Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis.
During meiotic prophase, a structure called the synaptonemal complex (SC) assembles at the interface between aligned pairs of homologous chromosomes, and crossover recombination events occur between their DNA molecules. Here we investigate the inter-relationships between these two hallmark features of the meiotic program in the nematode C. elegans, revealing dynamic properties of the SC that are modulated by recombination. We demonstrate that the SC incorporates new subunits and switches from a more highly dynamic/labile state to a more stable state as germ cells progress through the pachytene stage of meiotic prophase. We further show that the more dynamic state of the SC is prolonged in mutants where meiotic recombination is impaired. Moreover, in meiotic mutants where recombination intermediates are present in limiting numbers, SC central region subunits become preferentially stabilized on the subset of chromosome pairs that harbor a site where pro-crossover factors COSA-1 and MutSγ are concentrated. Polo-like kinase PLK-2 becomes preferentially localized to the SCs of chromosome pairs harboring recombination sites prior to the enrichment of SC central region proteins on such chromosomes, and PLK-2 is required for this enrichment to occur. Further, late pachytene nuclei in a plk-2 mutant exhibit the more highly dynamic SC state. Together our data demonstrate that crossover recombination events elicit chromosome-autonomous stabilizing effects on the SC and implicate PLK-2 in this process. We discuss how this recombination-triggered modulation of SC state might contribute to regulatory mechanisms that operate during meiosis to ensure the formation of crossovers while at the same time limiting their numbers.
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California, United States of America.
Divya
D
Pattabiraman
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California, United States of America.
Baptiste
http://orcid.org/0000-0003-0118-0229
B
Roelens
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California, United States of America.
Alexander
A
Woglar
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California, United States of America.
Anne M
http://orcid.org/0000-0001-5193-2076
AM
Villeneuve
D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D003434:Crossing Over, Genetic; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D036681:Fluorescence Recovery After Photobleaching; D007700:Kinetics; D008540:Meiosis / Q000235:genetics*; D049469:Meiotic Prophase I / Q000235:genetics; D018613:Microscopy, Confocal; D009154:Mutation; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D011995:Recombination, Genetic; D013573:Synaptonemal Complex / Q000235:genetics* / Q000378:metabolism; D000097868:Polo-like Kinases
D029742:Caenorhabditis elegans Proteins; D004268:DNA-Binding Proteins; D017346:Protein Serine-Threonine Kinases; C584819:COSA-1 protein, C elegans; C569597:polo-like kinase 2, C elegans; D000097868:Polo-like Kinases