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

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 MutS gamma 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 MutS gamma 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 MutS gamma 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-MutS gamma 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 MutS gamma 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. Author summary Reproductive cell formation relies on a nuclear division cycle called meiosis, wherein two homologous sets of chromosomes are reduced to one. At the crux of (and critically required for) meiotic chromosome segregation is a transient association between homologous chromosomes established by a crossover recombination event. Recombination intermediates embed within a 100 nm wide proteinaceous structure that connects aligned homologous axes, the synaptonemal complex (SC). While genetic data implicate certain SC structural proteins in crossover formation, it is unclear how such coiled-coil, rod-like proteins carry out their recombination function. Our structure-function analysis of the yeast SC transverse filament protein, Zip1, reveals pro-crossover and pro-synapsis functions that are encompassed by adjacent N terminal regions. We also discovered that the pro-crossover region of Zip1 promotes proper localization of pro-crossover factor and putative SUMO ligase, Zip3, to meiotic recombination sites. Zip3 is known to not only promote crossovers but also to influence the post-translational modification of another SC structural component, Ecm11, which is dispensable for crossovers. Our findings raise the possibility that Zip1's N terminus acts as a liaison to connect pro-crossover factors (like Zip3) to SC assembly proteins (such as Ecm11) in order to coordinate the two landmark meiotic chromosomal processes.