Diffusion within the synaptonemal complex can account for signal transduction along meiotic chromosomes

Abstract

Meiotic chromosomes efficiently transduce information along their length to regulate the distribution of genetic exchanges (crossovers). However, the mode of signal transduction remains unknown. A conserved protein interface called the synaptonemal complex forms between the parental chromosomes. The synaptonemal complex exhibits liquid-like behaviors, suggesting that the diffusion of signaling molecules along its length could coordinate crossover formation. Here, we directly test the feasibility of such a mechanism by tracking a component of the synaptonemal complex (SYP-3) and a conserved regulator of exchanges (ZHP-3) in live Caenorhabditis elegans gonads. While we find that both proteins diffuse within the synaptonemal complex, ZHP-3 diffuses 4- and 9-fold faster than SYP-3 before and after crossover designation, respectively. We use these measurements to parameterize a physical model for signal transduction. We find that ZHP-3, but not SYP-3, can explore the lengths of chromosomes on the time scale of crossover designation, consistent with a role in the spatial regulation of exchanges. Given the conservation of ZHP-3 paralogues across eukaryotes, we propose that diffusion along the synaptonemal complex may be a conserved mechanism of meiotic regulation. More broadly, our work explores how diffusion compartmentalized by condensates could regulate crucial chromosomal functions.