Abstract

During meiotic prophase, telomeres cluster, forming the bouquet chromosome arrangement, and facilitate homologous chromosome pairing. In fission yeast, bouquet formation requires switching of telomere and centromere positions. Centromeres are located at the spindle pole body (SPB) during mitotic interphase, and upon entering meiosis, telomeres cluster at the SPB, followed by centromere detachment from the SPB. Telomere clustering depends on the formation of the microtubule-organizing center at telomeres by the linker of nucleoskeleton and cytoskeleton complex (LINC), while centromere detachment depends on disassembly of kinetochores, which induces meiotic centromere formation. However, how the switching of telomere and centromere positions occurs during bouquet formation is not fully understood. Here, we show that, when impaired telomere interaction with the LINC or microtubule disruption inhibited telomere clustering, kinetochore disassembly-dependent centromere detachment and accompanying meiotic centromere formation were also inhibited. Efficient centromere detachment required telomere clustering-dependent SPB recruitment of a conserved telomere component, Taz1, and microtubules. Furthermore, when artificial SPB recruitment of Taz1 induced centromere detachment in telomere clustering-defective cells, spindle formation was impaired. Thus, detachment of centromeres from the SPB without telomere clustering causes spindle impairment. These findings establish novel regulatory mechanisms, which prevent concurrent detachment of telomeres and centromeres from the SPB during bouquet formation and secure proper meiotic divisions.

Highlights

  • Chromosome positioning changes dynamically during development and differentiation, and contributes to various chromosomal events including gene expression and DNA metabolism [1,2,3,4,5]

  • Telomeres cluster on a small region of the nuclear periphery, PLOS Genetics | DOI:10.1371/journal.pgen

  • To explore the relationship between telomere clustering and centromere detachment in bouquet formation, we examined telomere and centromere positioning during karyogamy and the horsetail stage in telomere clustering-defective cells

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Summary

Introduction

Chromosome positioning changes dynamically during development and differentiation, and contributes to various chromosomal events including gene expression and DNA metabolism [1,2,3,4,5]. During meiosis, chromosomes adopt a characteristic position called the “bouquet” arrangement, in which telomeres cluster at the nuclear periphery. Studies of various organisms show that the bouquet arrangement facilitates homologous chromosome pairing [7,8,9]. In Caenorhabditis elegans, special chromosome regions called “pairing centers” cluster instead of telomeres, and impaired clustering of pairing centers causes similar defects [24,25,26,27,28,29]. Homologous chromosome pairing is essential for formation of chiasmata, which physically link homologous chromosomes and enable their segregation at meiosis I (reductional segregation). Bouquet-defective organisms exhibit impaired chromosome segregation [10, 14, 30]

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