Abstract

Condensin complexes are key determinants of higher-order chromatin structure and are required for mitotic and meiotic chromosome compaction and segregation. We identified a new role for condensin in the maintenance of sister chromatid cohesion during C. elegans meiosis. Using conventional and stimulated emission depletion (STED) microscopy we show that levels of chromosomally-bound cohesin were significantly reduced in dpy-28 mutants, which lack a subunit of condensin I. SYP-1, a component of the synaptonemal complex central region, was also diminished, but no decrease in the axial element protein HTP-3 was observed. Surprisingly, the two key meiotic cohesin complexes of C. elegans were both depleted from meiotic chromosomes following the loss of condensin I, and disrupting condensin I in cohesin mutants increased the frequency of detached sister chromatids. During mitosis and meiosis in many organisms, establishment of cohesion is antagonized by cohesin removal by Wapl, and we found that condensin I binds to C. elegans WAPL-1 and counteracts WAPL-1-dependent cohesin removal. Our data suggest that condensin I opposes WAPL-1 to promote stable binding of cohesin to meiotic chromosomes, thereby ensuring linkages between sister chromatids in early meiosis.

Highlights

  • Meiosis is a specialized form of cell division in which one round of DNA replication is followed by two rounds of chromosome segregation to produce haploid gametes

  • Dosage compensation is not implemented in males, which remain viable in the absence of functional condensin IDC, allowing the study of dosage compensation-independent roles of DPY-28 and CAPG-1

  • As in coh-4 coh-3 double mutants, SYP-1 formed short, fragmented stretches on chromosomes in pachytene nuclei of capg-1(RNAi); coh-4 coh-3 animals. This phenotype was distinct from that resulting from complete failure of synaptonemal complex (SC) assembly, as occurs in htp-3 mutants in which SYP-1 is present in nuclear aggregates (S4 Fig, [55]). These results indicate that the limited quantity of REC-8 remaining on the chromosomes of capg-1(RNAi); coh-4 coh-3 animals is sufficient for SC components to associate with chromosomes, and that SYP-1 is more sensitive to reductions in REC-8 levels than is HTP-3

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Summary

Introduction

Meiosis is a specialized form of cell division in which one round of DNA replication is followed by two rounds of chromosome segregation to produce haploid gametes. Critical to this process is the timely establishment and sequential release of connections between homologous chromosomes and sister chromatids. Cohesin complexes tether sister chromatids from S-phase until the complete release of sister chromatid cohesion (SCC) at anaphase onset. Stepwise release of meiotic SCC allows separation of homologs in meiosis I and sisters in meiosis II. Meiotic cohesin is required for assembly of the synaptonemal complex (SC) between homologous chromosomes (synapsis) and for interhomolog crossover recombination. Underlying the unique functions of cohesin during gametogenesis, meiotic and mitotic cohesin complexes differ both in subunit composition and regulation

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