Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 523 (7559), 240-4

Condensin-driven Remodelling of X Chromosome Topology During Dosage Compensation

Affiliations

Condensin-driven Remodelling of X Chromosome Topology During Dosage Compensation

Emily Crane et al. Nature.

Abstract

The three-dimensional organization of a genome plays a critical role in regulating gene expression, yet little is known about the machinery and mechanisms that determine higher-order chromosome structure. Here we perform genome-wide chromosome conformation capture analysis, fluorescent in situ hybridization (FISH), and RNA-seq to obtain comprehensive three-dimensional (3D) maps of the Caenorhabditis elegans genome and to dissect X chromosome dosage compensation, which balances gene expression between XX hermaphrodites and XO males. The dosage compensation complex (DCC), a condensin complex, binds to both hermaphrodite X chromosomes via sequence-specific recruitment elements on X (rex sites) to reduce chromosome-wide gene expression by half. Most DCC condensin subunits also act in other condensin complexes to control the compaction and resolution of all mitotic and meiotic chromosomes. By comparing chromosome structure in wild-type and DCC-defective embryos, we show that the DCC remodels hermaphrodite X chromosomes into a sex-specific spatial conformation distinct from autosomes. Dosage-compensated X chromosomes consist of self-interacting domains (∼1 Mb) resembling mammalian topologically associating domains (TADs). TADs on X chromosomes have stronger boundaries and more regular spacing than on autosomes. Many TAD boundaries on X chromosomes coincide with the highest-affinity rex sites and become diminished or lost in DCC-defective mutants, thereby converting the topology of X to a conformation resembling autosomes. rex sites engage in DCC-dependent long-range interactions, with the most frequent interactions occurring between rex sites at DCC-dependent TAD boundaries. These results imply that the DCC reshapes the topology of X chromosomes by forming new TAD boundaries and reinforcing weak boundaries through interactions between its highest-affinity binding sites. As this model predicts, deletion of an endogenous rex site at a DCC-dependent TAD boundary using CRISPR/Cas9 greatly diminished the boundary. Thus, the DCC imposes a distinct higher-order structure onto X chromosomes while regulating gene expression chromosome-wide.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Extended Data Figure 1
Extended Data Figure 1. Genome-wide chromatin interaction maps for wild-type or DC mutant embryos and genome-wide difference chromatin interaction map
a, b Genome-wide chromatin interaction maps for wild-type embryos (a) and DC mutant embryos (b) from Hi-C data of combined replicates binned at 50 kb and corrected with ICE. c, f Scatter plots comparing normalized interactions between pairs of 50 kb bins in the two replicates from wild-type embryos (c) or DC mutant embryos (f) (both excluding x = y diagonal). A strong correlation between biological replicates is shown for wild-type embryos (Pearson’s correlation coefficient = 0.9854) and for DC mutant embryos (Pearson’s correlation coefficient = 0.9919). d, g Overall interaction frequency decays with increasing genomic distance in wild-type embryos (d) and in DC mutant embryos (g). e, h Cumulative reads versus linear genomic distance in wild-type embryos (e) and in DC mutant embryos (h). i, Genome-wide difference chromatin interaction map. Shown is the 50 kb binned heatmap depicting the Z-score difference between wild-type and DC mutant embryos (see Methods for Z-score difference calculation). The most apparent differences are on the X chromosome: blue signal within TADs (loss of intra-TAD interactions) and red signal between TADs (gain of inter-TAD interactions).
Extended Data Figure 2
Extended Data Figure 2. Insulation profile calculation parameters and boundary calling
