Ribosomal DNA replication time coordinates completion of genome replication and anaphase in yeast.
CP: Molecular biology
Cdc14
Fob1
anaphase
cell cycle
copy number variation
nucleolus
origin of replication
rDNA
replication timing
ribosomal DNA
Journal
Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691
Informations de publication
Date de publication:
28 03 2023
28 03 2023
Historique:
received:
31
05
2022
revised:
19
12
2022
accepted:
09
02
2023
medline:
3
4
2023
pubmed:
27
2
2023
entrez:
26
2
2023
Statut:
ppublish
Résumé
Timely completion of genome replication is a prerequisite for mitosis, genome integrity, and cell survival. A challenge to this timely completion comes from the need to replicate the hundreds of untranscribed copies of rDNA that organisms maintain in addition to the copies required for ribosome biogenesis. Replication of these rDNA arrays is relegated to late S phase despite their large size, repetitive nature, and essentiality. Here, we show that, in Saccharomyces cerevisiae, reducing the number of rDNA repeats leads to early rDNA replication, which results in delaying replication elsewhere in the genome. Moreover, cells with early-replicating rDNA arrays and delayed genome-wide replication aberrantly release the mitotic phosphatase Cdc14 from the nucleolus and enter anaphase prematurely. We propose that rDNA copy number determines the replication time of the rDNA locus and that the release of Cdc14 upon completion of rDNA replication is a signal for cell cycle progression.
Identifiants
pubmed: 36842087
pii: S2211-1247(23)00172-9
doi: 10.1016/j.celrep.2023.112161
pmc: PMC10142053
mid: NIHMS1887269
pii:
doi:
Substances chimiques
DNA, Ribosomal
0
Saccharomyces cerevisiae Proteins
0
Cell Cycle Proteins
0
DNA-Binding Proteins
0
Protein Tyrosine Phosphatases
EC 3.1.3.48
CDC14 protein, S cerevisiae
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
112161Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM117466
Pays : United States
Organisme : NHGRI NIH HHS
ID : RM1 HG010461
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM117446
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM122497
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM139532
Pays : United States
Organisme : NHGRI NIH HHS
ID : T32 HG000035
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM122088
Pays : United States
Informations de copyright
Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests C.Q. is a Cell Reports Advisory Board member, Ecology and Evolution.
Références
Mol Cell Biol. 2007 Jan;27(2):568-78
pubmed: 17101800
Cell. 1988 Nov 18;55(4):637-43
pubmed: 3052854
J Mol Biol. 1992 Apr 5;224(3):545-58
pubmed: 1569546
Cell. 1992 Oct 16;71(2):267-76
pubmed: 1423594
Science. 1997 Aug 29;277(5330):1313-6
pubmed: 9271578
Nucleic Acids Res. 1995 May 11;23(9):1447-53
pubmed: 7784195
EMBO J. 2011 Nov 11;30(23):4805-14
pubmed: 22081107
Nat Commun. 2014 Sep 11;5:4850
pubmed: 25209200
Nature. 2003 Oct 16;425(6959):686-91
pubmed: 14562095
