Recruitment of Polo-like kinase couples synapsis to meiotic progression via inactivation of CHK-2

Abstract

Meiotic chromosome segregation relies on synapsis and crossover recombination between homologous chromosomes. These processes require multiple steps that are coordinated by the meiotic cell cycle and monitored by surveillance mechanisms. In diverse species, failures in chromosome synapsis can trigger a cell cycle delay and/or lead to apoptosis. How this key step in 'homolog engagement' is sensed and transduced by meiotic cells is unknown. Here we report that in C. elegans, recruitment of the Polo-like kinase PLK-2 to the synaptonemal complex triggers phosphorylation and inactivation of CHK-2, an early meiotic kinase required for pairing, synapsis, and double-strand break induction. Inactivation of CHK-2 terminates double-strand break formation and enables crossover designation and cell cycle progression. These findings illuminate how meiotic cells ensure crossover formation and accurate chromosome segregation.

Distinct intersecting pathways link homolog pairing to initiation of meiotic chromosome synapsis

“…PLK-2 undergoes a dynamic localization in the germ line, as it concentrates into aggregates at the nuclear periphery during TZ stage, and it redistributes along the SC in pachytene in response to CO site designation and to promote timely inactivation of CHK-2 17,20,60 . Importantly, PLK-2, together with phosphorylated SUN-1, can delay exit from TZ (visible as prolonged nuclear clustering) in the presence of defects in synapsis or recombination 17,20,21,57 .…”

Length-sensitive partitioning ofCaenorhabditis elegansmeiotic chromosomes senses proximity and number of crossover sites

“…PLK-2 has also been shown to be required for the timely partitioning of ZHP-1/2 at pachytene, but not for its later partitioning at diakinesis 16 . PLK-2's influence on both phospho-SYP-1 and ZHP-1/2 may be due either to a specific interaction involved in length sensing at this stage, or alternatively due to its role in inactivating CHK-2 and promoting later steps of CO designation in a timely fashion 49 . For the former case, we hypothesize that after PLK-2 is recruited to the SC, it may phosphorylate further targets that promote partitioning by slowing down the dynamics of the SC, specifically by lowering the rate of SC dissociation from the chromosome.…”