Neighbourhood Continuity Is Not Required for Correct Testis Gene Expression in Drosophila

Abstract

Author SummaryThe order of genes within eukaryotic genomes is not completely random. In all genomes characterised to date there are regions of the genome, known as gene expression neighbourhoods, which contain clusters of genes that are expressed together in a particular tissue or at a particular developmental stage. Comparative genomics indicates that at least some neighbourhoods have been conserved during evolution, suggesting that this facet of genome organisation may be functionally advantageous. While several models explaining the organisation of the genome into neighbourhoods have been proposed, the functional significance of neighbourhood organisation has not been experimentally tested. Here, we report experiments that disrupt defined testis gene expression neighbourhoods in the Drosophila genome. We generated chromosomal inversions with a breakpoint within a neighbourhood, defined as having genes co-expressed within the testis. Comparing gene expression in flies carrying inversions with their otherwise identical progenitors shows that maintaining the linear organisation of genes in a neighbourhood is not necessary for correct gene expression. We also show that it is not necessary for genes in a neighbourhood to be in close proximity in the nucleus for them to be co-expressed, since the inversions disrupt the spatial organisation of neighbourhood genes in the nucleus. Our experiments indicate that the current models used to account for the existence of gene expression neighbourhoods are unlikely to be sufficient.