Chromosome segregation in sperm has unique features that make it different from oocyte meiosis. Oocytes undergo two rounds of asymmetrical chromosome segregation without centrosomes, while sperm have symmetrical divisions and utilize centrosomes to organize microtubule attachment to chromosomes. This attachment is mediated by a protein complex called the kinetochore, but the role of the kinetochore during sperm meiosis remains poorly understood. We report here that sperm-specific phosphatases GSP-3/4 may regulate kinetochore-microtubule connection to organize sister chromatid orientation from segregating to the same pole in meiosis I to opposite poles in meiosis II.
gsp-3/4 mutant sperm exhibit delayed resolution of a univalent lagging X chromosome and sisters fail to separate. Therefore, I hypothesize that sperm uniquely require kinetochore-microtubule attachment/detachment and GSP-3/4 regulate detachment. Interestingly, GSP-3/4 localize in a kinetochore-like pattern, which suggests these phosphatases may regulate kinetochore function. Sperm also have distinct outer kinetochore localization patterns (KNL-1, KNL-3, and NDC-80), compared to oocytes. For example, similar to oocyte meiosis, KNL-1 and KNL-3 localize in a cup shape on chromosomes, but NDC-80 surrounds chromosomes only in sperm. A bigger difference between oocyte and sperm meiosis is kinetochore presence at anaphase. In oocytes, immunofluorescence results depicted the kinetochore disassembles from chromosomes during anaphase I. However, the kinetochore is retained during anaphase in sperm suggesting kinetochore importance for chromosome segregation. The question still remains, do kinetochores mediate the connection between chromosomes and microtubules in sperm? Recent super-resolution images of immunostained sperm in anaphase I show there is a gap between chromosomes and microtubules where NDC-80 localizes, indicating the kinetochore functions in sperm meiosis to connect chromosomes to microtubules during anaphase separation. Further, live imaging of H2B labeled DNA and GFP labeled tubulin show that sperm meiosis exhibits pole-chromosome shortening (anaphase A) in anaphase I, which contrast to oocyte meiosis and mitosis, which rely on anaphase B mechanisms. This result taken together with the
gsp-3/4 mutant phenotypes of delayed lagging X resolution and sister separation failure, support GSP-3/4 role in detaching microtubules from kinetochores. GSP-3/4-regulated detachment would allow X resolution and sisters to shift orientation towards opposite poles. Microtubule detachment from kinetochores may be unique in sperm to reconcile the combination of centrosome organized microtubules and chromosomes going through two rounds of segregation.