Abstract

The formation of healthy gametes requires pairing of homologous chromosomes (homologs) as a prerequisite for their correct segregation during meiosis. Initially, homolog alignment is promoted by meiotic chromosome movements feeding into intimate homolog pairing by homologous recombination and/or synaptonemal complex formation. Meiotic chromosome movements in the fission yeast, Schizosaccharomyces pombe, depend on astral microtubule dynamics that drag the nucleus through the zygote; known as horsetail movement. The response of microtubule-led meiotic chromosome movements to environmental stresses such as ionizing irradiation (IR) and associated reactive oxygen species (ROS) is not known. Here, we show that, in contrast to budding yeast, the horsetail movement is largely radiation-resistant, which is likely mediated by a potent antioxidant defense. IR exposure of sporulating S. pombe cells induced misrepair and irreparable DNA double strand breaks causing chromosome fragmentation, missegregation and gamete death. Comparing radiation outcome in fission and budding yeast, and studying meiosis with poisoned microtubules indicates that the increased gamete death after IR is innate to fission yeast. Inhibition of meiotic chromosome mobility in the face of IR failed to influence the course of DSB repair, indicating that paralysis of meiotic chromosome mobility in a genotoxic environment is not a universal response among species.

Highlights

  • The formation of healthy gametes requires pairing of homologous chromosomes as a prerequisite for their correct segregation during meiosis

  • Since quality control of meiosis is linked to generation of viable progeny[30] we determined spore viability after irradiation in 6 technical replicates

  • Irradiation of diploid prophase I cells in the horsetail stage with 300 Gy 240 kV X rays still allowed for 68% sporulation, indicating that sporulating diploid fission yeast cells are quite radioresistant

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Summary

Introduction

The formation of healthy gametes requires pairing of homologous chromosomes (homologs) as a prerequisite for their correct segregation during meiosis. IR exposure of sporulating S. pombe cells induced misrepair and irreparable DNA double strand breaks causing chromosome fragmentation, missegregation and gamete death. Meiosis halves the genome to compensate its doubling at fertilization To this end, two successive rounds of chromosome segregation follow a single phase of DNA replication leading to the formation of haploid gametes or spores. In most organisms homolog pairing relies on the formation of physiological DNA double strand breaks (DSBs) that are formed by the transesterase Spo[11] during the leptonema substage of prophase I6. In the asynaptic meiosis of the fission yeast Schizosaccharomyces pombe a synaptonemal complex is absent but chromosomes are aligned by oscillating nuclear mobility driven by the astral microtubule-bound spindle pole body (SPB) to which telomeres are attached, giving rise to the so-called horsetail nucleus throughout much of prophase I7,16. Meiotic chromosome mobility is thought to support the chromosome pairing process in meiotic prophase and is generally driven by cytoskeletal forces, either by microtubules (mammals, worms and fission yeast)[15,17,18,19,20] or www.nature.com/scientificreports/

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