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Abstract
Late-replicating domains (intercalary heterochromatin) in the Drosophila genome display a number of features suggesting their organization is quite unique. Typically, they are quite large and encompass clusters of functionally unrelated tissue-specific genes. They correspond to the topologically associating domains and conserved microsynteny blocks. Our study aims at exploring further details of molecular organization of intercalary heterochromatin and has uncovered surprising heterogeneity of chromatin composition in these regions. Using the 4HMM model developed in our group earlier, intercalary heterochromatin regions were found to host chromatin fragments with a particular epigenetic profile. Aquamarine chromatin fragments (spanning 0.67% of late-replicating regions) are characterized as a class of sequences that appear heterogeneous in terms of their decompactization. These fragments are enriched with enhancer sequences and binding sites for insulator proteins. They likely mark the chromatin state that is related to the binding of cis-regulatory proteins. Malachite chromatin fragments (11% of late-replicating regions) appear to function as universal transitional regions between two contrasting chromatin states. Namely, they invariably delimit intercalary heterochromatin regions from the adjacent active chromatin of interbands. Malachite fragments also flank aquamarine fragments embedded in the repressed chromatin of late-replicating regions. Significant enrichment of insulator proteins CP190, SU(HW), and MOD2.2 was observed in malachite chromatin. Neither aquamarine nor malachite chromatin types appear to correlate with the positions of highly conserved non-coding elements (HCNE) that are typically replete in intercalary heterochromatin. Malachite chromatin found on the flanks of intercalary heterochromatin regions tends to replicate earlier than the malachite chromatin embedded in intercalary heterochromatin. In other words, there exists a gradient of replication progressing from the flanks of intercalary heterochromatin regions center-wise. The peculiar organization and features of replication in large late-replicating regions are discussed as possible factors shaping the evolutionary stability of intercalary heterochromatin.
Highlights
IntroductionAlbeit not necessarily overlapping, have been used to identify Drosophila genomic domains: these include functional similarity, temporal and absolute levels of gene expression, replication timing, association with histone modifications and chromosomal proteins, chromatin accessibility, physical contacts, evolutionary conservation, topological associations, etc [1,2,3,4,5,6,7,8,9,10,11,12,13,14]
Domain organization is essential for appropriate regulation of eukaryotic genomes
Large bands scattered over euchromatic arms of Drosophila polytene chromosomes and resembling pericentric heterochromatin in terms of chromatin packaging were described as intercalary heterochromatin (IH) [16]
Summary
Albeit not necessarily overlapping, have been used to identify Drosophila genomic domains: these include functional similarity, temporal and absolute levels of gene expression, replication timing, association with histone modifications and chromosomal proteins, chromatin accessibility, physical contacts, evolutionary conservation, topological associations, etc [1,2,3,4,5,6,7,8,9,10,11,12,13,14]. The very first domains in the chromosomes of diploid cells,—euchromatin and heterochromatin, were identified back in 1932 by Heitz based on their contrasting morphological features associated with distinct levels of chromatin packaging [15]. Molecular borders of IH have been mapped and these were demonstrated to be highly stable across various types of somatic cells tested [23]
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