Direct Visualization Reveals Kinetics of Meiotic Chromosome Synapsis.

Ofer Rog,Abby F Dernburg

doi:10.1016/j.celrep.2015.02.032

Abstract

The synaptonemal complex (SC) is a conserved protein complex that stabilizes interactions along homologous chromosomes (homologs) during meiosis. The SC regulates genetic exchanges between homologs, thereby enabling reductional division and the production of haploid gametes. Here, we directly observe SC assembly (synapsis) by optimizing methods for long-term fluorescence recording in C.elegans. We report that synapsis initiates independently on each chromosome pair at or near pairing centers-specialized regions required for homolog associations. Once initiated, the SC extends rapidly and mostly irreversibly to chromosome ends. Quantitation of SC initiation frequencies and extension rates reveals that initiation is a rate-limiting step in homolog interactions. Eliminating the dynein-driven chromosome movements that accompany synapsis severely retards SC extension, revealing a new role for these conserved motions. This work provides the first opportunity to directly observe and quantify key aspects of meiotic chromosome interactions andwill enable future invivo analysis of germline processes.

Highlights

Meiosis is the specialized cell division program that produces haploid gametes from diploid precursors and is essential for sexual reproduction
Special sites on each chromosome establish connections through the nuclear envelope to the microtubule cytoskeleton and initiate movements along the nuclear periphery through the action of dynein and/or other motors (Hiraoka and Dernburg, 2009; Rog and Dernburg, 2013). This is a meiotic function of telomeres, but in C. elegans, this role has been acquired by a region near one end of each chromosome known as a pairing center (PC) (MacQueen et al, 2005; Sato et al, 2009)
A major challenge in understanding the mechanisms that contribute to homolog interactions is that pairing and synapsis occur over many hours or days, commonly within internal reproductive organs

Summary

Graphical Abstract

Each chromosome must fully align with its homologous partner. By refining methods for long-term imaging of living nematodes, Rog and Dernburg have visualized assembly of the synaptonemal complex (SC), which stabilizes homolog pairing. They determine the rates of SC initiation and elongation, illuminating the dynamics of this process. Highlights d Addition of serotonin enables long-term live imaging of meiosis in C. elegans d Each pair of chromosomes initiates synapsis stochastically at a special site d Initiation of synapsis is a rate-limiting step in homolog alignment d Dynein-driven chromosome motion promotes SC extension.

SUMMARY

INTRODUCTION

RESULTS AND DISCUSSION

EXPERIMENTAL PROCEDURES