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Global chromatin domain organization of the Drosophila genome.

de Wit E, Braunschweig U, Greil F, Bussemaker HJ, van Steensel B - PLoS Genet. (2008)

Bottom Line: Furthermore, during evolution fewer chromosomal rearrangements occur inside chromatin domains than outside domains.Our results indicate that a substantial portion of the Drosophila genome is packaged into functionally coherent, multi-gene chromatin domains.This has broad mechanistic implications for gene regulation and genome evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

ABSTRACT
In eukaryotes, neighboring genes can be packaged together in specific chromatin structures that ensure their coordinated expression. Examples of such multi-gene chromatin domains are well-documented, but a global view of the chromatin organization of eukaryotic genomes is lacking. To systematically identify multi-gene chromatin domains, we constructed a compendium of genome-scale binding maps for a broad panel of chromatin-associated proteins in Drosophila melanogaster. Next, we computationally analyzed this compendium for evidence of multi-gene chromatin domains using a novel statistical segmentation algorithm. We find that at least 50% of all fly genes are organized into chromatin domains, which often consist of dozens of genes. The domains are characterized by various known and novel combinations of chromatin proteins. The genes in many of the domains are coregulated during development and tend to have similar biological functions. Furthermore, during evolution fewer chromosomal rearrangements occur inside chromatin domains than outside domains. Our results indicate that a substantial portion of the Drosophila genome is packaged into functionally coherent, multi-gene chromatin domains. This has broad mechanistic implications for gene regulation and genome evolution.

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Genome-wide domainograms reveal non-random local enrichment of chromatin components.(A–C) domainograms for Lamin (A), D1 (B) and Mnt (C) along all major chromosome arms. Simple and nested patterns of local enrichment are visible. D) Domainogram comparison for Polycomb (mapped by DamID [21]) and H3K27me3 (mapped by ChIP [21]) on chromosome 3R. E) HP1 distribution on chromosome 2R in Kc167 cells grown in serum-containing (BPYE) and serum-free (HyQ) medium. A strong telomere-proximal region of enrichment is only observed in BPYE medium (indicated by the red bar). Data from BPYE medium is the same as in Fig. 1A–B. F) Domainograms of chromosome 2L for HP6 binding after RNAi of its binding partner HP1 and after a control RNAi (data from [24]). In D–F, only the bottom parts of the domainogram triangles are shown.
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pgen-1000045-g002: Genome-wide domainograms reveal non-random local enrichment of chromatin components.(A–C) domainograms for Lamin (A), D1 (B) and Mnt (C) along all major chromosome arms. Simple and nested patterns of local enrichment are visible. D) Domainogram comparison for Polycomb (mapped by DamID [21]) and H3K27me3 (mapped by ChIP [21]) on chromosome 3R. E) HP1 distribution on chromosome 2R in Kc167 cells grown in serum-containing (BPYE) and serum-free (HyQ) medium. A strong telomere-proximal region of enrichment is only observed in BPYE medium (indicated by the red bar). Data from BPYE medium is the same as in Fig. 1A–B. F) Domainograms of chromosome 2L for HP6 binding after RNAi of its binding partner HP1 and after a control RNAi (data from [24]). In D–F, only the bottom parts of the domainogram triangles are shown.

Mentions: We systematically generated domainograms for all proteins in the compendium (Fig. 2 and Supplementary Fig. S1). Strikingly, nearly all proteins exhibit non-random enrichment at multiple sites in the genome. In some cases, such as for Lamin (Lam; Fig. 2A) and Polycomb (Pc; Fig. 2D) this is consistent with previously reported evidence for clustering of target genes [21],[22],[31]. For many other proteins, such as the HMG protein D1 and the transcription factor Mnt (Fig. 2B and C), the non-random genomic distribution has not been reported before. In several instances, the patterns of enrichment suggest a nested architecture, with larger domains subdivided into two or more smaller regions of enrichment (e.g., Fig. 2A–C). More complex enrichment patterns, sometimes covering a substantial part of a chromosome arm, can also be seen (e.g., D1 on chromosome 2L, Fig. 2B). Taken together, these results indicate that most chromatin components are highly non-randomly distributed along the Drosophila genome.


