Quantitative Cytogenetics Reveals the Longitudinal Architecture of Meiotic Chromosome Axes

Here, we use quantitative cytogenetics in C. elegans to elucidate the molecular stoichiometry and longitudinal architecture of the cohesin-based meiotic chromosome axis, a structure required for most meiotic prophase-specific biology. We reveal a modular organization of the axis wherein different meiotic HORMAD proteins assemble into cohorts in defined numbers and co-organize the axis together with two functionally-distinct cohesin complexes in defined stoichiometry. Half of the REC-8-containing cohesin complexes loaded during S phase are lost concurrently with axis assembly, and the resulting axis contains single cohesion-mediating REC-8 complexes occurring with an average spacing of 1/130-200 kb, alternating with cohorts of axis-organizing COH-3/4 cohesin complexes (averaging 3 per module) that can associate with individual chromatids. The resulting axis/loop architecture yields an inherent asymmetry in genomic content between the loops formed on sister chromatids, potentially explaining essential but enigmatic aspects of meiotic recombination, such as the inter-homolog bias of DNA repair.