Genes Dev. 2002 Oct 1;16(19):2479-84
pubmed: 12368258
Annu Rev Cell Dev Biol. 2008;24:131-57
pubmed: 18616426
Mol Cell Biol. 1988 Nov;8(11):4927-35
pubmed: 3062373
Nucleic Acids Res. 1992 Apr 11;20(7):1463-9
pubmed: 1349740
Elife. 2018 Feb 13;7:
pubmed: 29436367
Curr Genet. 2019 Apr;65(2):429-434
pubmed: 30456647
G3 (Bethesda). 2020 Jan 7;10(1):417-430
pubmed: 31757929
Nature. 1999 Apr 29;398(6730):818-23
pubmed: 10235265
PLoS Genet. 2016 Nov 7;12(11):e1006414
pubmed: 27820830
Mol Cell Biol. 2001 Jan;21(1):136-47
pubmed: 11113188
Methods Mol Biol. 2013;1077:11-37
pubmed: 24014397
Nucleic Acids Res. 2007 Jan;35(Database issue):D40-6
pubmed: 17065467
EMBO J. 2017 Jan 4;36(1):79-101
pubmed: 27852625
PLoS Genet. 2011 Apr;7(4):e1001376
pubmed: 21533076
Plasmid. 1995 Nov;34(3):184-97
pubmed: 8825371
Genes Dev. 1998 Dec 15;12(24):3821-30
pubmed: 9869636
J Biol Chem. 2001 Jun 15;276(24):21924-31
pubmed: 11274204
Mol Cell Biol. 2007 Sep;27(18):6396-406
pubmed: 17636020
Trends Genet. 2022 Jun;38(6):587-597
pubmed: 35272860
Cell. 2016 Apr 21;165(3):580-92
pubmed: 27062929
Proc Natl Acad Sci U S A. 1958 Jul 15;44(7):671-82
pubmed: 16590258
PLoS Genet. 2017 Sep 7;13(9):e1006994
pubmed: 28880866
Nat Genet. 2002 Nov;32(3):438-42
pubmed: 12355067
Elife. 2019 Jan 23;8:
pubmed: 30672733
Nat Commun. 2017 Aug 30;8(1):328
pubmed: 28855503
Cell. 1987 Nov 6;51(3):463-71
pubmed: 2822257
Nat Commun. 2016 Nov 25;7:13599
pubmed: 27886181
Genes Dev. 2003 Sep 1;17(17):2162-76
pubmed: 12923057
Trends Biochem Sci. 2022 Apr;47(4):328-341
pubmed: 35063340
Science. 2001 Oct 5;294(5540):115-21
pubmed: 11588253
Mol Cell. 2002 Sep;10(3):647-57
pubmed: 12408831
Cell. 1992 Jan 24;68(2):333-9
pubmed: 1733502
Genes Dev. 2002 Oct 1;16(19):2459-64
pubmed: 12368256
Nucleic Acids Res. 1993 May 25;21(10):2331-8
pubmed: 8506130
Methods. 1999 Jul;18(3):329-34
pubmed: 10454994
Nat Cell Biol. 2006 Feb;8(2):148-55
pubmed: 16429127
J Biophys Biochem Cytol. 1959 Dec;6:457-66
pubmed: 14416993
Gene. 2008 May 15;414(1-2):32-40
pubmed: 18372119
Dev Biol. 1970 Jul;22(3):495-512
pubmed: 5463671
Mol Cell Biol. 1993 Sep;13(9):5360-9
pubmed: 8355687
J Hered. 1994 May-Jun;85(3):211-7
pubmed: 8014461
Nature. 1979 Nov 1;282(5734):39-43
pubmed: 388229
Mol Cell. 1998 Dec;2(6):709-18
pubmed: 9885559
Nat Cell Biol. 2003 Mar;5(3):249-54
pubmed: 12598903
Mol Cell. 2014 May 22;54(4):691-7
pubmed: 24856221
Nature. 1998 Oct 8;395(6702):615-8
pubmed: 9783589
G3 (Bethesda). 2013 Nov 06;3(11):1955-63
pubmed: 24022751
FEBS J. 2008 Dec;275(23):5774-84
pubmed: 19021755
J Mol Biol. 2014 Dec 12;426(24):3917-3928
pubmed: 25308339
Plant Physiol. 2018 Mar;176(3):2166-2185
pubmed: 29301956
J Struct Biol. 2019 Nov 1;208(2):152-164
pubmed: 31449968
PLoS Genet. 2017 Oct 16;13(10):e1007041
pubmed: 29036220
PLoS Genet. 2019 May 13;15(5):e1008138
pubmed: 31083663
Proc Natl Acad Sci U S A. 1966 Aug;56(2):496-9
pubmed: 5229971
Cell. 1999 Apr 16;97(2):233-44
pubmed: 10219244
Trends Genet. 2019 Oct;35(10):734-742
pubmed: 31395390
