In meiosis, germ cells undergo two meiotic chromosome segregation events to generate haploid gametes. While many events during chromosome segregation are similar in both sperm and oocyte meiosis, there are key features that are unique to sperm. In spermatogenesis, cell division is symmetrical, and sperm spindle microtubules are organized by centrosomes. We report here that sperm have unique kinetochore composition, dynamics, and regulation in C. elegans. Another distinct feature are the sperm-specific PP1 phosphatases GSP-3/4 –key regulatory proteins during sperm meiotic chromosome segregation. gsp-3/4 mutant males have defects in anaphase I, which takes nearly twice as long to complete when compared to wildtype sperm. In meiosis II, sister chromatids fail to segregate resulting in sperm aneuploidy. It is unclear what targets GSP-3/4 are regulating, or the reason for the segregation defects. One clue is that GSP-3/4 localize to chromosomes in a pattern similar to that of kinetochore components. Interestingly, kinetochore composition is different in sperm when compared to oocytes. Sperm inner kinetochores lack HCP-3 (CENP-A) and are enriched with HCP-4 (CENP-C), while oocyte kinetochores are composed of both. Furthermore, outer kinetochores in oocytes have two CENP-F proteins, HCP-1 and HCP-2, while sperm only rely on HCP-2. Using immunostaining, we show the outer kinetochore protein HCP-2, as well as NDC-80 and KNL-3, have distinct dynamics during sperm chromosome segregation. In oocyte meiosis, outer kinetochore components move between segregating chromosomes in anaphase I. In sperm meiosis, kinetochore proteins remain localized to chromosomes as they segregate. Furthermore, we show that these kinetochore components are dependent on the regulation of the sperm-specific PP1 phosphatases. In gsp-3/4 mutant males, we see a mislocalization of HCP-2, NDC-80 and KNL-3 during anaphase I and meiosis II. This defect is consistent with the timing of the segregation defect previously described. Simultaneously, microtubule-associated protein CLASP-2 also shows a defect in gsp-3/4 mutants, further supporting outer kinetochore function is compromised. Taken together these results support that sperm-specific features of kinetochore components are regulated by the sperm-specific PP1 phosphatases. .
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