a, Cartoon shows approach for calculating the insulation profile. A square is slid along each diagonal bin of the interaction matrix to aggregate the amount of interactions that occur across each bin (up to a specified distance up- and downstream of the bin). Bins with a high insulation effect (e.g. at a TAD boundary) have a low insulation score (as measured by the insulation square). Bins with low insulation or boundary activity (e.g. in the middle of a TAD) have a high insulation score. Minima along the insulation profile are potential TAD boundaries. b, c, Heatmaps of X and I represent the insulation profiles calculated using insulation square sizes ranging from 10 kb to 1 Mb. At the 100 kb scale, weak boundaries are observed on X and autosomes, but they are generally not changed in DC mutants. These boundaries cannot be detected at larger scales, meaning they do not insulate over distances beyond ~100 kb (see e). These smaller scale structures may represent sub-TAD domains not correlated with dosage compensation. Boundaries called using a 500 kb insulation square represent TAD boundaries that define domains observed in chromosome-wide interaction maps of X at 10 kb resolution. These boundaries are used in this paper (Fig. 1) and insulate over the larger distances defining the Mb-sized TADs. Boundaries on X are the strongest and are DC dependent. d, e, f, Pile up plots depict aggregate (mean) Hi-C 10 kb Z-score data centered on specified ‘anchors’ (e.g. rex sites, boundaries, changed boundaries). d, Pile up plots centered on all rex sites or top 25 rex sites in wild-type and DC mutant. e, Pile up plots centered on all boundaries called using insulation squares of 100 kb (left) or 500 kb (right) for X and I in wild-type and DC mutant. f, Pile up plots using boundaries called with a 500 kb insulation square, centered (left) on the single 10 kb bin at the midpoint of all 8 changed boundaries or (right) on all seven 10 kb bins within changed boundaries.
Extended Data Figure 3
Extended Data Figure 3. TAD boundary analysis
a, Insulation/Delta plot of the 10 kb binned wild-type combined replicate chromosome X Hi-C data calculated using a 500 kb insulation square size. The insulation profile is depicted in black. In red, the ‘delta’ vector is depicted. It is derived from the insulation vector using a 200 kb delta window (see insulation methods). The ‘delta’ vector is used to facilitate the detection of the valleys/minima along the insulation profile. b, Cartoon example showing how the delta vector is calculated from the insulation data vector. For each bin (reference point) the average insulation differences are calculated between all points up to 100 kb left of the reference point relative to the reference point. The same is repeated for all points up to 100 kb right of the reference point. The delta value is then defined as the difference between the mean (left difference) and mean (right difference). c, Bar plot shows the distribution of distances between boundary calls obtained with biological replicate Hi-C data across all chromosomes. Dotted vertical line indicates that +/− 30 kb was chosen for boundary definition, as it was the window in which the majority of replicate boundary calls (> 80%) overlap. d, Boxplots compare boundary strength (left) and spacing (right) in wild-type vs. DC mutant embryos. Wild-type boundary strength on X (defined as the distance from the insulation minimum to the largest neighboring maximum in the insulation profile) is higher than the DC mutant chromosome X boundary strength (P = 0.024) and higher than the boundary strength on wild-type autosomes (P = 0.03). TAD boundary strength on autosomes does not change in the DC mutant compared to wild-type (P = 0.979). Boundaries on X have less variance in spacing (interquartile range (IQR) = 253 kb) compared to the DC mutant (IQR = 525 kb) embryos. DC mutant X boundary spacing is more similar to the boundary spacing on the autosomes in wild-type (IQR = 625 kb) and DC mutant embryos (IQR = 550 kb).
Extended Data Figure 4
Extended Data Figure 4. Compartment and insulation analysis for chromosome I in wild-type and DC mutant embryos. (see next page.)
a, ICE corrected chromatin interaction maps are shown for wild-type and DC mutant embryos for both 10 kb binned and 50 kb binned data across replicate 1, replicate 2, and the combined replicates. b, Insulation profiles are shown for each biological replicate (replicate 1, orange line; replicate 2, blue line) for 50 kb and 10 kb binned data in wild-type and DC mutant embryos. Insulation profiles are calculated using a 500 kb × 500 kb insulation square (10 bins × 10 bins for the 50 kb binned Hi-C data, and 50 bins × 50 bins for the 10 kb binned Hi-C data). The insulation profiles are consistent across replicates. Green tick marks, TAD boundaries identified using combined replicate data. c, Differential insulation plots derived from the insulation profiles calculated above (50 kb binned and 10 kb binned Hi-C data). d, 50 kb binned heatmap depicting the difference in chromatin interactions expressed as the difference in Z-scores between wild-type and DC mutant. e, Plot showing the compartment analysis calculated using the 50 kb binned wild-type Hi-C