Multilayered mechanisms ensure that short chromosomes recombine in meiosis

To segregate accurately during meiosis in most species, homologous chromosomes must recombine(1). Small chromosomes would risk missegregation if recombination were randomly distributed, so the double-strand breaks (DSBs) initiating recombination are not haphazard(2). How this nonrandomness is controlled is not understood, although several pathways ensuring that DSBs occur at the appropriate time, number, and place are known. Meiotic DSBs are made by Spo11 and accessory “DSB proteins,” including Rec114 and Mer2, which assemble on chromosomes(3–7) and are nearly universal in eukaryotes(8–11). Here we demonstrate how Saccharomyces cerevisiae integrates multiple temporally distinct pathways to regulate chromosomal binding of Rec114 and Mer2, thereby controlling the duration of a DSB-competent state. Engagement of homologous chromosomes with one another regulates the dissociation of Rec114/Mer2 later in prophase I, whereas replication timing and proximity to centromeres or telomeres influence Rec114/Mer2 accumulation early. Another early mechanism boosts Rec114/Mer2 binding specifically on the shortest chromosomes, subject to selection pressure to maintain hyperrecombinogenic properties of these chromosomes. Thus, an organism’s karyotype and risk of meiotic missegregation influence the shape and evolution of its recombination landscape. Our results create a cohesive view of a multifaceted and evolutionarily constrained system that ensures DSB allocation to all pairs of homologous chromosomes.