Late Replication Domains Are Evolutionary Conserved in the Drosophila Genome

Natalya G Andreyenkova,Lidiya V Boldyreva,Igor F Zhimulev,Tatyana D Kolesnikova,Igor V Makunin,Tatyana Yu Zykova,Elena S Belyaeva,Galina V Pokholkova,Kristin C Scott

doi:10.1371/journal.pone.0083319

Natalya G Andreyenkova, Lidiya V Boldyreva + Show 7 more

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https://doi.org/10.1371/journal.pone.0083319

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Abstract

Drosophila chromosomes are organized into distinct domains differing in their predominant chromatin composition, replication timing and evolutionary conservation. We show on a genome-wide level that genes whose order has remained unaltered across 9 Drosophila species display late replication timing and frequently map to the regions of repressive chromatin. This observation is consistent with the existence of extensive domains of repressive chromatin that replicate extremely late and have conserved gene order in the Drosophila genome. We suggest that such repressive chromatin domains correspond to a handful of regions that complete replication at the very end of S phase. We further demonstrate that the order of genes in these regions is rarely altered in evolution. Substantial proportion of such regions significantly coincide with large synteny blocks. This indicates that there are evolutionary mechanisms maintaining the integrity of these late-replicating chromatin domains. The synteny blocks corresponding to the extremely late-replicating regions in the D. melanogaster genome consistently display two-fold lower gene density across different Drosophila species.

Highlights

Domain organization of the genome has recently become central to our understanding of how eukaryotic genome functions
We analyzed the evolution of gene order in repressive latereplicating domains of Drosophila genome
orthologous landmarks» (OLs) were identified upon comparison of 9 Drosophila species: D. melanogaster, D. erecta, D. yakuba, D. ananassae, D. pseudoobscura, D. willistoni, D. virilis, D. mojavensis and D. grimshawi

Summary

Introduction

Domain organization of the genome has recently become central to our understanding of how eukaryotic genome functions. There are many ways to subdivide a genome into distinct domains and search for the correlation between the distribution of genes and specific chromatin features. Domain organization is essential for proper functioning of the genome. The very functionality of such domains typically remains untested. Recent studies of Drosophila genome evolution showed that there are regions where chromosome rearrangement breakpoints tend to cluster, and which have been recurrently used in evolution. There are regions that are virtually never involved in rearrangements [1,2]. The question is what is so special about these regions where gene order remains intact across different species?

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