Crossover recombination and synapsis are linked by adjacent regions within the N terminus of the Zip1 synaptonemal complex protein

Abstract

Accurate chromosome segregation during meiosis relies on the prior establishment of at least one crossover recombination event between homologous chromosomes. Most meiotic recombination intermediates that give rise to interhomolog crossovers are embedded within a hallmark chromosomal structure called the synaptonemal complex (SC), but the mechanisms that coordinate the processes of SC assembly (synapsis) and crossover recombination remain poorly understood. Among known structural components of the budding yeast SC, the Zip1 protein is unique for its independent role in promoting crossover recombination; Zip1 is specifically required for the large subset of crossovers that also rely on the meiosis-specific MutSγ complex. Here we report that adjacent regions within Zip1’s N terminus encompass its crossover and synapsis functions. We previously showed that deletion of Zip1 residues 21–163 abolishes tripartite SC assembly and prevents robust SUMOylation of the SC central element component, Ecm11, but allows excess MutSγ crossover recombination. We find the reciprocal phenotype when Zip1 residues 2–9 or 10–14 are deleted; in these mutants SC assembles and Ecm11 is hyperSUMOylated, but MutSγ crossovers are strongly diminished. Interestingly, Zip1 residues 2–9 or 2–14 are required for the normal localization of Zip3, a putative E3 SUMO ligase and pro-MutSγ crossover factor, to Zip1 polycomplex structures and to recombination initiation sites. By contrast, deletion of Zip1 residues 15–20 does not detectably prevent Zip3’s localization at Zip1 polycomplex and supports some MutSγ crossing over but prevents normal SC assembly and Ecm11 SUMOylation. Our results highlight distinct N terminal regions that are differentially critical for Zip1’s roles in crossing over and SC assembly; we speculate that the adjacency of these regions enables Zip1 to serve as a liaison, facilitating crosstalk between the two processes by bringing crossover recombination and synapsis factors within close proximity of one another.

Meiotic budding yeast assemble bundled triple helices but not ladders

“…Two known yeast central-element proteins, Ecm11 and Gcm2 (Voelkel-Meiman et al, 2013), may form complexes are either too small or too skinny to be detected in our data. Our data could not definitively reveal which densities belong to the LEs, which flank the CR (Voelkel-Meiman et al, 2013;Voelkel-Meiman et al, 2019). While treatment with high concentrations of 1,6hexanediol leaves thinner protein filaments intact, there is insufficient evidence for their assignment as LE subunits.…”

Meiosis-Specific Functions of Kinesin Motors in Cohesin Removal and Maintenance of Chromosome Integrity in Budding Yeast

“…S1B at the URL mentioned above). These results suggest that Cin8 and Kip3 together are involved in force generation on the chromosomes toward the opposite spindle poles, which is consistent with the fact that these motors have microtubule cross-linking (19,20,38,82) and depolymerase (28,37,38) activities. Therefore, in cin8Δ kip3Δ meiotic cells, the homologs and, thus, the sisters are not under tension in meiosis I and meiosis II, respectively.…”

Synaptonemal Complex dimerization regulates chromosome alignment and crossover patterning in meiosis

“…The contributions of other domains to specific functions or structural features are much less clear. For example, the ability of the SC to hold paired axes together was suggested to involve, based on in vitro analysis, dimerization and cooperative assembly of the N-terminus of the mammalian transverse filament protein SYCP1 [17], and based on genetic data, the N-terminus of budding yeast Zip1p [25,26]. However, while several genetic perturbations in C. elegans cause the SC to be associated with all chromosomes without holding paired axes together [10,27,28], the molecular details underlying pairing interactions have not been elucidated.…”