data. A/B compartment profile was determined by principle component analysis. First Eigen Vector value representing compartments (black) is plotted along the chromosome, revealing three zones for each autosome: two outer sections and the middle third of the chromosome. Positive Eigen1 signals represent the B (inactive compartment) and negative Eigen1 signals represent the A (active compartment). The compartments at chromosome ends display increased interactions with each other, both in cis and in trans (see Extended Data Fig. 1a). Also shown is the average binding of the lamin-associated protein LEM-2 along the chromosomes (grey). Overall compartmentalization correlates with LEM-2 binding, showing that compartments at both ends of chromosome I are located near the nuclear periphery.
Extended Data Figure 5
Extended Data Figure 5. Compartment and insulation analysis for chromosome X in wild-type and DC mutant embryos
a–e, See legend to Extended Data Fig. 4. In e, only two compartments are observed for X, compared to three for chromosome I. Overall compartmentalization correlates with LEM-2 binding, showing that the compartment at the left end of X is located near the nuclear periphery.
Extended Data Figure 6
Extended Data Figure 6. Compartment and insulation analysis for chromosomes II, III, IV, and V in wild-type and DC mutant embryos
a–d, Chromosome II. e–h, Chromosome III. i–l, Chromosome IV. m–p, Chromosome V. a, e, i, m, Insulation profiles for each biological replicate (replicate 1, orange line; replicate 2, blue line) for 50 kb or 10 kb binned Hi-C data in wild-type and DC mutant embryos. Green lines, TAD boundaries identified from combined replicate data. b, f, j, n, Differential insulation plots made from insulation profiles (50 kb binned or 10 kb binned Hi-C data). c, g, k, o, Plots show chromosome compartment analysis calculated with 50 kb binned data. Average binding of the lamin-associated protein LEM-2 is shown along the chromosomes (grey). Compartmentalization correlates with LEM-2 binding; compartments at both ends of autosomes are near the nuclear periphery. d, h, l, p, Heatmaps (50 kb bins) show differences in chromatin interactions as the differences in Z-scores (DC mutant minus wild-type).
Extended Data Figure 7
Extended Data Figure 7. rex sites are enriched at TAD boundaries and in top Hi-C interactions
a, Tick plots rank the interaction Z-scores for the top 25 highest-affinity rex sites (black) among all other 10 kb bin Hi-C interactions on X (light blue). Bottom plot amplifies top 2000 interactions. Density of black ticks (left) shows strong enrichment of rex-rex interactions among the most significant X interactions. b, Tick plots rank the Z-score differences (DC mutant minus wild-type) for interactions between the top 25 rex sites among all other differences on X. Bottom plot amplifies top 2000 changes. c, Quantification of Z-score differences for top 2000 changes in (b). d, Bar graphs depict overlap between X TAD boundaries and rex sites. Three sets of TAD boundaries are shown: all 17 boundaries; 8 boundaries with an insulation change (DC mutant minus wild-type) > 0.1; 5 boundaries present in wild-type embryos but absent in DC mutants. Overlap is calculated for the entire set of rex sites or just the top 25 rex sites. (left), Percent of boundaries that overlap rex sites. (right), Percent of rex sites that overlap each set of boundaries. Red bars, same sets of overlaps were calculated with 1000 random sets of rex-site positions along X. Average overlap and standard deviation are shown. No randomized set had as much overlap as the true rex set (P < 0.001). e, Cumulative comparison of Z-score differences for rex interactions and for 1000 randomized sets of non-rex interactions (same number as in rex set). These rex or non-rex interactions had Z-scores > 4 in wild-type embryos. rex interactions are reduced more in DC mutants than other similarly strong X interactions (P = 0.037; rex-interaction differences were significantly more reduced [KS test] than random interaction sets for 963 of 1000 cases). f, 3D plots of Hi-C interaction profiles (normalized read counts) around top 25 rex sites for 2 Hi-C replicates of wild-type or DC mutants. g, 3D plots of interactions between dox sites in wild-type and DC mutants show no interaction peak. h, Cumulative plots show no difference in DC mutants for the distribution of autosomal Hi-C interaction Z-scores (10 kb bins) in TADs or at boundaries.
Extended Data Figure 8
Extended Data Figure 8. Visualization and disruption of TAD boundaries
