Error-Prone ZW Pairing and No Evidence for Meiotic Sex Chromosome Inactivation in the Chicken Germ Line

Error-Prone ZW Pairing and No Evidence for Meiotic Sex Chromosome Inactivation in the Chicken Germ Line
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DOI:
10.1371/journal.pgen.1002560
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发表时间:
2012-03-01
期刊:
影响因子:
4.5
通讯作者:
Turner, James M. A.
Turner, James M. A.
中科院分区:
生物学2区
文献类型:
--
作者:
Guioli, Silvana;Lovell-Badge, Robin;Turner, James M. A.

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在雄性小鼠中,X和Y染色体配对并在小的假常染色体区域内重组。位于X和Y染色体未突触片段上的基因在粗线期被减数分裂性染色体失活(MSCI)转录沉默。MSCI在其他脊椎动物中的保守程度目前尚不清楚。在母鸡中,ZW二价体被认为在粗线期经历了一个完全突触的瞬时阶段,从同源末端开始,通过异源区域传播。有人提出,ZW DNA双链断裂(DSB)的修复被推迟到双线期,ZW二价体受到MSCI的影响,而MSCI不依赖于其突触状态。在这里,我们提出了一个独特的模式,减数分裂配对和沉默的ZW对在鸡的卵子发生。我们发现,在大多数卵母细胞中,ZW上的DNA DSB焦点在粗线期结束时被分解,ZW与常染色体广泛同步地去突触。我们意外地发现ZW配对非常容易出错,许多卵母细胞无法参与ZW突触和交叉形成。然而,具有未突触的Z和W染色体的卵母细胞仍进入双线期,这表明在鸡胚系的粗线期不存在检查点。结合表观遗传学和RNA-FISH分析,我们没有发现MSCI的证据,MSCI既不与哺乳动物中描述的非突触ZW相关,也不与突触ZW相关。鸡缺乏对MSCI的保护,重新引发了关于MSCI演变及其驱动力的辩论。
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.