{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T19:36:02Z","timestamp":1787168162232,"version":"build-2736575974"},"reference-count":40,"publisher":"Oxford University Press (OUP)","issue":"18","license":[{"start":{"date-parts":[[2023,8,7]],"date-time":"2023-08-07T00:00:00Z","timestamp":1691366400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/M010279\/1"],"award-info":[{"award-number":["BB\/M010279\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004412","name":"Human Frontier Science Program","doi-asserted-by":"publisher","award":["CDA00060\/2010"],"award-info":[{"award-number":["CDA00060\/2010"]}],"id":[{"id":"10.13039\/100004412","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010663","name":"H2020 European Research Council","doi-asserted-by":"publisher","award":["311336"],"award-info":[{"award-number":["311336"]}],"id":[{"id":"10.13039\/100010663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000837","name":"University of Nottingham","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000837","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007723","name":"Oxford University Press","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100007723","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,10,13]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>DNA double-strand break (DSB) repair by homologous recombination (HR) uses a DNA template with similar sequence to restore genetic identity. Allelic DNA repair templates can be found on the sister chromatid or homologous chromosome. During meiotic recombination, DSBs preferentially repair from the homologous chromosome, with a proportion of HR events generating crossovers. Nevertheless, regions of similar DNA sequence exist throughout the genome, providing potential DNA repair templates. When DSB repair occurs at these non-allelic loci (termed ectopic recombination), chromosomal duplications, deletions and rearrangements can arise. Here, we characterize in detail ectopic recombination arising between a dispersed pair of inverted repeats in wild-type Saccharomyces cerevisiae at both a local and a chromosomal scale\u2014the latter identified via gross chromosomal acentric and dicentric chromosome rearrangements. Mutation of the DNA damage checkpoint clamp loader Rad24 and the RecQ helicase Sgs1 causes an increase in ectopic recombination. Unexpectedly, additional mutation of the RecA orthologues Rad51 and Dmc1 alters\u2014but does not abolish\u2014the type of ectopic recombinants generated, revealing a novel class of inverted chromosomal rearrangement driven by the single-strand annealing pathway. These data provide important insights into the role of key DNA repair proteins in regulating DNA repair pathway and template choice during meiosis.<\/jats:p>","DOI":"10.1093\/nar\/gkad650","type":"journal-article","created":{"date-parts":[[2023,7,25]],"date-time":"2023-07-25T08:15:58Z","timestamp":1690272958000},"page":"9703-9715","source":"Crossref","is-referenced-by-count":3,"title":["Recombinase-independent chromosomal rearrangements between dispersed inverted repeats in\n                    <i>Saccharomyces cerevisiae<\/i>\n                    meiosis"],"prefix":"10.1093","volume":"51","author":[{"given":"Rachal M","family":"Allison","sequence":"first","affiliation":[{"name":"Genome Damage and Stability Centre, University of Sussex , Falmer\u00a0 BN1 9RQ , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominic J","family":"Johnson","sequence":"additional","affiliation":[{"name":"Genome Damage and Stability Centre, University of Sussex , Falmer\u00a0 BN1 9RQ , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew J","family":"Neale","sequence":"additional","affiliation":[{"name":"Genome Damage and Stability Centre, University of Sussex , Falmer\u00a0 BN1 9RQ , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1483-560X","authenticated-orcid":false,"given":"Stephen","family":"Gray","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Queen\u2019s Medical Centre, University of Nottingham , Nottingham\u00a0 NG7 2UH , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,8,7]]},"reference":[{"key":"2023101301481918000_B1","doi-asserted-by":"crossref","first-page":"a012740","DOI":"10.1101\/cshperspect.a012740","article-title":"Repair of strand breaks by homologous recombination","volume":"5","author":"Jasin","year":"2013","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"2023101301481918000_B2","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.dnarep.2018.08.020","article-title":"The pendulum of the Ku-Ku clock","volume":"71","author":"Shibata","year":"2018","journal-title":"DNA Repair (Amst.)"},{"key":"2023101301481918000_B3","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/S0092-8674(00)81876-0","article-title":"Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family","volume":"88","author":"Keeney","year":"1997","journal-title":"Cell"},{"key":"2023101301481918000_B4","doi-asserted-by":"crossref","first-page":"e1002305","DOI":"10.1371\/journal.pgen.1002305","article-title":"Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways","volume":"7","author":"Martini","year":"2011","journal-title":"PLoS Genet."},{"key":"2023101301481918000_B5","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1016\/j.cell.2011.02.009","article-title":"A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation","volume":"144","author":"Pan","year":"2011","journal-title":"Cell"},{"key":"2023101301481918000_B6","doi-asserted-by":"crossref","first-page":"e324","DOI":"10.1371\/journal.pbio.0050324","article-title":"Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae","volume":"5","author":"Buhler","year":"2007","journal-title":"PLoS Biol."