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

Abstract

Meiosis 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.

Challenges and costs of asexuality: Variation in premeiotic genome duplication in gynogenetic hybrids from Cobitis taenia complex

“…Differences between sexes in meiotic checkpoints were also observed in other organisms, but the patterns somewhat contradict each other (Fielder et al, 2020; Kurahashi et al, 2012; Lane and Kauppi, 2019). For example, the hybrids between Medaka fish Oryzias latipes × O. curvinotus showed similar patterns to Cobitis since oocytes with aberrantly paired chromosomes could not proceed beyond pachytene, while spermatocytes with aberrant pairing did not disrupt meiotic prophase but also progressed to metaphase 1 meiosis (Shimizu et al, 2000, 1997).…”

“…Spindle assembly checkpoint machinery assesses the stringency of the spindle in each bivalent and allows progression beyond metaphase only when all bivalents are correctly arranged (Lane and Kauppi, 2019; Musacchio and Salmon, 2007). Thus, meiotic progression in male hybrids is prevented at later stages by the failure of the equal stringency from the spindle caused by univalents (Burgoyne et al, 2009; Eaker et al, 2002).Differences between sexes in meiotic checkpoints were also observed in other organisms, but the patterns somewhat contradict each other(Fielder et al, 2020;Kurahashi et al, 2012;Lane and Kauppi, 2019). For example, the hybrids between Medaka fish Oryzias latipes × O. curvinotus showed similar patterns to Cobitis since oocytes with aberrantly paired chromosomes could not proceed beyond pachytene, while spermatocytes with aberrant pairing did not disrupt meiotic prophase but also progressed to metaphase 1 meiosis(Shimizu et al, 2000(Shimizu et al, , 1997.…”

Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori

“…In C. elegans, either telomere on any given chromosome can harbor kinetochore activity, and both do so with equal probability, depending on where crossovers form during meiotic prophase I [42,48]. Additionally, this telokinetic kinetochore activity is independent of the centromere-specifying histone CENP-A [46,50,54].…”

“…Furthermore, meiotic segregation in C. elegans occurs in the absence of the centromere-specifying factor Centromere Protein A (CENP-A) [50]. Instead, microtubules either run parallel to chromosomes to facilitate segregation or connect directly to cup-shaped kinetochores that form at chromosome ends [46,54]. Interestingly, CENP-A is entirely absent from the genomes of butterflies and moths [55].…”

Oligopaint DNA FISH as a tool for investigating meiotic chromosome dynamics in the silkworm,Bombyx mori

“…A similar telokinetic mechanism for segregation meiotic chromosomes was also previously hypothesized to occur in B. mori (52)(53)(54) but has never before been directly observed. Furthermore, meiotic segregation in C. elegans occurs in the absence of the centromere-specifying factor Centromere Protein A (CENP-A) (51), and instead, microtubules either run parallel to chromosomes to facilitate segregation or directly penetrate chromosome ends (47,55). Interestingly, CENP-A is entirely absent from the genomes of butterflies and moths (56).…”