Multiple Sex-Specific Differences in the Regulation of Meiotic Progression in C. elegans

ABSTRACTMeiosis is a highly conserved sexual process, yet significant differences exist between males and females in meiotic regulation in many species. Meiotic progression in C. elegans males proceeds more rapidly than female meiosis, suggesting that female meiotic regulation may be more stringent than in males. We have identified multiple differences in the regulation of synapsis, including a difference that suggests the presence of a female-specific meiotic checkpoint that senses the proper initiation of synapsis. This checkpoint is detected by sex differences in the targeting of histone H3 lysine 9 dimethylation (H3K9me2) to unsynapsed chromatin. During oogenic meiosis in hermaphrodites, the failure to initiate synapsis leads to failure to target H3K9me2 enrichment on unsynapsed chromosomes. Loss of the pachytene checkpoint does not reintroduce H3K9me2 enrichment in hermaphrodites, indicating these checkpoints are separable. In contrast, widespread H3K9me2 enrichment occurs as a result of loss of synapsis initiation in both male meiosis and during spermatogenic meiosis in larval XX hermaphrodites. Additionally, male synapsis is insensitive to loss of the dynein motor light chain DLC-1 and to elevated temperatures, whereas female synapsis is prevented by both conditions. We also show that loss of spindle assembly checkpoint proteins, which provide a kinetic barrier to meiotic progression and are required for DLC-1-dependent synapsis phenotypes in hermaphrodites, does not speed up the rate of synapsis in spermatogenic meiosis. These results indicate that meiosis proceeds more rapidly in males because males lack barriers to meiotic progression that are activated by defective synapsis initiation in females.