The Ecm11-Gmc2 Complex Promotes Synaptonemal Complex Formation through Assembly of Transverse Filaments in Budding Yeast

During meiosis, homologous chromosomes pair at close proximity to form the synaptonemal complex (SC). This association is mediated by transverse filament proteins that hold the axes of homologous chromosomes together along their entire length. Transverse filament proteins are highly aggregative and can form an aberrant aggregate called the polycomplex that is unassociated with chromosomes. Here, we show that the Ecm11-Gmc2 complex is a novel SC component, functioning to facilitate assembly of the yeast transverse filament protein, Zip1. Ecm11 and Gmc2 initially localize to the synapsis initiation sites, then throughout the synapsed regions of paired homologous chromosomes. The absence of either Ecm11 or Gmc2 substantially compromises the chromosomal assembly of Zip1 as well as polycomplex formation, indicating that the complex is required for extensive Zip1 polymerization. We also show that Ecm11 is SUMOylated in a Gmc2-dependent manner. Remarkably, in the unSUMOylatable ecm11 mutant, assembly of chromosomal Zip1 remained compromised while polycomplex formation became frequent. We propose that the Ecm11-Gmc2 complex facilitates the assembly of Zip1 and that SUMOylation of Ecm11 is critical for ensuring chromosomal assembly of Zip1, thus suppressing polycomplex formation.

在减数分裂过程中，同源染色体将在紧密邻近的区域内配对，形成联会复合体（synaptonemal complex, SC）。该结合过程由横向丝蛋白介导，这类蛋白可将同源染色体的轴沿其全长紧密结合在一起。横向丝蛋白具有高度的聚集倾向，可形成一种不与染色体结合的异常聚集体，即多聚复合体（polycomplex）。本研究表明，Ecm11-Gmc2复合体是一种新型的SC组分，其功能是促进酵母横向丝蛋白Zip1的组装。Ecm11与Gmc2最初定位于联会起始位点，随后分布于配对同源染色体的联会区域中。若缺失Ecm11或Gmc2，均会显著破坏Zip1在染色体上的组装以及多聚复合体的形成，这提示该复合体对于Zip1的大规模聚合是必需的。本研究还证实，Ecm11会以Gmc2依赖的方式发生SUMO化修饰（SUMOylation）。值得注意的是，在无法发生SUMO化修饰的ecm11突变体中，Zip1在染色体上的组装仍受到破坏，但多聚复合体的形成却变得频繁。我们据此提出，Ecm11-Gmc2复合体可促进Zip1的组装，而Ecm11的SUMO化修饰对于确保Zip1在染色体上的正常组装、进而抑制多聚复合体的形成至关重要。