Meta-Analysis Reveals that Genes Regulated by the Y Chromosome in Drosophila melanogaster Are Preferentially Localized to Repressive Chromatin

The Drosophila Y chromosome is a degenerated, heterochromatic chromosome with few functional genes. Despite this, natural variation on the Y chromosome in D. melanogaster has substantial trans-acting effects on the regulation of X-linked and autosomal genes. It is not clear, however, whether these genes simply represent a random subset of the genome or whether specific functional properties are associated with susceptibility to regulation by Y-linked variation. Here, we present a meta-analysis of four previously published microarray studies of Y-linked regulatory variation (YRV) in D. melanogaster. We show that YRV genes are far from a random subset of the genome: They are more likely to be in repressive chromatin contexts, be expressed tissue specifically, and vary in expression within and between species than non-YRV genes. Furthermore, YRV genes are more likely to be associated with the nuclear lamina than non-YRV genes and are generally more likely to be close to each other in the nucleus (although not along chromosomes). Taken together, these results suggest that variation on the Y chromosome plays a role in modifying how the genome is distributed across chromatin compartments, either via changes in the distribution of DNA-binding proteins or via changes in the spatial arrangement of the genome in the nucleus.