Centromere-Proximal Meiotic Crossovers in Drosophila melanogaster Are Suppressed by Both Highly Repetitive Heterochromatin and Proximity to the Centromere

Abstract

Crossovers are essential for the accurate segregation of chromosomes, but it is important that they be properly positioned. Crossovers must not occur too close to the centromere, but reduced crossover density may extend outward for some distance... Crossovers are essential in meiosis of most organisms to ensure the proper segregation of chromosomes, but improper placement of crossovers can result in nondisjunction and aneuploidy in progeny. In particular, crossovers near the centromere can cause nondisjunction. Centromere-proximal crossovers are suppressed by what is termed the centromere effect, but the mechanism is unknown. Here, we investigate contributions to centromere-proximal crossover suppression in Drosophila melanogaster. We mapped a large number of centromere-proximal crossovers, and find that crossovers are essentially absent from the highly repetitive (HR)-heterochromatin surrounding the centromere but occur at a low frequency within the less-repetitive (LR)-heterochromatic region and adjacent euchromatin. Previous research suggested that flies that lack the Bloom syndrome helicase (Blm) lose meiotic crossover patterning, including the centromere effect. Mapping of centromere-proximal crossovers in Blm mutants reveals that the suppression within the HR-heterochromatin is intact, but the distance-dependent centromere effect is lost. We conclude that centromere-proximal crossovers are suppressed by two separable mechanisms: an HR-heterochromatin effect that completely suppresses crossovers in the HR-heterochromatin, and the centromere effect, which suppresses crossovers with a dissipating effect with distance from the centromere.