The SMC-5/6 complex and the HIM-6 (BLM) helicase synergistically promote meiotic recombination intermediate processing and chromosome maturation during Caenorhabditis elegans meiosis

Hong, Ye, Sonneville, Remi, Agostinho, Ana, Meier, Bettina, Wang, Bin, Blow, J. Julian and Gartner, Anton (2016) The SMC-5/6 complex and the HIM-6 (BLM) helicase synergistically promote meiotic recombination intermediate processing and chromosome maturation during Caenorhabditis elegans meiosis. PLoS Genetics, 12 (3). ISSN 1553-7390

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Abstract

Meiotic recombination is essential for the repair of programmed double strand breaks (DSBs) to generate crossovers (COs) during meiosis. The efficient processing of meiotic recombination intermediates not only needs various resolvases but also requires proper meiotic chromosome structure. The Smc5/6 complex belongs to the structural maintenance of chromosome (SMC) family and is closely related to cohesin and condensin. Although the Smc5/6 complex has been implicated in the processing of recombination intermediates during meiosis, it is not known how Smc5/6 controls meiotic DSB repair. Here, using Caenorhabditis elegans we show that the SMC-5/6 complex acts synergistically with HIM-6, an ortholog of the human Bloom syndrome helicase (BLM) during meiotic recombination. The concerted action of the SMC-5/6 complex and HIM-6 is important for processing recombination intermediates, CO regulation and bivalent maturation. Careful examination of meiotic chromosomal morphology reveals an accumulation of inter-chromosomal bridges in smc-5; him-6 double mutants, leading to compromised chromosome segregation during meiotic cell divisions. Interestingly, we found that the lethality of smc-5; him-6 can be rescued by loss of the conserved BRCA1 ortholog BRC-1. Furthermore, the combined deletion of smc-5 and him-6 leads to an irregular distribution of condensin and to chromosome decondensation defects reminiscent of condensin depletion. Lethality conferred by condensin depletion can also be rescued by BRC-1 depletion. Our results suggest that SMC-5/6 and HIM-6 can synergistically regulate recombination intermediate metabolism and suppress ectopic recombination by controlling chromosome architecture during meiosis.

Item Type:	Article
Additional Information:	Data Availability: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by a Wellcome Trust Senior Research award (090944/Z/09/Z) and Biotechnology and Biological Sciences Research Council (BB/J015199/1) to AG and Cancer Research UK grants C303/A7399 and C303/A14301 to JJB (http://www.wellcome.ac.uk/funding/biomedical-science/funding-schemes/fellowships/basic-biomedical-fellowships/wtd004442.htm, http://www.bbsrc.ac.uk, http://www.cancerresearchuk.org). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Depositing User:	LivePure Connector
Date Deposited:	10 Jun 2024 10:31
Last Modified:	10 Jun 2024 10:31
URI:	https://ueaeprints.uea.ac.uk/id/eprint/95432
DOI:	10.1371/journal.pgen.1005872

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