Replicative aging is associated with loss of genetic heterogeneity from extrachromosomal circular DNA in Saccharomyces cerevisiae.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
20 08 2020
Historique:
accepted: 17 06 2020
revised: 28 05 2020
received: 08 12 2019
pubmed: 2 7 2020
medline: 25 9 2020
entrez: 2 7 2020
Statut: ppublish

Résumé

Circular DNA can arise from all parts of eukaryotic chromosomes. In yeast, circular ribosomal DNA (rDNA) accumulates dramatically as cells age, however little is known about the accumulation of other chromosome-derived circles or the contribution of such circles to genetic variation in aged cells. We profiled circular DNA in Saccharomyces cerevisiae populations sampled when young and after extensive aging. Young cells possessed highly diverse circular DNA populations but 94% of the circular DNA were lost after ∼15 divisions, whereas rDNA circles underwent massive accumulation to >95% of circular DNA. Circles present in both young and old cells were characterized by replication origins including circles from unique regions of the genome and repetitive regions: rDNA and telomeric Y' regions. We further observed that circles can have flexible inheritance patterns: [HXT6/7circle] normally segregates to mother cells but in low glucose is present in up to 50% of cells, the majority of which must have inherited this circle from their mother. Interestingly, [HXT6/7circle] cells are eventually replaced by cells carrying stable chromosomal HXT6 HXT6/7 HXT7 amplifications, suggesting circular DNAs are intermediates in chromosomal amplifications. In conclusion, the heterogeneity of circular DNA offers flexibility in adaptation, but this heterogeneity is remarkably diminished with age.

Identifiants

pubmed: 32609810
pii: 5866106
doi: 10.1093/nar/gkaa545
pmc: PMC7430651
doi:

Substances chimiques

DNA, Circular 0
HXT7 protein, S cerevisiae 0
Hxt6 protein, S cerevisiae 0
Monosaccharide Transport Proteins 0
Saccharomyces cerevisiae Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7883-7898

Subventions

Organisme : Wellcome Trust
ID : 088335
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 110216
Pays : United Kingdom

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Cell. 1983 Oct;34(3):961-70
pubmed: 6354471
PLoS Genet. 2011 Mar;7(3):e1002015
pubmed: 21436897
G3 (Bethesda). 2017 Oct 5;7(10):3295-3303
pubmed: 28801508
Science. 2012 Apr 6;336(6077):82-6
pubmed: 22403181
Front Microbiol. 2018 Feb 22;9:288
pubmed: 29520259
Elife. 2014 Nov 17;3:
pubmed: 25402830
PLoS Biol. 2019 Dec 3;17(12):e3000471
pubmed: 31794573
Am J Med Genet A. 2004 Nov 1;130A(4):340-4
pubmed: 15384084
Proc Natl Acad Sci U S A. 2018 Mar 27;115(13):3332-3337
pubmed: 29531028
Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):10877-81
pubmed: 17581878
Genome Res. 2002 Jun;12(6):996-1006
pubmed: 12045153
Elife. 2015 Nov 06;4:
pubmed: 26544680
BMC Bioinformatics. 2019 Dec 12;20(1):663
pubmed: 31830908
Nat Commun. 2018 Mar 14;9(1):1069
pubmed: 29540679
G3 (Bethesda). 2015 Dec 17;6(2):453-62
pubmed: 26681518
Genome Biol. 2014;15(12):550
pubmed: 25516281
Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18551-6
pubmed: 20937885
Cell Rep. 2019 Jul 9;28(2):408-422.e4
pubmed: 31291577
Nucleic Acids Res. 2012 Jan;40(Database issue):D682-6
pubmed: 22121216
Mol Cell Biol. 1997 Dec;17(12):7061-8
pubmed: 9372937
Mol Cell Biol. 1985 Sep;5(9):2369-80
pubmed: 3915542
Plasmid. 1979 Oct;2(4):536-54
pubmed: 394173
Mol Cell. 2018 Nov 1;72(3):583-593.e4
pubmed: 30293780
Cell. 1997 Dec 26;91(7):1033-42
pubmed: 9428525
Curr Biol. 2011 Jan 11;21(1):25-33
pubmed: 21194950
Science. 2014 Jan 3;343(6166):72-6
pubmed: 24310612
Proc Natl Acad Sci U S A. 2015 Jun 16;112(24):E3114-22
pubmed: 26038577
PLoS Genet. 2008 Dec;4(12):e1000303
pubmed: 19079573
PLoS Biol. 2004 Dec;2(12):e398
pubmed: 15534694
Nat Genet. 2008 Jan;40(1):90-5
pubmed: 18059269
Nature. 2017 Mar 2;543(7643):122-125
pubmed: 28178237
Proc Natl Acad Sci U S A. 1990 Apr;87(8):2955-9
pubmed: 2326258
Nat Genet. 2008 Dec;40(12):1499-504
pubmed: 19029899
Mol Biol Evol. 1998 Aug;15(8):931-42
pubmed: 9718721
Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):7921-6
pubmed: 10859355
J Vis Exp. 2016 Apr 04;(110):e54239 |
pubmed: 27077531
J Theor Biol. 2004 Jul 21;229(2):189-96
pubmed: 15207474
Genome Biol Evol. 2020 Jan 1;12(1):3762-3777
pubmed: 31882998
Anticancer Drugs. 1991 Feb;2(1):11-25
pubmed: 1720337
Mech Ageing Dev. 1980 Jan;12(1):47-52
pubmed: 6986516
Genetics. 2009 Oct;183(2):413-22, 1SI-13SI
pubmed: 19652178
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Elife. 2018 Oct 02;7:
pubmed: 30274593
Methods Mol Biol. 2016;1418:335-51
pubmed: 27008022
Nature. 2008 Aug 7;454(7205):728-34
pubmed: 18660802

Auteurs

Iñigo Prada-Luengo (I)

Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.

Henrik D Møller (HD)

Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.
Department of Biology, Institute of Biochemistry, ETH Zürich, Zurich CH-8093, Switzerland.

Rasmus A Henriksen (RA)

Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.

Qian Gao (Q)

Epigenetics Programme, The Babraham Institute, Babraham, Cambridge CB22 3-AT, UK.
Adaptimmune Ltd, Oxfordshire OX14 4RX, UK.

Camilla Eggert Larsen (CE)

Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.

Sefa Alizadeh (S)

Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.

Lasse Maretty (L)

Department of Molecular Medicine, Aarhus University Hospital, Aarhus DK-8200, Denmark.

Jonathan Houseley (J)

Epigenetics Programme, The Babraham Institute, Babraham, Cambridge CB22 3-AT, UK.

Birgitte Regenberg (B)

Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.

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Classifications MeSH