Pattabiraman Divya, Roelens Baptiste, Woglar Alexander, Villeneuve Anne M
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California, United States of America.
PLoS Genet. 2017 Mar 24;13(3):e1006670. doi: 10.1371/journal.pgen.1006670. eCollection 2017 Mar.
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.
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齐对的界面处组装，并且在它们的DNA分子之间发生交叉重组事件。在这里，我们研究了线虫秀丽隐杆线虫减数分裂程序的这两个标志性特征之间的相互关系，揭示了受重组调节的SC的动态特性。我们证明，随着生殖细胞在减数分裂前期的粗线期阶段的进展，SC纳入新的亚基并从更高动态/不稳定状态转变为更稳定状态。我们进一步表明，在减数分裂重组受损的突变体中，SC的更动态状态会延长。此外，在重组中间体数量有限的减数分裂突变体中，SC中央区域亚基优先稳定在携带前交叉因子COSA-1和MutSγ集中位点的染色体对的子集上。在SC中央区域蛋白在此类染色体上富集之前，类Polo样激酶PLK-2优先定位于携带重组位点的染色体对的SCs上，并且这种富集的发生需要PLK-2。此外，plk-2突变体中的晚粗线期细胞核表现出更高动态的SC状态。我们的数据共同表明，交叉重组事件对SC产生染色体自主稳定作用，并在此过程中涉及PLK-2。我们讨论了这种由重组触发的SC状态调节如何可能有助于在减数分裂期间起作用的调节机制，以确保交叉的形成，同时限制它们的数量。
