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PLoS Genet. 2013;9(12):e1004071. doi: 10.1371/journal.pgen.1004071. Epub 2013 Dec 26.

Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions.

Author information

1
MRC Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom.
2
Howard Hughes Medical Institute, University of California, Davis, Davis, California, United States of America ; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, California, United States of America.
3
Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, United States of America.
4
Department of Life Sciences, University of Warwick, Coventry, United Kingdom.
5
Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, United States of America ; Department of Biology, New York University, New York, New York, United States of America.
6
Howard Hughes Medical Institute, University of California, Davis, Davis, California, United States of America ; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, California, United States of America ; Department of Biology, New York University, New York, New York, United States of America ; Department of Molecular & Cellular Biology, University of California, Davis, Davis, California, United States of America ; Department of Cell Biology & Human Anatomy, University of California, Davis, Davis, California, United States of America.

Abstract

During meiosis, Structural Maintenance of Chromosome (SMC) complexes underpin two fundamental features of meiosis: homologous recombination and chromosome segregation. While meiotic functions of the cohesin and condensin complexes have been delineated, the role of the third SMC complex, Smc5/6, remains enigmatic. Here we identify specific, essential meiotic functions for the Smc5/6 complex in homologous recombination and the regulation of cohesin. We show that Smc5/6 is enriched at centromeres and cohesin-association sites where it regulates sister-chromatid cohesion and the timely removal of cohesin from chromosomal arms, respectively. Smc5/6 also localizes to recombination hotspots, where it promotes normal formation and resolution of a subset of joint-molecule intermediates. In this regard, Smc5/6 functions independently of the major crossover pathway defined by the MutLγ complex. Furthermore, we show that Smc5/6 is required for stable chromosomal localization of the XPF-family endonuclease, Mus81-Mms4(Eme1). Our data suggest that the Smc5/6 complex is required for specific recombination and chromosomal processes throughout meiosis and that in its absence, attempts at cell division with unresolved joint molecules and residual cohesin lead to severe recombination-induced meiotic catastrophe.

PMID:
24385939
PMCID:
PMC3873251
DOI:
10.1371/journal.pgen.1004071
[Indexed for MEDLINE]
Free PMC Article

Conflict of interest statement

The authors have declared that no competing interests exist.

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