Abstract
In the male mouse the X and Y chromosomes pair and recombine within the small pseudoautosomal region. Genes located on the unsynapsed segments of the X and Y are transcriptionally silenced at pachytene by Meiotic Sex Chromosome Inactivation (MSCI). The degree to which MSCI is conserved in other vertebrates is currently unclear. In the female chicken the ZW bivalent is thought to undergo a transient phase of full synapsis at pachytene, starting from the homologous ends and spreading through the heterologous regions. It has been proposed that the repair of the ZW DNA double-strand breaks (DSBs) is postponed until diplotene and that the ZW bivalent is subject to MSCI, which is independent of its synaptic status. Here we present a distinct model of meiotic pairing and silencing of the ZW pair during chicken oogenesis. We show that, in most oocytes, DNA DSB foci on the ZW are resolved by the end of pachytene and that the ZW desynapses in broad synchrony with the autosomes. We unexpectedly find that ZW pairing is highly error prone, with many oocytes failing to engage in ZW synapsis and crossover formation. Oocytes with unsynapsed Z and W chromosomes nevertheless progress to the diplotene stage, suggesting that a checkpoint does not operate during pachytene in the chicken germ line. Using a combination of epigenetic profiling and RNA–FISH analysis, we find no evidence for MSCI, associated with neither the asynaptic ZW, as described in mammals, nor the synaptic ZW. The lack of conservation of MSCI in the chicken reopens the debate about the evolution of MSCI and its driving forces.
Highlights
Meiosis is the process in which maternal and paternal homologous chromosomes engage in close physical pairing, termed synapsis, and exchange genetic information by recombination through the programmed formation and repair of DNA double-strand breaks (DSBs) [1]
In mouse the X and Y are highly divergent in gene content and size, and synapsis and recombination is restricted to a distal limited region of homology, called the pseudoautosomal region (PAR) [5]
The correct segregation of the homologous chromosomes is assured by the coordination of synapsis and repair of DNA double-strand breaks through homologous recombination
Summary
Meiosis is the process in which maternal and paternal homologous chromosomes engage in close physical pairing, termed synapsis, and exchange genetic information by recombination through the programmed formation and repair of DNA double-strand breaks (DSBs) [1]. Autosomal homologs synapse and recombine along their entire length, but the sex chromosomes are often largely non-homologous, or, in some species, even lack a pairing partner [2] and represent a challenge to a system based on homologous pairing and recombination. Genes located on the unsynapsed regions of the X and Y chromosomes are transcriptionally silenced at early pachytene by Meiotic Sex Chromosome Inactivation (MSCI) [6,7,8]. MSCI is thought to represent a manifestation of a more general mechanism that silences any chromosome that fails to synapse with its homologue, termed Meiotic Silencing of Unsynapsed Chromatin (MSUC)
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