Abstract

The synaptonemal complex (SC) links two meiotic prophase chromosomal events: homolog pairing and crossover recombination. SC formation involves the multimeric assembly of coiled-coil proteins (Zip1 in budding yeast) at the interface of aligned homologous chromosomes. However, SC assembly is indifferent to homology and thus is normally regulated such that it occurs only subsequent to homology recognition. Assembled SC structurally interfaces with and influences the level and distribution of interhomolog crossover recombination events. Despite its involvement in dynamic chromosome behaviors such as homolog pairing and recombination, the extent to which SC, once installed, acts as an irreversible tether or maintains the capacity to remodel is not clear. Experiments presented here reveal insight into the dynamics of the full-length SC in budding yeast meiotic cells. We demonstrate that Zip1 continually incorporates into previously assembled synaptonemal complex during meiotic prophase. Moreover, post-synapsis Zip1 incorporation is sufficient to rescue the sporulation defect triggered by SCs built with a mutant version of Zip1, Zip1-4LA. Post-synapsis Zip1 incorporation occurs initially with a non-uniform spatial distribution, predominantly associated with Zip3, a component of the synapsis initiation complex that is presumed to mark a subset of crossover sites. A non-uniform dynamic architecture of the SC is observed independently of (i) synapsis initiation components, (ii) the Pch2 and Pph3 proteins that have been linked to Zip1 regulation, and (iii) the presence of a homolog. Finally, the rate of SC assembly and SC central region size increase in proportion to Zip1 copy number; this and other observations suggest that Zip1 does not exit the SC structure to the same extent that it enters. Our observations suggest that, after full-length assembly, SC central region exhibits little global turnover but maintains differential assembly dynamics at sites whose distribution is patterned by a recombination landscape.

Highlights

  • The critical events that ensure a precise reduction in chromosome ploidy at the first meiotic division occur during meiotic prophase [1,2]

  • Accurate chromosome reduction relies on the prior establishment of pair-wise associations between homologous chromosomes; maintenance of paired associations typically occurs via interhomolog crossover recombination events

  • We explore the dynamics of budding yeast synaptonemal complex (SC) and find that full-length SCs exhibit ongoing subunit incorporation but little subunit turnover during a meiotic cell cycle arrest, SC grows over time

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Summary

Introduction

The critical events that ensure a precise reduction in chromosome ploidy at the first meiotic division occur during meiotic prophase [1,2]. A key accomplishment of meiotic prophase is the formation of stable partnerships between homologous chromosomes. The molecular mechanism that mediates initial pairing between partner chromosomes is still unclear, but must involve the capacity to recognize homology and productively link this recognition to reinforcement of a paired association between two chromosomes. For meiotic nuclei in most organisms, homolog associations are stabilized for the long term via a crossover recombination event. DNA double-strand breaks (DSBs) are deliberately induced and undergo regulated repair during meiotic prophase; the fraction of double-strand breaks that are repaired to a crossover outcome involving the homolog’s (nonsister) chromatid ensure that homologous partner chromosomes are linked, so long as sister cohesion remains intact

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