Interplay of pericentromeric genome organization and chromatin landscape regulates the expression of Drosophila melanoga
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Epigenetics & Chromatin Open Access
RESEARCH
Interplay of pericentromeric genome organization and chromatin landscape regulates the expression of Drosophila melanogaster heterochromatic genes Parna Saha1,2, Divya Tej Sowpati1, Mamilla Soujanya1,2, Ishanee Srivastava1 and Rakesh Kumar Mishra1,2*
Abstract Background: Transcription of genes residing within constitutive heterochromatin is paradoxical to the tenets of epigenetic code. The regulatory mechanisms of Drosophila melanogaster heterochromatic gene transcription remain largely unknown. Emerging evidence suggests that genome organization and transcriptional regulation are interlinked. However, the pericentromeric genome organization is relatively less studied. Therefore, we sought to characterize the pericentromeric genome organization and understand how this organization along with the pericentromeric factors influences heterochromatic gene expression. Results: Here, we characterized the pericentromeric genome organization in Drosophila melanogaster using 5C sequencing. Heterochromatic topologically associating domains (Het TADs) correlate with distinct epigenomic domains of active and repressed heterochromatic genes at the pericentromeres. These genes are known to depend on the heterochromatic landscape for their expression. However, HP1a or Su(var)3-9 RNAi has minimal effects on heterochromatic gene expression, despite causing significant changes in the global Het TAD organization. Probing further into this observation, we report the role of two other chromatin proteins enriched at the pericentromeresdMES-4 and dADD1 in regulating the expression of a subset of heterochromatic genes. Conclusions: Distinct pericentromeric genome organization and chromatin landscapes maintained by the interplay of heterochromatic factors (HP1a, H3K9me3, dMES-4 and dADD1) are sufficient to support heterochromatic gene expression despite the loss of global Het TAD structure. These findings open new avenues for future investigations into the mechanisms of heterochromatic gene expression. Keywords: Heterochromatic genes, Drosophila melanogaster, Pericentromeres, 5C, HP1a, Su(var)3-9, dMES-4, dADD1, H3K9me3, Het TADs Background The expression of genes present in the constitutive heterochromatin is counterintuitive, and their regulatory mechanisms remain elusive. Such genes are called the heterochromatic genes due to their *Correspondence: [email protected] 1 CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500007, India Full list of author information is available at the end of the article
centromere-proximal location, presence of repressive histone marks and dependence on the heterochromatic trans factors for expression. Heterochromatic genes across various species include the pericentromeric genes of Drosophila melanogaster [1, 2]; juxtacentromeric and X-chromosome inactivation escapee genes in mammals [3–6], and centromeric genes in the knob regions of Arabidopsis genome [7, 8]. Of these, Drosophila melanogaster heterochromatic genes are one of
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