Abstract

Meiosis is a specialized cell division used by diploid organisms to form haploid gametes for sexual reproduction. Central to this reductive division is repair of endogenous DNA double-strand breaks (DSBs) induced by the meiosis-specific enzyme Spo11. These DSBs are repaired in a process called homologous recombination using the sister chromatid or the homologous chromosome as a repair template, with the homolog being the preferred substrate during meiosis. Specific products of inter-homolog recombination, called crossovers, are essential for proper homolog segregation at the first meiotic nuclear division in budding yeast and mice. This study identifies an essential role for the conserved Structural Maintenance of Chromosomes (SMC) 5/6 protein complex during meiotic recombination in budding yeast. Meiosis-specific smc5/6 mutants experience a block in DNA segregation without hindering meiotic progression. Establishment and removal of meiotic sister chromatid cohesin are independent of functional Smc6 protein. smc6 mutants also have normal levels of DSB formation and repair. Eliminating DSBs rescues the segregation block in smc5/6 mutants, suggesting that the complex has a function during meiotic recombination. Accordingly, smc6 mutants accumulate high levels of recombination intermediates in the form of joint molecules. Many of these joint molecules are formed between sister chromatids, which is not normally observed in wild-type cells. The normal formation of crossovers in smc6 mutants supports the notion that mainly inter-sister joint molecule resolution is impaired. In addition, return-to-function studies indicate that the Smc5/6 complex performs its most important functions during joint molecule resolution without influencing crossover formation. These results suggest that the Smc5/6 complex aids primarily in the resolution of joint molecules formed outside of canonical inter-homolog pathways.

Highlights

  • Meiosis is the cell division by which haploid gametes are created in sexually reproducing organisms

  • CO and NCO levels remain unchanged, indicating that the majority of IH-joint molecule (JM) are processed normally, and suggesting that most of the unresolved JM intermediates are derived from inter-sister recombination events. These findings demonstrate that the Smc5/6 protein complex is directly involved in meiotic recombination and suggest that Smc6 plays a key role in resolving recombination intermediates during meiosis, especially those that form between sister chromatids

  • The mononucleate population in the smc6-9 and smc6-56 mutants resembles that observed in mitotic cells harboring the smc6-56 allele, in which approximately half of the cells arrest in G2/M after replication at non-permissive temperature [49]

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Summary

Introduction

Meiosis is the cell division by which haploid gametes are created in sexually reproducing organisms. Meiosis begins with the replication of each homologous parental chromosome (homolog) into a pair of sister chromatids. The first, MI, segregates the homologs away from each other, while the second, MII, separates the sister chromatids. This leads to the formation of four haploid cells from a single diploid parent. Prior to homolog segregation, programmed DNA double-strand breaks (DSBs) are induced that are repaired through a process called homologous recombination. Together with sister chromatid cohesion, recombination facilitates segregation by creating stable attachments between the maternal and paternal homologs, ensuring their correct organization in preparation for anaphase I [1]

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