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

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Abstract
According to the prevailing view, mammalian X chromosomes are enriched in spermatogenesis genes expressed before meiosis1,2,3 and deficient in spermatogenesis genes expressed after meiosis2,3. The paucity of postmeiotic 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 meiosis6,7,8 and that most genes on the X chromosome remain repressed in round spermatids7. Here, we report that 33 multicopy gene families, representing ∼273 mouse X-linked genes, are expressed in the testis and that this expression is predominantly in postmeiotic cells. RNA FISH and microarray analysis show that the maintenance of X chromosome postmeiotic repression is incomplete. Furthermore, X-linked multicopy genes exhibit a similar degree of expression as 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 are expressed in postmeiotic cells.