Females and males contribute in opposite ways to the evolution of gene order in Drosophila.

Carlos Díaz-Castillo

doi:10.1371/journal.pone.0064491

Abstract

An intriguing association between the spatial layout of chromosomes within nuclei and the evolution of chromosome gene order was recently uncovered. Chromosome regions with conserved gene order in the Drosophila genus are larger if they interact with the inner side of the nuclear envelope in D. melanogaster somatic cells. This observation opens a new door to understand the evolution of chromosomes in the light of the dynamics of the spatial layout of chromosomes and the way double-strand breaks are repaired in D. melanogaster germ lines. Chromosome regions at the nuclear periphery in somatic cell nuclei relocate to more internal locations of male germ line cell nuclei, which might prefer a gene order-preserving mechanism to repair double-strand breaks. Conversely, chromosome regions at the nuclear periphery in somatic cells keep their location in female germ line cell nuclei, which might be inaccessible for cellular machinery that causes gene order-disrupting chromosome rearrangements. Thus, the gene order stability for genome regions at the periphery of somatic cell nuclei might result from the active repair of double-strand breaks using conservative mechanisms in male germ line cells, and the passive inaccessibility for gene order-disrupting factors at the periphery of nuclei of female germ line cells. In the present article, I find evidence consistent with a DNA break repair-based differential contribution of both D. melanogaster germ lines to the stability/disruption of gene order. The importance of germ line differences for the layout of chromosomes and DNA break repair strategies with regard to other genomic patterns is briefly discussed.

Highlights

The distinction between chromosome domains at the periphery and more internal locations of nuclei is a general characteristic of eukaryotes [1,2,3,4,5,6]
Does the D. melanogaster peripherome show evidence of preferential non-homologous endjoining (NHEJ) repair? NHEJ is a remarkably flexible process, not just because it acts upon very diverse disrupted DNA ends, and because the succession of participating enzymes, including nucleases, polymerases, and ligases, can proceed differently even for two joined DNA ends [38]
An excess of retrogenes putatively originated in the Drosophila male germ line was found in the D. melanogaster peripherome, consistent with its accessibility in a moment where there might be a preference to use NHEJ to repair double-strand break (DSB) [21]

Summary

Introduction

The distinction between chromosome domains at the periphery and more internal locations of nuclei is a general characteristic of eukaryotes [1,2,3,4,5,6]. We can define the peripheral syndrome as the ensemble of features characteristic of the peripherome, the component of the genome occupying the nuclear periphery. The fraction of the genome that interacts with the nuclear lamina at the internal side of the nuclear envelope of Drosophila melanogaster somatic cells, hereinafter the D. melanogaster peripherome, has been shown to abound in chromosome domains with remarkable gene order stability in the Drosophila genus [17,18]. A possible cause for the D. melanogaster peripherome gene order stability would be the limited accessibility of loci located at the nuclear periphery for cellular elements that cause gene order disrupting chromosome rearrangements. Since the disruption of gene order depends on DNA breaks, the cellular elements that cause gene order-disrupting chromosome rearrangements would include those that cause and repair DNA breaks

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