Manipulation of Karyotype in Caenorhabditis elegans Reveals Multiple Inputs Driving Pairwise Chromosome Synapsis During Meiosis.
Meiotic chromosome segregation requires pairwise association between homologs, stabilized by the synaptonemal complex (SC). Here, we investigate factors contributing to pairwise synapsis by investigating meiosis in polyploid worms. We devised a strategy, based on transient inhibition of cohesin function, to generate polyploid derivatives of virtually any Caenorhabditis elegans strain. We exploited this strategy to investigate the contribution of recombination to pairwise synapsis in tetraploid and triploid worms. In otherwise wild-type polyploids, chromosomes first sort into homolog groups, then multipartner interactions mature into exclusive pairwise associations. Pairwise synapsis associations still form in recombination-deficient tetraploids, confirming a propensity for synapsis to occur in a strictly pairwise manner. However, the transition from multipartner to pairwise association was perturbed in recombination-deficient triploids, implying a role for recombination in promoting this transition when three partners compete for synapsis. To evaluate the basis of synapsis partner preference, we generated polyploid worms heterozygous for normal sequence and rearranged chromosomes sharing the same pairing center (PC). Tetraploid worms had no detectable preference for identical partners, indicating that PC-adjacent homology drives partner choice in this context. In contrast, triploid worms exhibited a clear preference for identical partners, indicating that homology outside the PC region can influence partner choice. Together, our findings, suggest a two-phase model for C. elegans synapsis: an early phase, in which initial synapsis interactions are driven primarily by recombination-independent assessment of homology near PCs and by a propensity for pairwise SC assembly, and a later phase in which mature synaptic interactions are promoted by recombination.
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California 94305.
Baptiste
B
Roelens
Department of Biology, Brooklyn College, City University of New York (CUNY), Brooklyn, New York 11210 Molecular, Cellular, and Developmental Biology Program, The Graduate Center, CUNY, New York, New York 10016 annev@stanford.edu mschvarzstein@brooklyn.cuny.edu.
Mara
M
Schvarzstein
Departments of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, California 94305 annev@stanford.edu mschvarzstein@brooklyn.cuny.edu.
Anne M
AM
Villeneuve
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics*; D029742:Caenorhabditis elegans Proteins / Q000037:antagonists & inhibitors / Q000502:physiology; D018797:Cell Cycle Proteins / Q000037:antagonists & inhibitors / Q000502:physiology; D002868:Chromosomal Proteins, Non-Histone / Q000037:antagonists & inhibitors / Q000502:physiology; D023902:Chromosome Pairing; D020090:Chromosome Segregation; D005260:Female; D059785:Karyotype; D008297:Male; D008540:Meiosis; D008957:Models, Genetic; D057891:Tetraploidy; D000097722:Cohesins
D029742:Caenorhabditis elegans Proteins; D018797:Cell Cycle Proteins; D002868:Chromosomal Proteins, Non-Histone; D000097722:Cohesins
C. elegans; meiosis; polyploidy; recombination; synaptonemal complex