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Title: Direct visualization reveals kinetics of meiotic chromosome synapsis

Journal Article · · Cell Reports
 [1];  [2]
  1. Univ. of California, Berkeley, Berkeley, CA (United States); Howard Hughes Medical Institute, Chevy Chase, MD (United States)
  2. Univ. of California, Berkeley, Berkeley, CA (United States); Howard Hughes Medical Institute, Chevy Chase, MD (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); California Institute for Quantitative Biosciences, Berkeley, CA (United States)
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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 and will enable future in vivo analysis of germline processes.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
National Inst. of Health (NIH), Bethesda, MD (United States). NIH National Center for Research Resources (NCRR); Howard Hughes Medical Inst., Chevy Chase, MD (United States)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1215415
Journal Information:
Cell Reports, Vol. 10, Issue 10; Related Information: Supplemental Information includes Supplemental Experimental Procedures, four figures, and ten movies and can be found with this open access article online at http://dx.doi.org/10.1016/j.celrep.2015.02.032.; ISSN 2211-1247
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 46 works
Citation information provided by
Web of Science

References (28)

Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans journal December 2005
SYP-3 Restricts Synaptonemal Complex Assembly to Bridge Paired Chromosome Axes During Meiosis in Caenorhabditis elegans journal June 2007
Biogenic amine neurotransmitters in C. elegans journal January 2007
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Serotonin and the Neuropeptide PDF Initiate and Extend Opposing Behavioral States in C. elegans journal August 2013
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Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of X Chromosome Territories during Caenorhabditis elegans Meiosis journal August 2011
HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans journal November 2005
Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis journal November 2009
ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis journal February 1993
Cellular Analyses of the Mitotic Region in the Caenorhabditis elegans Adult Germ Line journal July 2006
The SUN Rises on Meiotic Chromosome Dynamics journal November 2009
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The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis journal June 2010
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Synaptonemal Complex Assembly in C. elegans Is Dispensable for Loading Strand-Exchange Proteins but Critical for Proper Completion of Recombination journal September 2003
Single-copy insertion of transgenes in Caenorhabditis elegans journal October 2008
Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans journal September 2002
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HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis journal November 2005
Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis journal January 2012
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The Nuclear Envelope Protein Matefin/SUN-1 Is Required for Homologous Pairing in C. elegans Meiosis journal June 2007
Long-Term Imaging of Caenorhabditis elegans Using Nanoparticle-Mediated Immobilization journal January 2013
THE GENETICS OF CAENORHABDITIS ELEGANS journal May 1974

Cited By (15)

Regulating chromosomal movement by the cochaperone FKB-6 ensures timely pairing and synapsis journal January 2017
Time-Course Analysis of Early Meiotic Prophase Events Informs Mechanisms of Homolog Pairing and Synapsis in Caenorhabditis elegans journal July 2017
N-terminal acetylation promotes synaptonemal complex assembly in C. elegans journal November 2016
Time-course analysis of early meiotic prophase events informs mechanisms of homolog pairing and synapsis in Caenorhabditis elegans journal May 2017
LINC complexes promote homologous recombination in part through inhibition of nonhomologous end joining journal December 2016
Live cell analyses of synaptonemal complex dynamics and chromosome movements in cultured mouse testis tubules and embryonic ovaries journal March 2018
Meiotic chromosome movement: what’s lamin got to do with it? journal January 2019
Nuclear Envelope-Associated Chromosome Dynamics during Meiotic Prophase I journal January 2018
The BRCA1-BARD1 complex associates with the synaptonemal complex and pro-crossover factors and influences RAD-51 dynamics during Caenorhabditis elegans meiosis journal March 2018
Spindle assembly checkpoint proteins regulate and monitor meiotic synapsis in C. elegans journal October 2015
A network of nuclear envelope proteins and cytoskeletal force generators mediates movements of and within nuclei throughout Caenorhabditis elegans development journal September 2019
Meiotic chromosomes in motion: a perspective from Mus musculus and Caenorhabditis elegans journal March 2019
A first genetic portrait of synaptonemal complex variation journal August 2019
Meiotic budding yeast assemble bundled triple helices but not ladders posted_content May 2021
The auxin-inducible degradation (AID) system enables versatile conditional protein depletion in C. elegans journal November 2015

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