Abstract
Author SummarySex chromosomes differ from non-sex chromosomes (“autosomes”) at the genomic, transcriptomic, and epigenomic level, yet the X and Y share a common evolutionary origin. The Drosophila Y chromosome is gene-poor and associated with a compact and transcriptionally inactive form of genetic material called heterochromatin. The X, in contrast, is enriched for activating chromatin marks and is consequently hyper-transcribed, a process thought to be an adaptation to decay and silencing of genes on the Y, resulting in “dosage compensation.” How sex chromosomes have altered their chromatin structure, and what genomic changes led to this dramatically different epigenetic makeup, however, has remained a mystery. By studying the genome, epigenome, and transcriptome of a species with a very recently evolved pair of sex chromosomes (the neo-X and neo-Y of a fruit fly, Drosophila miranda), we here recapitulate how both dosage compensation and heterochromatin formation evolve in Drosophila and establish several novel and important principles governing the evolution of chromatin structure. We dissect the evolutionary history of over 60 novel binding sites for the dosage compensation complex that evolved by natural selection on the neo-X within the last one million years. We show that the 21-bp consensus motifs for recruiting the dosage compensation complex were acquired by diverse molecular mechanisms along the neo-X, while the onset of heterochromatin formation is triggered by the accumulation of transposable elements, leading to silencing of adjacent neo-Y genes. We find that spreading of these chromatin modifications results in massive mis-expression of neo-sex linked genes, and that little correspondence exists between functional activity of genes on the neo-Y and whether they are dosage-compensated on the neo-X. Intriguingly, the genomic regions being targeted by the dosage compensation complex on the neo-X and those that are heterochromatic on the neo-Y show little overlap, possibly reflecting different propensities of the ancestral chromosome that formed the sex chromosome to evolve active versus repressive chromatin configurations. These findings have broad implications for current models of sex chromosome evolution.
Highlights
Sex chromosomes evolve from ordinary autosomes [1]
Epigenome, and transcriptome of a species with a very recently evolved pair of sex chromosomes, we here recapitulate how both dosage compensation and heterochromatin formation evolve in Drosophila and establish several novel and important principles governing the evolution of chromatin structure
We dissect the evolutionary history of over 60 novel binding sites for the dosage compensation complex that evolved by natural selection on the neo-X within the last one million years
Summary
Sex chromosomes evolve from ordinary autosomes [1]. Degeneration of the Y chromosome is a general facet of sex chromosome evolution, and old Y chromosomes are gene poor, often contain high amounts of repetitive DNA, and in Drosophila the Y is entirely heterochromatic [2]. The euchromatic, gene-rich X, in contrast, has adopted a hyperactive chromatin configuration, resulting in hyper-transcription of X-linked genes in male Drosophila (i.e., dosage compensation). While resulting in opposite phenotypic outcomes, the formation of hyperactive chromatin on the X and silent heterochromatin on the Y has intriguing parallels [3,4] Both are initiated at specific nucleation sites, are associated with characteristic histone modifications, and spreading of the modified chromatin configuration across tens of kilobases allows genomic neighborhoods to adopt a similar silent or hyperactive chromatin state. Dosage compensation in Drosophila occurs by doubling the transcription rate of X-linked genes in males [5], through recruitment of the MSL-complex to specific chromatin entry sites (CES) on the X in a sequence-specific manner [6,7]. Co-transcriptional targeting and spreading of the MSL-complex along the X
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