a–d, Visualization of DCC-dependent TAD boundaries in single cells confirms Hi-C analysis. a, Representative confocal images of embryonic nuclei of different genotypes stained with a DNA intercalating dye (blue) and FISH probes surrounding rex-32. Scale bar, 1 μm. b, Quantification of colocalization between FISH probes flanking rex-8 (see Fig. 2a) in XX and XO embryos confirms the DCC-dependent boundary identified by Hi-C. Because TADs on either side of rex-8 are small, we could only use one 500 kb FISH probe for each TAD. c, Quantification of colocalization between FISH probes for a TAD boundary on chromosome I (dashed line in d) in XX and XO embryos confirms the DCC-independent boundary identified by Hi-C. b–c, Box plots show the distribution of Pearson’s correlation coefficients between pairwise combinations of FISH probes. Boxes represent the middle 50% of coefficients, and the central bar within indicates the median coefficients (M). N, total number of nuclei. P-values derived using the one-tailed Mann-Whitney U Test are shown below each graph. ns, not significant. d, Insulation difference plot of chromosome I for DC mutant insulation profile minus wild-type insulation profile. e–g, Deletion of endogenous rex-47 by Cas9 disrupts DCC binding and TAD boundary formation. e, Schematic illustration of the sgRNA-Cas9 complex interacting with the rex-47 target sequence. f, Cas9-mediated deletion of rex-47. Top, diagram showing the location of DCC binding motifs within rex-47 (red bars) and Cas9-induced double strand break (arrow). Middle, diagram of the double-stranded repair template containing two ~500 bp homology arms and an NcoI restriction site. Bottom, after precise homology-directed repair, a 419 bp region containing all DCC binding motifs was deleted and replaced with NcoI. g, Loss of DCC binding at endogenous locus carrying the rex-47 deletion. DCC binding at three ~100 bp regions located upstream (a), within (b) or downstream (c) of the 419 bp deletion was examined using ChIP-qPCR. Histogram shows the ChIP-qPCR signal for DCC components DPY-27 or SDC-3 at target regions relative to the level at region b in wild-type embryos.
Extended Data Figure 9
Extended Data Figure 9. Quantitative FISH shows that rex sites colocalize more frequently if the DCC is bound to X
af, Data from histograms in Fig. 4b–g shown as cumulative plots. Number of nuclei and embryos (parentheses) assayed are shown (also for i–m). Distance between loci (red) and DCC dependence or independence of Hi-C interactions (black) are shown. P-values (chi-squared test) compare values in the 0–300 nm bin to those in 301–2700 nm bins. Same statistical analysis for (i–m). g, Correlation between DCC-dependent Hi-C interactions and DCC-dependent FISH colocalization. Y-axis, difference between wild-type and DC mutant Hi-C observed interaction frequency at 50 kb resolution. Higher number shows greater DCC-dependence. X-axis shows two categories defined by FISH: sites with unchanged colocalization frequency in DC mutant (DCC-independent) (left); sites with less frequent colocalization in a DC mutant (DCC-dependent) (right). Red dotted line, cutoff for calling a Hi-C interaction “changed” between wild-type and DC mutant. h, Scatter plot shows correlation between Hi-C and FISH data. Y-axis, Hi-C observed interaction frequency in 50 kb bins. X-axis, % colocalization (i.e. 300 nm bin) by FISH. R = 0.77 for all comparisons; R = 0.9 if the rex-47-rex-8 interaction is omitted. i–m, Histograms show quantification of 3D distances between two FISH probes. i, j, Distant loci on X or I with weak Hi-C interactions. k, DCC-dependent interaction between X sites lacking DCC binding. l–m, DCC-dependent interactions between distant rex sites.
Extended Data Figure 10
Extended Data Figure 10. DCC-dependent TADs influence global rather than local gene expression
Gene expression analysis was assayed using RNA-seq or GRO-seq, as indicated. a–b, Boxplots depict expression levels for wild-type or DC mutant embryos assayed by RNA-seq for X genes at changed TAD boundaries, unchanged TAD boundaries, all TAD boundaries or genes not at TAD boundaries. Expression levels are given as normalized read number per kilobase of gene length. c, Boxplots depict the fold change in expression assayed by RNA-seq between wild-type and DC mutant embryos for genes at changed TAD boundaries, unchanged TAD boundaries, all TAD boundaries or genes not at boundaries. The lowest-expressing genes (bottom 10%) were removed from analysis. d–f, As in a–c, but assayed by GRO-seq with gene expression levels given as fragments per kilobase of transcript per million mapped