Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis.
Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis.
复制标题
DOI：
10.1371/journal.pgen.1006670
复制
发表时间：
2017-03
期刊：
影响因子：
4.5
通讯作者：
Villeneuve AM
中科院分区：
文献类型：
--
作者：
Pattabiraman D;Roelens B;Woglar A;Villeneuve AM
在减数分裂前期，一种称为联会复合体（SC）的结构在同源染色体对之间的界面组装，并且在它们的DNA分子之间发生交叉重组事件。在这里，我们研究了线虫C中减数分裂程序的这两个标志性特征之间的相互关系。elegans，揭示了动态特性的SC调制重组。我们证明，SC纳入新的亚基和开关从一个更高的动态/不稳定的状态，以更稳定的状态作为生殖细胞的进展，通过粗线期阶段的减数分裂前期。我们进一步表明，更多的动态状态的SC延长突变体减数分裂重组受损。此外，在减数分裂突变体中，重组中间体以有限的数量存在，SC中心区亚基优先稳定在染色体对的子集上，这些染色体对含有促交换因子COSA-1和MutSγ集中的位点。Polo样激酶PLK-2在SC中心区蛋白富集在染色体上之前优先定位于含有重组位点的染色体对的SC，并且PLK-2是这种富集发生所必需的。此外，plk-2突变体中的晚粗线期细胞核表现出更高的动态SC状态。我们的数据共同表明，交叉重组事件会对SC产生染色体自主稳定效应，并在此过程中涉及PLK-2。我们讨论了如何重组触发调制SC状态可能有助于调节机制，在减数分裂过程中，以确保形成的交叉，而在同一时间限制其数量。有性生殖过程中可靠的染色体遗传依赖于同源染色体之间临时连接的形成，这些连接使它们能够在减数分裂I分裂时向相反的纺锤体两极分离。这些连接是在延长的减数分裂前期建立的，其特征在于两个突出的特征：一种高度有序的结构，称为联会复合体（SC），其在对齐的染色体对之间的界面处组装，以及在SC的背景下完成的它们的DNA分子之间的交叉重组事件。在目前的工作中，我们研究了线虫C.优雅的我们的工作揭示了C. elegans SC的结构比EM图像中高度有序的外观所表明的更具动态性，并进一步证明随着生殖细胞通过减数分裂前期的进展，SC从更高度动态/不稳定的状态切换到更稳定的状态。此外，我们表明，交叉重组中间体的形成可以触发稳定的SC在染色体自主的方式。我们推测，重组触发的SC稳定可能提供了一种手段，生殖细胞监测染色体对是否已获得必要的交叉中间体，以确保正确的同源分离。
During meiotic prophase, a structure called the synaptonemal complex (SC) assembles at the interface between aligned pairs of homologous chromosomes, and crossover recombination events occur between their DNA molecules. Here we investigate the inter-relationships between these two hallmark features of the meiotic program in the nematode C. elegans, revealing dynamic properties of the SC that are modulated by recombination. We demonstrate that the SC incorporates new subunits and switches from a more highly dynamic/labile state to a more stable state as germ cells progress through the pachytene stage of meiotic prophase. We further show that the more dynamic state of the SC is prolonged in mutants where meiotic recombination is impaired. Moreover, in meiotic mutants where recombination intermediates are present in limiting numbers, SC central region subunits become preferentially stabilized on the subset of chromosome pairs that harbor a site where pro-crossover factors COSA-1 and MutSγ are concentrated. Polo-like kinase PLK-2 becomes preferentially localized to the SCs of chromosome pairs harboring recombination sites prior to the enrichment of SC central region proteins on such chromosomes, and PLK-2 is required for this enrichment to occur. Further, late pachytene nuclei in a plk-2 mutant exhibit the more highly dynamic SC state. Together our data demonstrate that crossover recombination events elicit chromosome-autonomous stabilizing effects on the SC and implicate PLK-2 in this process. We discuss how this recombination-triggered modulation of SC state might contribute to regulatory mechanisms that operate during meiosis to ensure the formation of crossovers while at the same time limiting their numbers. Reliable chromosome inheritance during sexual reproduction depends on the formation of temporary connections between homologous chromosomes that enable them to segregate toward opposite spindle poles at the meiosis I division. These connections are established during an extended meiotic prophase characterized by two prominent features: a highly-ordered structure called the synaptonemal complex (SC) that assembles at the interface between aligned pairs of chromosomes, and crossover recombination events between their DNA molecules that are completed in the context of the SC. In the current work, we investigate the inter-relationships between these two hallmark features of the meiotic program in the nematode C. elegans. Our work reveals the C. elegans SC as a much more dynamic structure than is suggested by its highly-ordered appearance in EM images, and further demonstrates that the SC switches from a more highly dynamic/labile state to a more stable state as germ cells progress through meiotic prophase. Moreover, we show that formation of crossover recombination intermediates can trigger stabilization of the SC in a chromosome autonomous manner. We speculate that recombination-triggered SC stabilization may provide a means for germ cells to monitor whether chromosome pairs have acquired the prerequisite crossover intermediate needed to ensure correct homolog segregation.