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Global chromatin conformation differences in the Drosophila dosage compensated chromosome X.

ABSTRACT: In Drosophila melanogaster the single male chromosome X undergoes an average twofold transcriptional upregulation for balancing the transcriptional output between sexes. Previous literature hypothesised that a global change in chromosome structure may accompany this process. However, recent studies based on Hi-C failed to detect these differences. Here we show that global conformational differences are specifically present in the male chromosome X and detectable using Hi-C data on sex-sorted embryos, as well as male and female cell lines, by leveraging custom data analysis solutions. We find the male chromosome X has more mid-/long-range interactions. We also identify differences at structural domain boundaries containing BEAF-32 in conjunction with CP190 or Chromator. Weakening of these domain boundaries in male chromosome X co-localizes with the binding of the dosage compensation complex and its co-factor CLAMP, reported to enhance chromatin accessibility. Together, our data strongly indicate that chromosome X dosage compensation affects global chromosome structure.

SUBMITTER: Pal K

PROVIDER: S-EPMC6877619 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Global chromatin conformation differences in the Drosophila dosage compensated chromosome X.

Pal Koustav K Forcato Mattia M Jost Daniel D Sexton Thomas T Vaillant Cédric C Salviato Elisa E Mazza Emilia Maria Cristina EMC Lugli Enrico E Cavalli Giacomo G Ferrari Francesco F

Nature communications 20191125 1

In Drosophila melanogaster the single male chromosome X undergoes an average twofold transcriptional upregulation for balancing the transcriptional output between sexes. Previous literature hypothesised that a global change in chromosome structure may accompany this process. However, recent studies based on Hi-C failed to detect these differences. Here we show that global conformational differences are specifically present in the male chromosome X and detectable using Hi-C data on sex-sorted emb ...[more]

PMID: 31767860

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Project description:BackgroundIn Drosophila melanogaster dosage compensation of most X-linked genes is mediated by the male-specific lethal (MSL) complex, which includes MOF. MOF acetylates histone H4 at lysine 16 (H4K16ac). The X-linked Larval serum protein one alpha (Lsp1alpha) gene has long been known to be not dosage compensated. Here we have examined possible explanations for why the Lsp1alpha gene is not dosage compensated.ResultsQuantitative RNase protection analysis showed that the genes flanking Lsp1alpha are expressed equally in males and females and confirmed that Lsp1alpha is not dosage compensated. Unlike control X-linked genes, Lsp1alpha was not enriched for H4K16ac in the third instar larval fat body, the tissue in which the gene is actively expressed. X-linked Lsp1alpha promoter-lacZ reporter transgenes are enriched for H4K16ac in third instar larval fat body. An X-linked reporter gene bracketed by Lsp1alpha flanking regions was dosage compensated. One of the genes flanking Lsp1alpha is expressed in the same tissue. This gene shows a modest enrichment for H4K16ac but only at the part of the gene most distant from Lsp1alpha. Phylogenetic analyses of the sequences of the genomes of 12 Drosophila species shows that Lsp1alpha is only present within the melanogaster subgroup of species.ConclusionLsp1alpha is not modified by the MSL complex but is in a region of the X chromosome that is regulated by the MSL complex. The high activity or tissue-specificity of the Lsp1alpha promoter does not prevent regulation by the MSL complex. The regions flanking Lsp1alpha do not appear to block access by the MSL complex. Lsp1alpha appears to have recently evolved within the melanogaster subgroup of Drosophila species. The most likely explanation for why Lsp1alpha is not dosage compensated is that the gene has not evolved a mechanism to independently recruit the MSL complex, possibly because of its recent evolutionary origin, and because there appears to be a low level of bound MSL complex in a nearby gene that is active in the same tissue.

Dataset Information

Global chromatin conformation differences in the Drosophila dosage compensated chromosome X.

Publications

Global chromatin conformation differences in the Drosophila dosage compensated chromosome X.

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