},{"key":"2023101301481918000_B7","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1038\/nature07135","article-title":"High-resolution mapping of meiotic crossovers and non-crossovers in yeast","volume":"454","author":"Mancera","year":"2008","journal-title":"Nature"},{"key":"2023101301481918000_B8","article-title":"Separable roles of the DNA damage response kinase Mec1ATR and its activator Rad24RAD17 within the regulation of meiotic recombination","author":"Crawford","year":"2018"},{"key":"2023101301481918000_B9","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1038\/nature03872","article-title":"Endonucleolytic processing of covalent protein-linked DNA double-strand breaks","volume":"436","author":"Neale","year":"2005","journal-title":"Nature"},{"key":"2023101301481918000_B10","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1038\/nature10515","article-title":"Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1","volume":"479","author":"Garcia","year":"2011","journal-title":"Nature"},{"key":"2023101301481918000_B11","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/j.molcel.2010.11.032","article-title":"Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions","volume":"40","author":"Zakharyevich","year":"2010","journal-title":"Mol. 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Cell Res."},{"key":"2023101301481918000_B14","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1038\/nature13993","article-title":"Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation","volume":"520","author":"Garcia","year":"2015","journal-title":"Nature"},{"key":"2023101301481918000_B15","doi-asserted-by":"crossref","first-page":"130019","DOI":"10.1098\/rsob.130019","article-title":"Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR)","volume":"3","author":"Gray","year":"2013","journal-title":"Open Biol."},{"key":"2023101301481918000_B16","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1101\/gr.213587.116","article-title":"Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1","volume":"27","author":"Mohibullah","year":"2017","journal-title":"Genome Res."},{"key":"2023101301481918000_B17","doi-asserted-by":"crossref","first-page":"e1003545","DOI":"10.1371\/journal.pgen.1003545","article-title":"Budding yeast ATM\/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery","volume":"9","author":"Carballo","year":"2013","journal-title":"PLoS Genet."},{"key":"2023101301481918000_B18","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1016\/j.cell.2008.01.035","article-title":"Phosphorylation of the axial element protein Hop1 by Mec1\/Tel1 ensures meiotic interhomolog recombination","volume":"132","author":"Carballo","year":"2008","journal-title":"Cell"},{"key":"2023101301481918000_B19","doi-asserted-by":"crossref","first-page":"11125","DOI":"10.1074\/jbc.M117.787614","article-title":"Sequence imperfections and base triplet recognition by the Rad51\/RecA family of recombinases","volume":"292","author":"Lee","year":"2017","journal-title":"J. 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Chem."},{"key":"2023101301481918000_B20","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1016\/0092-8674(90)90072-M","article-title":"A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae","volume":"61","author":"Cao","year":"1990","journal-title":"Cell"},{"key":"2023101301481918000_B21","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1093\/genetics\/153.2.607","article-title":"Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice","volume":"153","author":"Grushcow","year":"1999","journal-title":"Genetics"},{"key":"2023101301481918000_B22","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1534\/genetics.119.302427","article-title":"Distinct functions in regulation of meiotic crossovers for DNA damage response clamp loader Rad24(Rad17) and Mec1(ATR) kinase","volume":"213","author":"Shinohara","year":"2019","journal-title":"Genetics"},{"key":"2023101301481918000_B23","doi-asserted-by":"crossref","first-page":"e63144","DOI":"10.1371\/journal.pone.0063144","article-title":"Multiple pathways suppress non-allelic homologous recombination during meiosis in Saccharomyces cerevisiae","volume":"8","author":"Shinohara","year":"2013","journal-title":"PLoS One"},{"key":"2023101301481918000_B24","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.cell.2007.05.035","article-title":"BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules","volume":"130","author":"Oh","year":"2007","journal-title":"Cell"},{"key":"2023101301481918000_B25","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1016\/j.molcel.2015.01.021","article-title":"Pervasive and essential roles of the Top3\u2013Rmi1 decatenase orchestrate recombination and facilitate chromosome segregation in meiosis","volume":"57","author":"Tang","year":"2015","journal-title":"Mol. 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Cell"},{"key":"2023101301481918000_B39","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1046\/j.1365-2443.1997.1480347.x","article-title":"Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination","volume":"2","author":"Shinohara","year":"1997","journal-title":"Genes Cells"},{"key":"2023101301481918000_B40","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/0092-8674(92)90446-J","article-title":"DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression","volume":"69","author":"Bishop","year":"1992","journal-title":"Cell"}],"container-title":["Nucleic Acids Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/nar\/article-pdf\/51\/18\/9703\/51975302\/gkad650.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/nar\/article-pdf\/51\/18\/9703\/51975302\/gkad650.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,12]],"date-time":"2023-10-12T21:49:01Z","timestamp":1697147341000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/nar\/article\/51\/18\/9703\/7238144"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,7]]},"references-count":40,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2023,8,7]]},"published-print":{"date-parts":[[2023,10,13]]}},"URL":"https:\/\/doi.org\/10.1093\/nar\/gkad650","relation":{},"ISSN":["0305-1048","1362-4962"],"issn-type":[{"value":"0305-1048","type":"print"},{"value":"1362-4962","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,10,13]]},"published":{"date-parts":[[2023,8,7]]}}}