Synaptonemal complex proteins direct and constrain the localization of crossover-promoting proteins duringCaenorhabditis elegansmeiosis

Abstract

Crossovers (COs) between homologous chromosomes are critical for meiotic chromosome segregation and form in the context of the synaptonemal complex (SC), a meiosis-specific structure that assembles between aligned homologs. During Caenorhabditis elegans meiosis, central region components of the SC (SYP proteins) are essential to repair double-strand DNA breaks (DSBs) as COs, but the roles of these SYP proteins in promoting CO formation are poorly understood. Here, we investigate the relationships between the SYP proteins and conserved CO-promoting factors by examining the immunolocalization of these factors in meiotic mutants where SYP proteins are absent, reduced, or mis-localized. Although COs do not form in syp null mutants, CO-promoting proteins COSA-1, MSH-5, and ZHP-3 nevertheless become co-localized at a variable number of DSB-dependent sites during late prophase, reflecting an inherent affinity of these factors for DSB repair sites. In contrast, in mutants where SYP proteins are present but form aggregates or display abnormal synapsis, CO-promoting proteins consistently track with SYP-1 localization. Moreover, CO-promoting proteins usually localize to a single site per SYP-1 structure, even in SYP aggregates or in mutants where SC forms between sister-chromatids, suggesting that CO regulation occurs within these structures. Further, we find that sister chromatids in the meiotic cohesin mutant rec-8 require both CO-promoting proteins and the SC to remain connected. Taken together, our findings support a model in which SYP proteins promote CO formation by directing and constraining the localization of CO-promoting factors to ensure that CO maturation occurs only between properly aligned homologous chromosomes.

Chromosome segregation during spermatogenesis occurs through a unique center-kinetic mechanism in holocentric moth species

“…In C. elegans, this structure is achieved via crossover regulation. Crossovers in C. elegans are almost always limited to one per chromosome, and these crossovers form in one of the two distal arm-like regions [55][56][57][58][59][60]. The arm-like region of the homologs with the chiasma remains connected and is positioned along the metaphase I plate, while the opposite arm-like region points out toward the spindle poles [16,31,[61][62][63].…”