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

摘要

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. Author Summary Meiosis is central to the life cycle of sexually reproducing organisms. The first round of division (meiosis I) is unique to meiosis in that homologous chromosomes are segregated to opposite poles. The tight association between homologous chromosomes is essential for their faithful segregation. To establish such association, meiosis employs a unique, homologous recombination-dependent mechanism that facilitates the recognition, association, and reciprocal exchange of DNA strands of homologous chromosomes, thus providing physical connections between homologous chromosomes. All these events take place in the context of an intricate structure called the synaptonemal complex (SC). Within this complex, the axis of one chromosome is aligned at close proximity with the axis of its homologue. This alignment stretches along the entire length of the chromosome pair, with zipper-like structures, called transverse filaments, holding axes together. In this work, we identified the Ecm11-Gmc2 complex as a novel component of the SC, promoting the assembly of transverse filaments. Importantly, we demonstrate that post-translational modification of Ecm11 with SUMO (small ubiquitin-like modifier) is critical for ensuring the chromosomal loading of transverse filaments. Thus, our work provides a molecular basis for how homologous chromosomes become tightly associated during meiotic prophase.