Polytene Chromosomes - A Portrait of Functional Organization of the Drosophila Genome

Abstract

This mini-review is devoted to the problem genetic meaning of main polytene chromosome structures - bands and interbands. Generally, densely packed chromatin forms black bands, moderately condensed regions form grey loose bands, whereas decondensed regions of the genome appear as interbands. Recent progress in the annotation of the Drosophila genome and epigenome has made it possible to compare the banding pattern and the structural organization of genes, as well as their activity. This was greatly aided by our ability to establish the borders of bands and interbands on the physical map, which allowed to perform comprehensive side-by-side comparisons of cytology, genetic and epigenetic maps and to uncover the association between the morphological structures and the functional domains of the genome. These studies largely conclude that interbands 5'-ends of housekeeping genes that are active across all cell types. Interbands are enriched with proteins involved in transcription and nucleosome remodeling, as well as with active histone modifications. Notably, most of the replication origins map to interband regions. As for grey loose bands adjacent to interbands, they typically host the bodies of house-keeping genes. Thus, the bipartite structure composed of an interband and an adjacent grey band functions as a standalone genetic unit. Finally, black bands harbor tissue-specific genes with narrow temporal and tissue expression profiles. Thus, the uniform and permanent activity of interbands combined with the inactivity of genes in bands forms the basis of the universal banding pattern observed in various Drosophila tissues.

Keywords: Bands and interbands; Drosophila; Genes; Origin recognition complexes; P-elements; Polytene chromosomes; Promoters; Proteins of open chromatin.

Fig. (1)

Fragment of the polytene chromosome arm 3R showing compacted dark-staining bands (thick arrows), loose bands appearing grey (thin arrows), as well as interbands (arrowheads). The image is the courtesy of Dr. V.F. Semeshin.

Fig. (2)

Proteins, histone modifications and genomiс elements that are stably present across the four chromatin types in S2, BG3 and Cl.8 cell lines.

Fig. (3)

GRO-Seq signal in four chromatin types of Drosophila

Fig. (4)

Detailed classification of relative positioning of aquamarine, lazurite, malachite and ruby chromatin domains and gene structure in the four chromatin types. Bent arrows and red vertical dashed lines indicate the positions of TSSes. Grey boxes represent coding parts of exons and white boxes correspond to 5’ and 3’ UTRs. Introns are shown as broken lines. Horizontal bars depict different possible overlaps between chromatin domains and genes for all localization classes: TSS, GENE, INTRON and INTERGENIC REGION. The width of each bar reflects the number of each localization subclass in each chromatin type (according to [14]). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this paper.)

Fig. (5)

Localization frequencies for all pairwise combinations of the four chromatin types. All transitions were counted in a sense direction of transcription. X axis shows the structural parts considered in the analysis: 5’UTR and 3’UTR exons, 1^st, 2^nd, 3^rd and the rest of the coding exons, all introns, and intergenic spacers. Y axis shows the number of transitions between chromatin types normalized by the length of an appropriate structural part.

Fig. (6)

Comparison of the mapping data for bands and interbands in the region 10А1-2 - 10B1-2 of the polytene X chromosome and chromatin states and types, as defined by Kharchenko et al. (C, D) [9, 5] and Zhimulev et al. (E, F) [3].