Meiotic Nuclear Oscillations Are Necessary to Avoid Excessive Chromosome Associations

• Published in: Cell reports (Cambridge) 2016-11, Vol.17 (6), p.1632-1645
• Main Authors: Chacón, Mariola R., Delivani, Petrina, Tolić, Iva M.
• Format: Article
• Language: English
• Subjects: Cell Nucleus - metabolism; chromosome missegregation; Chromosome Pairing; Chromosome Segregation; Chromosomes, Fungal - metabolism; double-strand breaks; Genetic Loci; Green Fluorescent Proteins - metabolism; Holliday Junction Resolvases; horsetail movement; Meiosis; meiotic prophase; Mus81; nuclear oscillations; Rec25; recombination; Schizosaccharomyces - cytology; Schizosaccharomyces - genetics; Schizosaccharomyces - metabolism; Schizosaccharomyces pombe Proteins - metabolism; Spindle Pole Bodies - metabolism; Time-Lapse Imaging
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2016.10.014

Pairing of homologous chromosomes is a crucial step in meiosis, which in fission yeast depends on nuclear oscillations. However, how nuclear oscillations help pairing is unknown. Here, we show that homologous loci typically pair when the spindle pole body is at the cell pole and the nucleus is elongated, whereas they unpair when the spindle pole body is in the cell center and the nucleus is round. Inhibition of oscillations demonstrated that movement is required for initial pairing and that prolonged association of loci leads to mis-segregation. The double-strand break marker Rec25 accumulates in elongated nuclei, indicating that prolonged chromosome stretching triggers recombinatory pathways leading to mis-segregation. Mis-segregation is rescued by overexpression of the Holliday junction resolvase Mus81, suggesting that prolonged pairing results in irresolvable recombination intermediates. We conclude that nuclear oscillations exhibit a dual role, promoting initial pairing and restricting the time of chromosome associations to ensure proper segregation. [Display omitted] •Nuclear oscillations promote the dynamics of homologous loci in meiotic prophase•The first pairing events of homologous loci require nuclear movement•Prolonged chromosome pairing is accompanied by mis-segregation•Mis-segregation is rescued by Mus81 overexpression Chacón et al. find that meiotic nuclear oscillations have a dual role in chromosome dynamics. They enable proper spatial alignment of homologous chromosomes for their initial pairing and favor pairing/unpairing dynamics that prevent excessive chromosome connections and mis-segregation.