The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression

Abstract

According to the prevailing view, mammalian X chromosomes are enriched in spermatogenesis genes expressed before meiosis1–3 and deficient in spermatogenesis genes expressed after meiosis2,3. The paucity of post-meiotic genes on the X chromosome has been interpreted as a consequence of Meiotic Sex Chromosome Inactivation (MSCI) – the complete silencing of genes on the XY bivalent at meiotic prophase4,5. Recent studies have concluded that MSCI-initiated silencing persists beyond meiosis6–8 and that most X-genes remain repressed in round spermatids7. We report here that 33 multi-copy gene families, representing ~273 mouse X-linked genes, are expressed in the testis and that this expression is predominantly in post-meiotic cells. RNA FISH and microarray analysis show that the maintenance of X chromosome post-meiotic repression is incomplete. Furthermore, X-linked multi-copy genes exhibit expression levels similar to those of autosomal genes. Thus, not only is the mouse X chromosome enriched for spermatogenesis genes functioning before meiosis, but in addition ~18% of mouse X-linked genes exhibit post-meiotic expression.

Extreme selective sweeps independently targeted the X chromosomes of the great apes

“…Only 31% of ampliconic genes are shared with mouse compared with 95% for single-copy genes (24), showing a rapid turnover of these regions. In the mouse, these genes are expressed postmeiotically (25). The ampliconic regions show a striking concordance with low-diversity regions that are most strongly affected by selection in the species (Fig.…”

“…We predict that the association should increase if the hypothesis is true. Direct expression analyses at different stages during spermatogenesis and individual differences may also reveal whether escape from meiotic sex chromosome inactivation (25) or interference with XY body formation is a source of meiotic drive.…”

Parental epigenetic control of embryogenesis: a balance between inheritance and reprogramming?

“…Following meiosis, most single copy genes on the X and Y chromosomes remain in a transcriptionally silent state known as Post-meiotic Sex Chromatin (PMSC) [106], [101], [104], while genes present in multicopy arrays show expression in postmeiotic cells [107]. The role that PMSC plays in paternal inheritance in the early embryo is unknown.…”

DNA double strand break repair, chromosome synapsis and transcriptional silencing in meiosis

“…85 During postmeitotic spermatid development, the X and Y appear to remain globally repressed although a selected set of single-and multi-copy genes is (re)expressed. 84,[95][96][97] Recently, Cocquet et al 98 showed that the multicopy gene Sly is specifically required for the maintenance of postmeiotic X chromosome repression. In addition to SLY, the above-mentioned ubiquitin conjugating enzyme HR6B is also required for the maintenance of meiotic and postmeiotic sex chromosome inactivation.…”