Reactivation of chromosome signalling induces reversal of the meiotic program

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. We show that termination of chromosome movement and DSB formation is reversible and is continuously implemented by the synaptonemal complex (SC), which silences chromosome signals that promote CHK-2 activity. Forced removal of the SC or different meiosis-specific cohesin complexes, which are individually required for SC stability, causes rapid CHK-2-dependent reinstallation of the DSB-formation and chromosome-movement machinery. This nuclear reorganization occurs without transcriptional changes, but requires signalling from HORMA protein HTP-1. Conversely, CHK-2 inactivation causes rapid disassembly of the DSB-formation and chromosome-movement machinery. Thus, nuclear organization is constantly controlled by the level of CHK-2 activity. Our results uncover an unexpected plasticity of the meiotic program and show how chromosome signalling integrates nuclear organization with meiotic progression.