Shuffling the yeast genome using CRISPR/Cas9-generated DSBs that target the transposable Ty1 elements.
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
received:
22
07
2022
accepted:
21
12
2022
entrez:
26
1
2023
pubmed:
27
1
2023
medline:
31
1
2023
Statut:
epublish
Résumé
Although homologous recombination between transposable elements can drive genomic evolution in yeast by facilitating chromosomal rearrangements, the details of the underlying mechanisms are not fully clarified. In the genome of the yeast Saccharomyces cerevisiae, the most common class of transposon is the retrotransposon Ty1. Here, we explored how Cas9-induced double-strand breaks (DSBs) directed to Ty1 elements produce genomic alterations in this yeast species. Following Cas9 induction, we observed a significant elevation of chromosome rearrangements such as deletions, duplications and translocations. In addition, we found elevated rates of mitotic recombination, resulting in loss of heterozygosity. Using Southern analysis coupled with short- and long-read DNA sequencing, we revealed important features of recombination induced in retrotransposons. Almost all of the chromosomal rearrangements reflect the repair of DSBs at Ty1 elements by non-allelic homologous recombination; clustered Ty elements were hotspots for chromosome rearrangements. In contrast, a large proportion (about three-fourths) of the allelic mitotic recombination events have breakpoints in unique sequences. Our analysis suggests that some of the latter events reflect extensive processing of the broken ends produced in the Ty element that extend into unique sequences resulting in break-induced replication. Finally, we found that haploid and diploid strain have different preferences for the pathways used to repair double-stranded DNA breaks. Our findings demonstrate the importance of DNA lesions in retrotransposons in driving genome evolution.
Identifiants
pubmed: 36701275
doi: 10.1371/journal.pgen.1010590
pii: PGENETICS-D-22-00871
pmc: PMC9879454
doi:
Substances chimiques
Retroelements
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1010590Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM118020
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM130322
Pays : United States
Informations de copyright
Copyright: © 2023 Qi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Nucleic Acids Res. 2009 Aug;37(15):5081-92
pubmed: 19553188
Genetics. 2008 Jan;178(1):67-82
pubmed: 18202359
PLoS Genet. 2011 May;7(5):e1002089
pubmed: 21637792
Fed Proc. 1982 Aug;41(10):2653-5
pubmed: 6286365
Genome Res. 2017 Dec;27(12):2072-2082
pubmed: 29113982
Cell. 1980 Aug;21(1):239-49
pubmed: 6250713
G3 (Bethesda). 2014 Sep 17;4(11):2259-69
pubmed: 25236733
Cell. 2005 Mar 11;120(5):587-98
pubmed: 15766523
DNA Repair (Amst). 2006 Sep 8;5(9-10):1010-20
pubmed: 16798113
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):9947-52
pubmed: 22665764
Proc Natl Acad Sci U S A. 2008 Aug 19;105(33):11845-50
pubmed: 18701715
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Genetics. 1992 Oct;132(2):387-402
pubmed: 1427035
Proc Natl Acad Sci U S A. 2014 May 27;111(21):E2210-8
pubmed: 24799712
Mol Cell Biol. 1997 May;17(5):2851-8
pubmed: 9111357
Microbiol Spectr. 2015 Apr 1;3(2):1-35
pubmed: 25893143
Nat Methods. 2018 Jun;15(6):461-468
pubmed: 29713083
Genetics. 2002 Jan;160(1):97-110
pubmed: 11805048
Genome Res. 1998 May;8(5):464-78
pubmed: 9582191
PLoS Genet. 2020 Feb 21;16(2):e1008632
pubmed: 32084126
Genome Res. 2015 May;25(5):762-74
pubmed: 25840857
Curr Opin Genet Dev. 2021 Dec;71:163-170
pubmed: 34481360
Mol Cell Biol. 1996 Mar;16(3):1085-93
pubmed: 8622653
Genetics. 1995 May;140(1):67-77
pubmed: 7635309
J Genet. 1949 Dec;49(3):264-85
pubmed: 24536673
PLoS Genet. 2013 Apr;9(4):e1003434
pubmed: 23593029
Cell. 2022 Aug 4;185(16):3025-3040.e6
pubmed: 35882231
Lett Appl Microbiol. 2010 Jul;51(1):114-8
pubmed: 20536704
Mol Cell Biol. 1994 Jun;14(6):3834-41
pubmed: 8196626
Genetics. 1989 Oct;123(2):261-8
pubmed: 2684745
PLoS Genet. 2008 Sep 05;4(9):e1000175
pubmed: 18773114
Proc Natl Acad Sci U S A. 2016 Dec 13;113(50):E8114-E8121
pubmed: 27911848
Genetics. 2014 Nov;198(3):795-835
pubmed: 25381364
Nature. 2000 May 25;405(6785):451-4
pubmed: 10839539
Curr Opin Genet Dev. 2021 Dec;71:78-85
pubmed: 34311384
Genetics. 1988 Jul;119(3):549-59
pubmed: 2841187
Mol Cell Biol. 1992 Oct;12(10):4441-8
pubmed: 1328855
PLoS Genet. 2010 Dec 02;6(12):e1001228
pubmed: 21151956
PLoS Genet. 2019 Aug 29;15(8):e1008332
pubmed: 31465441
BMC Bioinformatics. 2012 Sep 19;13:238
pubmed: 22988817
Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11465-70
pubmed: 20534547
Nat Methods. 2016 Dec;13(12):1050-1054
pubmed: 27749838
Bioinformatics. 2021 Apr 20;37(3):413-415
pubmed: 32766814
Genetics. 1984 Jun;107(2):179-97
pubmed: 6329902
Proc Natl Acad Sci U S A. 2020 Nov 10;117(45):28191-28200
pubmed: 33106417
Genome Res. 2012 Mar;22(3):568-76
pubmed: 22300766
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Nat Methods. 2013 Jun;10(6):563-9
pubmed: 23644548
Science. 2010 Jul 2;329(5987):82-5
pubmed: 20595613
Genome Res. 2018 Aug;28(8):1228-1242
pubmed: 29907612
Cell. 1980 Nov;22(2 Pt 2):427-36
pubmed: 6256080
Proc Natl Acad Sci U S A. 2018 Jul 24;115(30):E7109-E7118
pubmed: 29987035
Genetics. 2012 Apr;190(4):1267-84
pubmed: 22267500