Reconstitution of a flexible SYCP3-DNA fibre suggests a mechanism for SYCP3 coating of the meiotic chromosome axis

Abstract

The synaptonemal complex (SC) keeps homologous chromosomes in close alignment during meiotic crossover. A hallmark of SC formation is the presence of its protein component SYCP3 on the chromosome axis. As SC assembly progresses, SYCP3 is deposited on both axes of the homologue pair, forming the lateral element (LE) in the tripartite structure of the mature SC. We have used cryo-electron tomography and atomic force microscopy to study the mechanism of assembly and DNA binding of the SYCP3 fibre. We find that the three-dimensional architecture of the fibre is built on a highly irregular arrangement of SYCP3 molecules displaying very limited local geometry. Interaction between SYCP3 molecules is driven by the intrinsically disordered tails of the protein, with no contact between the helical cores, resulting in a flexible fibre assembly. We demonstrate that the SYCP3 fibre can engage in extensive interactions with DNA, indicative of an efficient mechanism for incorporation of DNA within the fibre. Taken together, our findings suggest that, upon deposition on the chromosome axis, SYCP3 spreads by polymerising into a fibre that is fastened to the chromosome surface via DNA binding. The resulting layer of SYCP3 coating the chromosome axis might provide a structural basis for LE assembly in meiotic prophase.