are not concentrated at a single region on each chromosome. Instead, H3K9 methylation is enriched on chromosome arms, coincident with zones of elevated meiotic recombination. Active genes in chromosome arms and centers have very similar histone mark distributions, suggesting that active domains in the arms are interspersed with heterochromatin-like structure. These data, which confirm and extend previous studies, allow for in-depth analysis of the organization and deployment of the C. elegans genome during development.
Footnotes
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↵11 Corresponding authors.
For L3 data: E-mail ja219{at}cam.ac.uk.
For embryo data: E-mail sstrome{at}ucsc.edu.
For data analysis: E-mail xsliu{at}jimmy.harvard.edu.
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[Supplemental material is available for this article. The data in this paper are available online from the modENCODE Data Coordination Center website (http://intermine.modencode.org/). Accession numbers for all ChIP-chip experiments are in Supplemental Table S1.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.115519.110.
- Received September 17, 2010.
- Accepted December 8, 2010.
- Copyright © 2011 by Cold Spring Harbor Laboratory Press
Freely available online through the Genome Research Open Access option.