reads (FPKM). For a–f, P-values were calculated using the Mann-Whitney U Test; significance did not withstand multiple testing correction. g–h, Boxplots depict the fold change in the gene expression between wild-type and DC mutant embryos based on RNA-seq or GRO-seq for X and I. Each box has genes from one TAD on X (left) or I (right). Lowest-expressing genes (bottom 10%) were removed from analysis. No discernible pattern was evident for expression changes versus gene location. i, Boxplots depict the fold change in X gene expression between wild-type and DC mutant embryos relative to the distance from the TAD boundary. Each box contains genes in 10 kb bins radiating out from the center of each TAD boundary. The lowest-expressing genes (bottom 10%) were removed from analysis. No discernible pattern to the gene expression changes exists, as assayed by RNA-seq (left) or GRO-seq (right). Weak significance and lack of concordance between RNA-seq and GRO-seq data suggest no biologically relevant correlation between TAD boundaries and local regulation of gene expression.
Figure 1
Figure 1. DCC modulates spatial organization of X chromosomes
a, b, d, e, Chromatin interaction maps binned at 10 kb resolution show interactions 0–4 Mb apart on chromosomes X and I in wild-type and DC mutant embryos. Plots (black) show insulation profiles. Minima (green lines) reflect TAD boundaries. Darker green indicates stronger boundary. c, f, Bluered Z-score difference maps binned at 50 kb resolution for X and I show increased (orange-red) and decreased (blue) chromatin interactions between mutant and wild-type embryos. Differential insulation plots (red) show insulation changes between mutant and wild-type embryos.
Figure 2
Figure 2. FISH shows DCC-dependent TAD boundaries at high-affinity DCC rex sites
a, High DCC occupancy correlates with TAD boundaries lost or reduced upon DCC depletion. Top, ChIP-seq profiles of DCC subunit SDC-3 in wild-type (red) and DC mutant (green) embryos. Y-axis, reads per million (RPM) normalized to IgG control. Middle, insulation profiles of wild-type (red) and DC mutant (green) embryos. Bottom, insulation difference plot for wild-type insulation profile subtracted from DC mutant profile. Black lines, TAD boundary locations. Blue dots, boundaries with insulation changes > 0.1 between wild-type and DC mutant embryos. Red lines, locations of 25 highest DCC-occupied rex sites. Cyan bars, sites with the largest insulation loss. b, Confocal images of embryonic nuclei of various genotypes stained with a DNA intercalating dye (blue) and 500 kb FISH probes around the rex-47 TAD boundary. c, d, e, Quantification of FISH probe colocalization confirms DCC-dependent and DCC-independent boundaries found by Hi-C. Box plots, distribution of Pearson’s correlation coefficients between pairwise combinations of FISH probes within (blue) or across (orange) TADs. Boxes, middle 50% of coefficients. Center bars, median (M) coefficients. N, total number of nuclei. Asterisks of same color indicate values compared with one-tailed Mann-Whitney U test. ns, not significant.
Figure 3
Figure 3. Strong DCC-dependent interactions occur between high-affinity rex sites at TAD boundaries
a, Cumulative distribution of Hi-C Z-scores for interactions between 10 kb bins with rex sites or with other X interactions in wild-type or DC mutant embryos. Interactions > 4 Mb were excluded from panels (a–e). P-values are corrected for multiple testing. In wild-type embryos, rex-rex interactions are stronger than all other X interactions (P < 2 × 10−16; two-sided KS test) and stronger than rex-rex interactions in DC mutants (P = 1.5 × 10−9; Wilcoxon signed rank test). b, Distributions of Hi-C Z-scores show that rex-rex interactions are stronger than non-rex interactions (P < 2 × 10−16; two-sided KS test) or rex to non-rex interactions (P = 1.7 × 10−14; two-sided KS test). c, Distributions of Z-score differences (DC mutant minus wild-type) show that rex-rex interactions decrease more than any of 1,000 random sets of non-rex interactions of equal number (P < 0.001). d, Average Hi-C interaction profiles (normalized read counts) around pairs of top 25 rex sites or all known rex sites, in wild-type and DC mutants. rex sites are centered at 0. e, Distributions of Hi-C Z-scores for interactions between bins with rex or non-rex sites at TAD boundaries or within TADs of wild-type (left) or DC mutant (middle) embryos. rex sites interact more at TAD boundaries than in TADs (P = 0.0025). These sets of interactions are not different in DC mutants (P = 0.348). Interactions at TAD boundaries