Abstract
Chromosome movements and programmed DNA double-strand breaks (DSBs) promote homologue pairing and initiate recombination at meiosis onset. Meiotic progression involves checkpoint-controlled termination of these events when all homologue pairs achieve synapsis and form crossover precursors. Exploiting the temporo-spatial organisation of the C. elegans germline and time-resolved methods of protein removal, we show that surveillance of the synaptonemal complex (SC) controls meiotic progression. In nuclei with fully synapsed homologues and crossover precursors, removing different meiosis-specific cohesin complexes, which are individually required for SC stability, or a SC central region component causes functional redeployment of the chromosome movement and DSB machinery, triggering whole-nucleus reorganisation. This apparent reversal of the meiotic programme requires CHK-2 kinase reactivation via signalling from chromosome axes containing HORMA proteins, but occurs in the absence of transcriptional changes. Our results uncover an unexpected plasticity of the meiotic programme and show how chromosome signalling orchestrates nuclear organisation and meiotic progression.
Highlights
Chromosome movements and programmed DNA double-strand breaks (DSBs) promote homologue pairing and initiate recombination at meiosis onset
C. elegans expresses two types of meiosisspecific cohesin complexes defined by their kleisin subunit: REC84 and the highly identical (84%) and functionally redundant COH-3 and COH-43
Rec-8 and coh-3/4 mutants display severe chromosome organisation defects from the onset of meiosis, making mutant analysis impractical for clarifying the roles of REC-8 and COH-3/4 complexes during pachytene. To bypass this intrinsic limitation of kleisin mutant analysis, we created kleisin versions that can be removed from meiotic chromosomes in a temporally controlled manner by introducing three repeats of the TEV protease recognition motif in REC-8 and COH-3
Summary
Chromosome movements and programmed DNA double-strand breaks (DSBs) promote homologue pairing and initiate recombination at meiosis onset. In nuclei with fully synapsed homologues and crossover precursors, removing different meiosis-specific cohesin complexes, which are individually required for SC stability, or a SC central region component causes functional redeployment of the chromosome movement and DSB machinery, triggering whole-nucleus reorganisation. This apparent reversal of the meiotic programme requires CHK-2 kinase reactivation via signalling from chromosome axes containing HORMA proteins, but occurs in the absence of transcriptional changes. The presence (or absence) of these meiotic chromosome metabolism intermediates results in signals that feedback to regulate checkpoint kinases, which target components of the pairing, recombination, and cell cycle machineries[8] These quality control mechanisms fulfil two important roles. Nucleus-wide loss of CHK-2 activity is thought of as a unidirectional transition of the meiotic programme that leads to the completion of recombination and progression towards chromosome segregation
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
