Multi-Scale Organization of the Drosophila melanogaster Genome.

Samantha C Peterson,Kaylah B Samuelson,Stacey L Hanlon

doi:10.3390/genes12060817

Abstract

Interphase chromatin, despite its appearance, is a highly organized framework of loops and bends. Chromosomes are folded into topologically associating domains, or TADs, and each chromosome and its homolog occupy a distinct territory within the nucleus. In Drosophila, genome organization is exceptional because homologous chromosome pairing is in both germline and somatic tissues, which promote interhomolog interactions such as transvection that can affect gene expression in trans. In this review, we focus on what is known about genome organization in Drosophila and discuss it from TADs to territory. We start by examining intrachromosomal organization at the sub-chromosome level into TADs, followed by a comprehensive analysis of the known proteins that play a key role in TAD formation and boundary establishment. We then zoom out to examine interhomolog interactions such as pairing and transvection that are abundant in Drosophila but rare in other model systems. Finally, we discuss chromosome territories that form within the nucleus, resulting in a complete picture of the multi-scale organization of the Drosophila genome.

Highlights

Within the nucleus, the labyrinth of threads that comprise the genome does not, at first glance, appear to be organized
In Drosophila, an additional layer of organization operates through interhomolog interactions, where regions of one homolog can pair with the corresponding region on the other homolog
This pairing is mediated by proteins that play a role in TAD formation, suggesting that the multi-scale organization we observe may be the result of a unified protein network of genome architects

Summary

Introduction

The labyrinth of threads that comprise the genome does not, at first glance, appear to be organized. Advancements in cytological techniques and DNA sequencing applications have challenged our definition of what it means for a genome to be organized and are revealing how chromosomes self-organize, as well as how and when they interact with their homolog and form discrete territories within the nucleus. Fueled by this acceleration of more sensitive tools for genomic investigation, the field of genome organization has exploded. We chose to concentrate our focus on the multi-scale organization of chromosomes in the model system Drosophila melanogaster (Figure 1).

TADs in Drosophila

Interhomolog Interactions

Transvection and Interhomolog Communication

Chromosome Territories and the Rabl Configuration

Findings

Conclusions