The Smc5–Smc6 Complex Is Required to Remove Chromosome Junctions in Meiosis

Sarah Farmer,Pedro A San-Segundo,Luís Aragón

doi:10.1371/journal.pone.0020948

Abstract

Meiosis, a specialized cell division with a single cycle of DNA replication round and two consecutive rounds of nuclear segregation, allows for the exchange of genetic material between parental chromosomes and the formation of haploid gametes. The structural maintenance of chromosome (SMC) proteins aid manipulation of chromosome structures inside cells. Eukaryotic SMC complexes include cohesin, condensin and the Smc5–Smc6 complex. Meiotic roles have been discovered for cohesin and condensin. However, although Smc5–Smc6 is known to be required for successful meiotic divisions, the meiotic functions of the complex are not well understood. Here we show that the Smc5–Smc6 complex localizes to specific chromosome regions during meiotic prophase I. We report that meiotic cells lacking Smc5–Smc6 undergo catastrophic meiotic divisions as a consequence of unresolved linkages between chromosomes. Surprisingly, meiotic segregation defects are not rescued by abrogation of Spo11-induced meiotic recombination, indicating that at least some chromosome linkages in smc5–smc6 mutants originate from other cellular processes. These results demonstrate that, as in mitosis, Smc5-Smc6 is required to ensure proper chromosome segregation during meiosis by preventing aberrant recombination intermediates between homologous chromosomes.

Highlights

Sexual organisms require a specialized cellular division, known as meiosis, to reduce their chromosome number by half to produce gametes [reviewed in [1,2]
As cells progress into meiosis, Smc6p-9myc redistributes into distinct foci throughout the rest of the nucleus (Figure 1A)
Smc5p-9myc exhibits a similar pattern (Figure 1C). This pattern of localization is similar to various markers of meiotic recombination [31,32] which, added to the fact that the Smc5–Smc6 complex is recruited to mitotic double-strand breaks (DSBs) [33,34,35], prompted us to test whether the punctuate nuclear distribution of Smc5–Smc6 is dependent on meiotic DSBs

Summary

Introduction

Sexual organisms require a specialized cellular division, known as meiosis, to reduce their chromosome number by half to produce gametes [reviewed in [1,2]. This process entails a division with two rounds of chromosome segregation and only one of DNA replication. The chromosome-halving event occurs in the first division, during which homologous chromosomes pair up and undergo recombination, generating crossovers (CO) between them. The number of COs and their position is an important issue; if a chromosome pair fails to establish COs, the homologues may not segregate to opposite poles and, if too many COs are established between homologues, timely separation may not take place [3]. The number of DNA double-strand breaks (DSBs) initiating recombination far exceeds the number of COs [8]

Methods

Results

Conclusion