Surveillance of cohesin-supported chromosome structure controls meiotic progression

Maikel Castellano-Pozo, Sarai Pacheco, Georgios Sioutas, Angel Luis Jaso-Tamame, Marian H. Dore, Mohammad M. Karimi and Enrique Martinez-Perez ()
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Maikel Castellano-Pozo: MRC London Institute of Medical Sciences
Sarai Pacheco: MRC London Institute of Medical Sciences
Georgios Sioutas: MRC London Institute of Medical Sciences
Angel Luis Jaso-Tamame: MRC London Institute of Medical Sciences
Marian H. Dore: MRC London Institute of Medical Sciences
Mohammad M. Karimi: MRC London Institute of Medical Sciences
Enrique Martinez-Perez: MRC London Institute of Medical Sciences

Nature Communications, 2020, vol. 11, issue 1, 1-16

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-18219-9

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