Global chromatin domain organization of the Drosophila genome.

de Wit E, Braunschweig U, Greil F, Bussemaker HJ, van Steensel B - PLoS Genet. (2008)

Genome-wide domainograms reveal non-random local enrichment of chromatin components.(A–C) domainograms for Lamin (A), D1 (B) and Mnt (C) along all major chromosome arms. Simple and nested patterns of local enrichment are visible. D) Domainogram comparison for Polycomb (mapped by DamID [21]) and H3K27me3 (mapped by ChIP [21]) on chromosome 3R. E) HP1 distribution on chromosome 2R in Kc167 cells grown in serum-containing (BPYE) and serum-free (HyQ) medium. A strong telomere-proximal region of enrichment is only observed in BPYE medium (indicated by the red bar). Data from BPYE medium is the same as in Fig. 1A–B. F) Domainograms of chromosome 2L for HP6 binding after RNAi of its binding partner HP1 and after a control RNAi (data from [24]). In D–F, only the bottom parts of the domainogram triangles are shown.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2274884&req=5

pgen-1000045-g002: Genome-wide domainograms reveal non-random local enrichment of chromatin components.(A–C) domainograms for Lamin (A), D1 (B) and Mnt (C) along all major chromosome arms. Simple and nested patterns of local enrichment are visible. D) Domainogram comparison for Polycomb (mapped by DamID [21]) and H3K27me3 (mapped by ChIP [21]) on chromosome 3R. E) HP1 distribution on chromosome 2R in Kc167 cells grown in serum-containing (BPYE) and serum-free (HyQ) medium. A strong telomere-proximal region of enrichment is only observed in BPYE medium (indicated by the red bar). Data from BPYE medium is the same as in Fig. 1A–B. F) Domainograms of chromosome 2L for HP6 binding after RNAi of its binding partner HP1 and after a control RNAi (data from [24]). In D–F, only the bottom parts of the domainogram triangles are shown.
Mentions: We systematically generated domainograms for all proteins in the compendium (Fig. 2 and Supplementary Fig. S1). Strikingly, nearly all proteins exhibit non-random enrichment at multiple sites in the genome. In some cases, such as for Lamin (Lam; Fig. 2A) and Polycomb (Pc; Fig. 2D) this is consistent with previously reported evidence for clustering of target genes [21],[22],[31]. For many other proteins, such as the HMG protein D1 and the transcription factor Mnt (Fig. 2B and C), the non-random genomic distribution has not been reported before. In several instances, the patterns of enrichment suggest a nested architecture, with larger domains subdivided into two or more smaller regions of enrichment (e.g., Fig. 2A–C). More complex enrichment patterns, sometimes covering a substantial part of a chromosome arm, can also be seen (e.g., D1 on chromosome 2L, Fig. 2B). Taken together, these results indicate that most chromatin components are highly non-randomly distributed along the Drosophila genome.

Bottom Line: Furthermore, during evolution fewer chromosomal rearrangements occur inside chromatin domains than outside domains.Our results indicate that a substantial portion of the Drosophila genome is packaged into functionally coherent, multi-gene chromatin domains.This has broad mechanistic implications for gene regulation and genome evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

ABSTRACT
In eukaryotes, neighboring genes can be packaged together in specific chromatin structures that ensure their coordinated expression. Examples of such multi-gene chromatin domains are well-documented, but a global view of the chromatin organization of eukaryotic genomes is lacking. To systematically identify multi-gene chromatin domains, we constructed a compendium of genome-scale binding maps for a broad panel of chromatin-associated proteins in Drosophila melanogaster. Next, we computationally analyzed this compendium for evidence of multi-gene chromatin domains using a novel statistical segmentation algorithm. We find that at least 50% of all fly genes are organized into chromatin domains, which often consist of dozens of genes. The domains are characterized by various known and novel combinations of chromatin proteins. The genes in many of the domains are coregulated during development and tend to have similar biological functions. Furthermore, during evolution fewer chromosomal rearrangements occur inside chromatin domains than outside domains. Our results indicate that a substantial portion of the Drosophila genome is packaged into functionally coherent, multi-gene chromatin domains. This has broad mechanistic implications for gene regulation and genome evolution.

Show MeSH