Nat Commun. 2020 May 8;11(1):2267
pubmed: 32385287
Cell. 1989 Jun 2;57(5):753-61
pubmed: 2720786
EMBO J. 1994 Feb 15;13(4):906-13
pubmed: 8112304
Sci Adv. 2018 Feb 28;4(2):eaao0665
pubmed: 29503865
Genes Cells. 1997 Nov;2(11):667-78
pubmed: 9491801
PLoS Genet. 2013;9(3):e1003329
pubmed: 23505383
Science. 2013 Aug 23;341(6148):893-6
pubmed: 23907533
Mol Cell. 2002 May;9(5):1067-78
pubmed: 12049742
Mol Cell Biol. 1993 Oct;13(10):6600-13
pubmed: 8413256
Nucleic Acids Res. 2008 Oct;36(17):5623-34
pubmed: 18765475
Cell Rep. 2014 Apr 10;7(1):53-61
pubmed: 24656819
Genome Res. 2013 Oct;23(10):1749-62
pubmed: 23800452
Mol Cell. 2015 Dec 3;60(5):797-807
pubmed: 26656162
Mol Cell. 2018 Oct 18;72(2):239-249.e5
pubmed: 30146316
Nat Commun. 2016 Aug 30;8:16083
pubmed: 28853436
Genes Dev. 1997 Jan 15;11(2):241-54
pubmed: 9009206
Cell Rep. 2014 Apr 10;7(1):62-9
pubmed: 24685139
Genetics. 2015 Apr;199(4):1077-91
pubmed: 25701287
PLoS Genet. 2017 Jun 22;13(6):e1006771
pubmed: 28640831
Genome Res. 2020 Nov;30(11):1583-1592
pubmed: 33033057
Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5256-60
pubmed: 11607297
EMBO J. 2015 Jan 2;34(1):81-96
pubmed: 25371407
PLoS Genet. 2015 Apr 17;11(4):e1005148
pubmed: 25885886
Curr Biol. 2004 Mar 23;14(6):467-80
pubmed: 15043811
PLoS One. 2015 Jun 19;10(6):e0128604
pubmed: 26090959
Nucleic Acids Res. 2006 May 31;34(10):2914-24
pubmed: 16738130
PLoS Genet. 2019 Oct 4;15(10):e1008430
pubmed: 31584938
J Mol Biol. 1998 Mar 27;277(2):249-56
pubmed: 9514756
Science. 2010 Feb 5;327(5966):693-6
pubmed: 20133573
Genes Cells. 2002 Aug;7(8):781-9
pubmed: 12167157
G3 (Bethesda). 2016 Sep 08;6(9):2829-38
pubmed: 27449518
Science. 1974 Jan 11;183(4120):46-51
pubmed: 4587263
Genes Dev. 2012 Jan 15;26(2):137-50
pubmed: 22279046
Mol Cell. 2001 Apr;7(4):705-13
pubmed: 11336695
Mol Biol Cell. 2011 May 15;22(10):1753-65
pubmed: 21441303
Cell Cycle. 2005 Sep;4(9):1223-6
pubmed: 16082215
Genes Dev. 2005 May 15;19(10):1199-210
pubmed: 15905408
Proc Natl Acad Sci U S A. 2017 Jan 17;114(3):552-557
pubmed: 28049846
Nature. 2001 Jan 18;409(6818):355-9
pubmed: 11201745
PLoS Genet. 2017 Sep 15;13(9):e1007006
pubmed: 28915237
Mol Cell Biol. 2003 Mar;23(5):1558-68
pubmed: 12588976
Cell Rep. 2018 Apr 24;23(4):983-992
pubmed: 29694906
Aging Cell. 2020 Mar;19(3):e13108
pubmed: 32087607
Science. 2007 Mar 9;315(5817):1374-5
pubmed: 17347431
Science. 2007 Mar 9;315(5817):1411-5
pubmed: 17347440
Mol Cell Biol. 2007 Nov;27(21):7594-602
pubmed: 17724082
Nat Cell Biol. 2001 Nov;3(11):958-65
pubmed: 11715016
J Mol Cell Biol. 2022 Jan 29;13(12):902-917
pubmed: 34791311
Mol Cell Biol. 2006 Dec;26(23):8781-90
pubmed: 17000772
Cell. 1991 Aug 9;66(3):519-31
pubmed: 1651172
Genetics. 2013 Nov;195(3):643-81
pubmed: 24190922
EMBO J. 2003 Aug 15;22(16):4304-13
pubmed: 12912927
Cell Rep. 2020 Mar 24;30(12):3989-3995.e4
pubmed: 32209462
J Cell Biol. 1996 Apr;133(1):99-110
pubmed: 8601617
Science. 1993 Dec 17;262(5141):1838-44
pubmed: 8266071
Cell Cycle. 2006 Jun;5(11):1223-33
pubmed: 16721058