The Synaptonemal Complex Central Region Modulates Crossover Pathways and Feedback Control of Meiotic Double-strand Break Formation

Abstract

The synaptonemal complex (SC) is a proteinaceous structure that mediates homolog engagement and genetic recombination during meiosis. Zip-Mer-Msh (ZMM) proteins promote crossover (CO) formation and initiate SC formation. In SC elongation, the SUMOylated SC component Ecm11 and its interacting protein Gmc2 facilitate the polymerization of Zip1, a SC-central region component in budding yeast. Through physical recombination, cytological, and genetic analyses, we here demonstrate that ecm11 and gmc2 mutants exhibit chromosome-specific defects in meiotic recombination. CO frequencies were reduced on a short chromosome (chromosome III), whereas CO and non-crossover (NCO) frequencies were increased on a long chromosome (chromosome VII). Further, persistent double-strand breaks (DSBs) occurred in unsynapsed chromosome regions during the late prophase, suggesting the presence of a negative regulation of DSB formation. The Ecm11-Gmc2 (EG) complex could participate in joint molecule (JM) processing and/or double-Holliday junction resolution for CO-designated recombination of the ZMM-dependent pathway. However, absence of the EG complex ameliorated the JM-processing defect in zmm mutants, suggesting a role of these proteins in suppression of ZMM-independent recombination. Therefore, the EG complex fosters ZMM-dependent processing and resolution of JMs while suppressing ZMM-independent JM processing and late DSB formation. Hence, EG-mediated SC central regions, which display properties similar to those of liquid crystals, may function as a compartment for sequestering recombination proteins in and out of the process to ensure meiosis specificity during recombination.