or within TADs on autosomes (right). f, Circos plots depict all rex-rex interactions (Z-score >2, colored line) in 50 kb bins in wild-type embryos. Concentric circles show insulation difference plot (black and grey), wild-type TAD boundaries (green boxes), and rex sites (black lines, strongest sites named). g, rex-rex interactions in f that are retained in DC mutants. h, Deletion of rex-47 disrupts TAD boundary. Box plots of Pearson’s correlation coefficients for FISH probe combinations in wild-type, rex-47 Δ, and DC mutant. Probe overlap across TAD boundary increased in rex-47 Δ vs. wild-type (P < 0.01 ANOVA) but was not different in rex-47 Δ vs. DC mutants (P = ns, ANOVA). Probe overlap in TAD was not different in 3 strains (P = 0.075, ANOVA).
Figure 4
Figure 4. Quantitative FISH shows DCC-dependent association of rex sites in single cells
a, Representative embryonic nuclei show variability in spacing of FISH probes (red, green) targeting two rex sites. b-g, Quantification of the 3D distance between FISH probes in embryos of different genotypes. DCC binding to the single X of XO embryos was achieved using a xol-1 (XO lethal) mutation, which activates sdc-2, the XX-specific trigger of DCC assembly. bd, Pairs of rex sites at DCC-dependent TAD boundaries of varying genomic separation. e, A pair of sites on X that lack DCC binding sites within 100 kb but have DCC-dependent Hi-C interactions. f, g, Loci on chromosomes X and I that lack DCC binding sites within 80–90 kb and display DCC-independent Hi-C interactions. (b–g) Distances between FISH spots were binned in 300 nm intervals and represented in relative frequency histograms. Schematic above each histogram depicts the locations of FISH probes (arrows), their genomic separation (red text), and the location of all rex sites (red bars) or sites lacking DCC binding (black). The DCC dependence or independence of the corresponding Hi-C interactions is indicated above the histogram (grey). P values comparing genotypes were calculated using the chi-square test to compare the 0–300 nm bin with 301–2700 nm bins. The 0–300 nm bin contains FISH probes considered co-localized, because probes < 300 nm apart always overlap visually, while probes 700 nm apart appear only adjacent to each other.
Figure 5
Figure 5. DCC-dependent TADs influence global rather than local gene expression
a, Insulation changes and TAD boundaries are compared to median fold-changes in expression (10 kb bins across X) between wild-type and DC mutant embryos. a–h, No discernible pattern was detected between mutant-induced changes in expression and gene locations relative to TADs or TAD boundaries. b, Box plots show comparison of expression levels for X genes within or outside TAD boundaries in wild-type embryos. Expression levels, normalized read number per kilobase of gene length. c, Box plots show expression changes for X genes within or outside TAD boundaries. d, Comparison of expression changes (DC mutant/wild-type) for X gene sets with greater insulation scores in wild-type embryos (grey domains in a) versus in DC mutants (black domains in a). e–h, Same as ad but for genes on chromosome I. P-values for b–d and f–h, Mann-Whitney U Test; no significant P-values withstood multiple testing correction. ns, not significant. (a, c, d, e, g, h), Lowest-expressed genes (bottom 10%) were removed from analyses.

Comment in

  • A TAD Closer to Understanding Dosage Compensation
    AJ Wood et al. Dev Cell 33 (5), 498-9. PMID 26058053.
    Eukaryotic chromosomes are organized into topological domains, but how these are established and maintained is poorly understood. Writing in Nature, Crane et al. (2015) s …

Similar articles

See all similar articles

Cited by 166 PubMed Central articles

See all "Cited by" articles

References

    1. Bickmore WA, van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell. 2013;152:1270–1284. - PubMed
    1. de Laat W, Duboule D. Topology of mammalian developmental enhancers and their regulatory landscapes. Nature. 2013;502:499–506. - PubMed
    1. Jans J, et al. A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. Genes Dev. 2009;23:602–618. - PMC - PubMed
    1. Pferdehirt RR, Kruesi WS, Meyer BJ. An MLL/COMPASS subunit functions in the C. elegans dosage compensation complex to target X chromosomes for transcriptional regulation of gene expression. Genes Dev. 2011;25:499–515. - PMC - PubMed
    1. Csankovszki G, et al. Three distinct condensin complexes control C. elegans chromosome dynamics. Curr Biol. 2009;19:9–19. - PMC - PubMed

Publication types

MeSH terms

Associated data

Feedback