The synaptonemal complex (SC) is a tripartite protein structure consisting of two parallel axial elements (AEs) and a central region. During meiosis, the SC connects paired homologous chromosomes, promoting interhomologue (IH) recombination. Here, we report that, like the CE component Zip1, Saccharomyces cerevisiae axial-element structural protein, Red1, can bind small ubiquitin-like modifier (SUMO) polymeric chains. The Red1–SUMO chain interaction is dispensable for the initiation of meiotic DNA recombination, but it is essential for Tel1- and Mec1-dependent Hop1 phosphorylation, which ensures IH recombination by preventing the inter-sister chromatid DNA repair pathway. Our results also indicate that Red1 and Zip1 may directly sandwich the SUMO chains to mediate SC assembly. We suggest that Red1 and SUMO chains function together to couple homologous recombination and Mec1–Tel1 kinase activation with chromosome synapsis during yeast meiosis.

The synaptonemal complex (SC) is a meiosis-specific tripartite structure that forms between two homologous chromosomes; it consists of a central region and two parallel lateral elements. Lateral elements also are called axial elements prior to synapsis. In Saccharomyces cerevisiae, Red1, Hop1, and Mek1 are structural components of axial/lateral elements. The red1/mek1/hop1 mutants all exhibit reduced levels of interhomolog recombination and produce no viable spores. Red1 is a phosphoprotein. Several earlier reports proposed that phosphorylated Red1 plays important roles in meiosis, including in signaling meiotic DNA damage or in preventing exit from the pachytene chromosomes. We report here that the phosphorylation of Red1 is carried out in CDC28-dependent and CDC28-independent manners. In contrast to previous results, we found Red1 phosphorylation to be independent of meiotic DNA recombination, the Mec1/Tel1 DNA damage checkpoint kinases, and the Mek1 kinase. To functionally validate the phosphorylation of Red1, we mapped the phosphorylation sites on this protein. A red1 14A mutant showing no detectable Red1 phosphorylation did not exhibit decreased sporulation efficiency, defects in viable spore production, or defects in meiotic DNA damage checkpoints. Thus, our results suggest that the phosphorylation of Red1 is not essential for its functions in meiosis.Meiosis is a critical component in the cycle of sexual reproduction, because it reduces the chromosome complement to haploidy in preparation for fertilization. This event is achieved by a single round of premeiotic DNA replication followed by two successive rounds of chromosome segregation to produce four haploid gametes. The first nuclear division (MI) is reductional, separating the newly recombined homologs from one another while leaving sister chromatids attached. The second nuclear division (MII), in which the sister chromatids segregate, is more typical of mitotic division and is called equational division. A prominent feature of meiosis is that pairing and recombination must occur between homologous chromosomes during the meiotic prophase. In contrast, these events rarely happen in mitosis. Meiotic DNA recombination plays a crucial role in meiosis, not only providing a potent source of genetic variation but also playing a mechanical role during MI. Specifically, crossover recombination results in a physical connection (i.e., chiasmata) between homologous chromosomes that allows them to orient properly on the spindle (for a review, see reference 59).Meiotic DNA recombination is initiated by the formation of DNA double-strand breaks (DSBs). Spo11, a meiosis-specific type II topoisomerase, generates DSBs together with several other factors in a cell cycle-programmed manner (26). The Mre11-Rad50-Xrs2 nuclease complex then resects these DSBs to generate 3Ј single-stranded tails that invade the intact DNA duplexes used for DNA repair (35). Most of these events use homologous chromosomes, not sister chromatids, as the templates for DNA repair to yield crossove...