Abstract
Chromosome segregation during male meiosis is tailored to rapidly generate multitudes of sperm. Little is known about mechanisms that efficiently partition chromosomes to produce sperm. Using live imaging and tomographic reconstructions of spermatocyte meiotic spindles in Caenorhabditis elegans, we find the lagging X chromosome, a distinctive feature of anaphase I in C. elegans males, is due to lack of chromosome pairing. The unpaired chromosome remains tethered to centrosomes by lengthening kinetochore microtubules, which are under tension, suggesting that a 'tug of war' reliably resolves lagging. We find spermatocytes exhibit simultaneous pole-to-chromosome shortening (anaphase A) and pole-to-pole elongation (anaphase B). Electron tomography unexpectedly revealed spermatocyte anaphase A does not stem solely from kinetochore microtubule shortening. Instead, movement of autosomes is largely driven by distance change between chromosomes, microtubules, and centrosomes upon tension release during anaphase. Overall, we define novel features that segregate both lagging and paired chromosomes for optimal sperm production.
Highlights
Chromosome segregation during meiosis is regulated in each sex to produce different numbers of cells with distinct size, shape, and function
While oocyte meiosis and mitosis have been studied in detail in many organisms (Bennabi et al, 2016; Muller-Reichert et al, 2010; Pintard and Bowerman, 2019), our knowledge of sperm meiotic chromosome segregation is still limited to studies in grasshoppers and crane flies using chromosome manipulation and laser microsurgery (LaFountain et al, 2011; LaFountain et al, 2012; Nicklas and Kubai, 1985; Nicklas et al, 2001; Zhang and Nicklas, 1995)
Spermatocyte meiotic spindles are distinguished by delayed segregation of the unpaired X chromosome
Summary
Chromosome segregation during meiosis is regulated in each sex to produce different numbers of cells with distinct size, shape, and function. Electron microscopy has defined the microtubule organization in female meiotic (Laband et al, 2017; Redemann et al, 2018; Srayko et al, 2006; Yu et al, 2019) and embryonic mitotic spindles (Albertson, 1984; O’Toole et al, 2003; Redemann et al, 2017; Yu et al, 2019) but a detailed study on spindle ultrastructure in spermatocytes, at anaphase I showing the lagging X chromosome, is lacking. To better understand sex-specific regulation of meiotic chromosome segregation and the resolution of lagging chromosomes, we quantitatively characterized the three-dimensional (3D) organization of spindles and the dynamics of chromosomes in C. elegans male spermatocytes. Our approach defines molecular mechanisms of sperm-specific movements, focusing on the efficient segregation of both lagging and paired chromosomes
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
