Genetic identification of HIGH CROSSOVER RATE 3 co-chaperone network controlling meiotic crossover interference

Abstract

Meiosis is a specialized process in eukaryotic cells that generates genetic diversities for sexual reproduction. During meiosis, homologous chromosomes pair up and undergo reciprocal exchanges known as crossovers, which reshuffle genetic variation. The occurrence of meiotic crossovers is tightly regulated, ensuring that at least one crossover forms per chromosome pair, while closely spaced crossovers are restricted by a phenomenon called interference. In Arabidopsis, the positions of crossovers are proposed to follow a diffusion-mediated coarsening model, where large and evenly spaced foci of the pro-crossover enzyme HEI10 grow at the expense of smaller, closely spaced clusters. However, the precise mechanisms governing HEI10 dynamics during meiosis have remained unclear. In this study, a forward genetic screen in Arabidopsis led to the identification of a mutant called high crossover rate3 (hcr3). hcr3 acts dominantly to reduce crossover interference and increase genome-wide crossovers. The gene responsible for hcr3, known as J3, encodes a co-chaperone that belongs to HSP40 protein family. HSP40s, also refers to J proteins monitors protein molecular status, provides substrate specificity, and promotes HSP70 ATPase activity. They also target protein aggregates and biomolecular condensates to the disassembly chaperone HSP70, thus, promoting their proteasomal degradation. The study demonstrates that a network involving HCR3 and HSP70 chaperones facilitates the proteolysis of HEI10, thereby regulating interference and the distribution of crossovers across chromosomes. These findings unveil a novel role for the HSP40/J3-HSP70 chaperones in governing the chromosome-wide dynamics of recombination by controlling HEI10 proteolysis.