Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure.
Meiotic crossover (CO) recombination facilitates evolution and accurate chromosome segregation. CO distribution is tightly regulated: homolog pairs receive at least one CO, CO spacing is nonrandom, and COs occur preferentially in short genomic intervals called hotspots. We show that CO number and distribution are controlled on a chromosome-wide basis at the level of DNA double-strand break (DSB) formation by a condensin complex composed of subunits from two known condensins: the C. elegans dosage compensation complex and mitotic condensin II. Disruption of any subunit of the CO-controlling condensin dominantly changes DSB distribution, and thereby COs, and extends meiotic chromosome axes. These phenotypes are cosuppressed by disruption of a chromosome axis element. Our data implicate higher-order chromosome structure in the regulation of CO recombination, provide a model for the rapid evolution of CO hotspots, and show that reshuffling of interchangeable molecular parts can create independent machines with similar architectures but distinct biological functions.
Mets
David G
DG
Howard Hughes Medical Institute, University of California-Berkeley, Berkeley, CA 94720-3204, USA.
Meyer
Barbara J
BJ
D000251:Adenosine Triphosphatases / Q000235:genetics / Q000378:metabolism*; D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D002868:Chromosomal Proteins, Non-Histone; D003434:Crossing Over, Genetic; D053903:DNA Breaks, Double-Stranded; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D006801:Humans; D008540:Meiosis; D046912:Multiprotein Complexes / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D051135:Rad51 Recombinase / Q000378:metabolism
D029742:Caenorhabditis elegans Proteins; D002868:Chromosomal Proteins, Non-Histone; D004268:DNA-Binding Proteins; C544458:Dpy-28 protein, C elegans; C121599:HIM-3 protein, C elegans; D046912:Multiprotein Complexes; C108312:condensin complexes; D051135:Rad51 Recombinase; C495148:rad-51 protein, C elegans; D000251:Adenosine Triphosphatases