Meiotic DNA exchanges are promoted by proximity to the synaptonemal complex

Abstract

During meiosis, programmed double strand DNA breaks are repaired to form exchanges between the parental chromosomes called crossovers. Chromosomes lacking a crossover fail to segregate accurately into the gametes, leading to aneuploidy. Crossover formation requires the promotion of exchanges, rather than non-exchanges, as repair products. However, the mechanism underlying this meiosis-specific preference is not fully understood. Here, we study the regulation of meiotic sister chromatid exchanges in Caenorhabditis elegans by direct visualization. We find that a conserved chromosomal interface that promotes exchanges between the parental chromosomes, the synaptonemal complex, also promotes exchanges between the sister chromatids. In both cases, exchanges depend on recruitment of the same set of pro-exchange factors to repair sites. Surprisingly, while the synaptonemal complex usually assembles between the two DNA molecules undergoing an exchange, its activity does not rely on a specific chromosome conformation and it can also promote sister exchanges when assembling next to the sisters. This suggests that the synaptonemal complex regulates exchanges by establishing a nuclear domain conducive to nearby coalescence of exchange-promoting factors.