ZHP-3 Acts at Crossovers to Couple Meiotic Recombination with Synaptonemal Complex Disassembly and Bivalent Formation in C. elegans

Bhalla, Needhi; Wynne, David J.; Jantsch, Verena; Dernburg, Abby F.

doi:10.1371/journal.pgen.1000235

Title: ZHP-3 Acts at Crossovers to Couple Meiotic Recombination with Synaptonemal Complex Disassembly and Bivalent Formation in C. elegans

Journal Article · Fri Oct 24 00:00:00 EDT 2008 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1000235· OSTI ID:1627272

Bhalla, Needhi ^[1]; Wynne, David J. ^[2]; Jantsch, Verena ^[3]; Dernburg, Abby F. ^[1]

Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
Univ. of Vienna (Austria). Max F. Perutz Labs. Dept. of Chromosome Biology

Crossover recombination and the formation of chiasmata normally ensure the proper segregation of homologous chromosomes during the first meiotic division. zhp-3, the Caenorhabditis elegans ortholog of the budding yeast ZIP3 gene, is required for crossover recombination. We show that ZHP-3 protein localization is highly dynamic. At a key transition point in meiotic prophase, the protein shifts from along the length of the synaptonemal complex (SC) to an asymmetric localization on the SC and eventually becomes restricted to foci that mark crossover recombination events. A zhp-3::gfp transgene partially complements a null mutation and reveals a separation of function; although the fusion protein can promote nearly wild-type levels of recombination, aneuploidy among the progeny is high, indicating defects in meiotic chromosome segregation. The structure of bivalents is perturbed in this mutant, suggesting that the chromosome segregation defect results from an inability to properly remodel chromosomes in response to crossovers. smo-1 mutants exhibit phenotypes similar to zhp-3::gfp mutants at higher temperatures, and smo-1; zhp-3::gfp double mutants exhibit more severe meiotic defects than either single mutant, consistent with a role for SUMO in the process of SC disassembly and bivalent differentiation. We propose that coordination of crossover recombination with SC disassembly and bivalent formation reflects a conserved role of Zip3/ZHP-3 in coupling recombination with SC morphogenesis.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH); Vienna Science and Technology Fund (WWTF)

Grant/Contract Number:: AC02-05CH11231; K99RR024110/R00RR024110; R01 GM065591; LS0905

OSTI ID:: 1627272

Journal Information:: PLoS Genetics, Vol. 4, Issue 10; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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