Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans

  1. Amy J. MacQueen1,
  2. Mónica P. Colaiácovo1,
  3. Kent McDonald2, and
  4. Anne M. Villeneuve1,3
  1. 1Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California 94305-5329, USA; 2Electron Microscope Laboratory, University of California, Berkeley, Berkeley, California 94720, USA

Abstract

Analysis of Caenorhabditis elegans syp-1 mutants reveals that both synapsis-dependent and -independent mechanisms contribute to stable, productive alignment of homologous chromosomes during meiotic prophase. Early prophase nuclei undergo normal reorganization insyp-1 mutants, and chromosomes initially pair. However, the polarized nuclear organization characteristic of early prophase persists for a prolonged period, and homologs dissociate prematurely; furthermore, the synaptonemal complex (SC) is absent. The predicted structure of SYP-1, its localization at the interface between intimately paired, lengthwise-aligned pachytene homologs, and its kinetics of localization with chromosomes indicate that SYP-1 is an SC structural component. A severe reduction in crossing over together with evidence for accumulated recombination intermediates in syp-1mutants indicate that initial pairing is not sufficient for completion of exchange and implicates the SC in promoting crossover recombination. Persistence of polarized nuclear organization in syp-1 mutants suggests that SC polymerization may provide a motive force or signal that drives redispersal of chromosomes. Whereas our analysis suggests that the SC is required to stabilize pairing along the entire lengths of chromosomes, striking differences in peak pairing levels for opposite ends of chromosomes in syp-1 mutants reveal the existence of an additional mechanism that can promote local stabilization of pairing, independent of synapsis.

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Footnotes

  • 3 Corresponding author.

  • E-MAIL: villen{at}cmgm.stanford.edu, FAX: (650) 725-7739.

  • Article and publication are at http://www.genesdev.org/cgi/doi/10.1101/gad.1011602.

    • Received May 31, 2002.
    • Accepted July 29, 2002.
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