Abstract
Trisomy, the presence of a third copy of one chromosome, is deleterious and results in inviable or defective progeny if passed through the germ line. Random segregation of an extra chromosome is predicted to result in a high frequency of trisomic offspring from a trisomic parent. Caenorhabditis elegans with trisomy of the X chromosome, however, have far fewer trisomic offspring than expected. We found that the extra X chromosome was preferentially eliminated during anaphase I of female meiosis. We utilized a mutant with a specific defect in pairing of the X chromosome as a model to investigate the apparent bias against univalent inheritance. First, univalents lagged during anaphase I and their movement was biased toward the cortex and future polar body. Second, late-lagging univalents were frequently captured by the ingressing polar body contractile ring. The asymmetry of female meiosis can thus partially correct pre-existing trisomy.
Highlights
During female meiosis, a G2 oocyte containing four genome copies undergoes two asymmetric cell divisions depositing one genome in a single haploid egg, while the other three genomes are segregated into polar bodies
fluorescence in situ hybridization (FISH) with an X-specific probe revealed that in 6/6 metaphase II embryos with only 6 DAPIstaining bodies, a single hybridization signal was present in the spindle and 2–3 hybridization signals were present in the polar body (Figure 1D; Supplementary file 3)
Because only a single X-hybridization signal was observed in the first polar body in 5/5 spindles from diploids, these results demonstrate that single X univalents are deposited in the first polar body with greater than 50% frequency
Summary
A G2 oocyte containing four genome copies undergoes two asymmetric cell divisions depositing one genome in a single haploid egg, while the other three genomes are segregated into polar bodies. These divisions are mediated by meiotic spindles that are asymmetrically positioned against the oocyte cortex with the pole-to-pole axis of the spindle perpendicular to the cortex. Both the inheritance of only one of the four genome copies and the distinct perpendicular positioning of the meiotic spindle are remarkably conserved among animal phyla suggesting a selective advantage (Maro and Verlhac, 2002; Fabritius et al, 2011a; Maddox et al, 2012). We suggest a previously unrecognized advantage of asymmetric meiosis, the ability of meiotic spindles to correct trisomy by preferentially depositing the extra chromosome copy into a polar body
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