Conservation and divergence of meiotic DNA double strand break forming mechanisms in Arabidopsis thaliana.


Journal

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

Informations de publication

Date de publication:
27 09 2021
Historique:
accepted: 04 08 2021
revised: 16 07 2021
received: 01 02 2021
pubmed: 31 8 2021
medline: 17 12 2021
entrez: 30 8 2021
Statut: ppublish

Résumé

In the current meiotic recombination initiation model, the SPO11 catalytic subunits associate with MTOPVIB to form a Topoisomerase VI-like complex that generates DNA double strand breaks (DSBs). Four additional proteins, PRD1/AtMEI1, PRD2/AtMEI4, PRD3/AtMER2 and the plant specific DFO are required for meiotic DSB formation. Here we show that (i) MTOPVIB and PRD1 provide the link between the catalytic sub-complex and the other DSB proteins, (ii) PRD3/AtMER2, while localized to the axis, does not assemble a canonical pre-DSB complex but establishes a direct link between the DSB-forming and resection machineries, (iii) DFO controls MTOPVIB foci formation and is part of a divergent RMM-like complex including PHS1/AtREC114 and PRD2/AtMEI4 but not PRD3/AtMER2, (iv) PHS1/AtREC114 is absolutely unnecessary for DSB formation despite having a conserved position within the DSB protein network and (v) MTOPVIB and PRD2/AtMEI4 interact directly with chromosome axis proteins to anchor the meiotic DSB machinery to the axis.

Identifiants

pubmed: 34458909
pii: 6357737
doi: 10.1093/nar/gkab715
pmc: PMC8464057
doi:

Substances chimiques

ASY1 protein, Arabidopsis 0
ASY3 protein, Arabidopsis 0
Arabidopsis Proteins 0
Cell Cycle Proteins 0
Chromatin 0
DFO protein, Arabidopsis 0
DNA-Binding Proteins 0
Spo11-1 protein, Arabidopsis 0
PHS1 protein, Arabidopsis EC 3.1.3.48
Protein Tyrosine Phosphatases EC 3.1.3.48

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

9821-9835

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

PLoS Genet. 2020 Apr 20;16(4):e1007881
pubmed: 32310948
Chromosoma. 2005 Jul;114(2):127-34
pubmed: 15928951
Nat Genet. 2018 Jan;50(1):130-137
pubmed: 29255257
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12865-70
pubmed: 14563920
Mol Cell Biol. 2010 Sep;30(18):4391-403
pubmed: 20647542
Proteome Sci. 2010 Feb 15;8:8
pubmed: 20205919
J Cell Sci. 2005 Oct 15;118(Pt 20):4621-32
pubmed: 16176934
Cell Cycle. 2015;14(3):305-14
pubmed: 25590558
Genes Cells. 2006 Jun;11(6):615-22
pubmed: 16716192
Science. 2016 Feb 26;351(6276):943-9
pubmed: 26917764
Plant J. 2018 Jul;95(2):385-396
pubmed: 29681056
Genome Biol. 2016 Jul 05;17(1):148
pubmed: 27380939
Cell. 2011 Aug 5;146(3):372-83
pubmed: 21816273
Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15706-11
pubmed: 14668445
Annu Rev Genet. 1999;33:603-754
pubmed: 10690419
Plant Cell. 2007 Oct;19(10):3090-9
pubmed: 17965269
Plant J. 2012 Oct;72(2):271-81
pubmed: 22694475
PLoS Genet. 2013;9(8):e1003674
pubmed: 23950729
Plant Physiol. 2018 Sep;178(1):233-246
pubmed: 30002256
EMBO J. 2007 Sep 19;26(18):4126-37
pubmed: 17762870
Genes Dev. 2017 Sep 15;31(18):1880-1893
pubmed: 29021238
Methods Mol Biol. 2013;990:103-7
pubmed: 23559206
Proc Natl Acad Sci U S A. 2009 Nov 24;106(47):20121-6
pubmed: 19918061
PLoS Genet. 2012;8(7):e1002799
pubmed: 22844245
Front Cell Dev Biol. 2021 Mar 02;9:642737
pubmed: 33748134
Cell. 2002 Dec 13;111(6):791-802
pubmed: 12526806
Annu Rev Plant Biol. 2015;66:297-327
pubmed: 25494464
J Cell Sci. 2007 Oct 15;120(Pt 20):3678-87
pubmed: 17911168
PLoS Genet. 2009 Sep;5(9):e1000654
pubmed: 19763177
Cytogenet Genome Res. 2008;120(3-4):281-90
pubmed: 18504357
Front Plant Sci. 2021 May 18;12:672914
pubmed: 34084178
Genes Dev. 2005 Oct 15;19(20):2488-500
pubmed: 16230536
J Exp Bot. 2020 Dec 31;71(22):7046-7058
pubmed: 32842152
Mol Cell. 2019 Jun 6;74(5):1069-1085.e11
pubmed: 31000436
Cell. 2006 Jun 30;125(7):1321-32
pubmed: 16814718
Nucleic Acids Res. 2021 Mar 18;49(5):2609-2628
pubmed: 33619545
Nature. 2005 Aug 18;436(7053):1053-7
pubmed: 16107854
Genomics. 1998 Aug 1;51(3):351-8
pubmed: 9721205
Plant Cell. 2013 Aug;25(8):2998-3009
pubmed: 23943860
J Biol Chem. 1998 Apr 10;273(15):8549-52
pubmed: 9535825
EMBO J. 2020 Feb 3;39(3):e101625
pubmed: 31556459
Trends Genet. 2019 May;35(5):359-370
pubmed: 30948240
Mol Cell. 2004 Feb 27;13(4):549-59
pubmed: 14992724
Annu Rev Genet. 2013;47:563-99
pubmed: 24050176
Annu Rev Genet. 2014;48:187-214
pubmed: 25421598
Cold Spring Harb Perspect Biol. 2014 Oct 16;7(1):a016634
pubmed: 25324213
Science. 2016 Feb 26;351(6276):939-43
pubmed: 26917763
EMBO J. 2001 Feb 1;20(3):589-600
pubmed: 11157765
Genes Dev. 2010 Jun 15;24(12):1266-80
pubmed: 20551173
Elife. 2019 Jan 18;8:
pubmed: 30657449
Cell. 1997 Feb 7;88(3):375-84
pubmed: 9039264
PLoS Genet. 2007 May 25;3(5):e83
pubmed: 17530928
Cold Spring Harb Perspect Biol. 2015 Oct 28;7(12):
pubmed: 26511629
Genetics. 2006 Aug;173(4):1969-81
pubmed: 16783010
Genome Res. 2018 Apr;28(4):532-546
pubmed: 29530928
Nat Struct Mol Biol. 2021 Jan;28(1):92-102
pubmed: 33398171
Genes Dev. 2007 Sep 1;21(17):2220-33
pubmed: 17785529
Science. 2013 Jan 11;339(6116):215-8
pubmed: 23160953
Mol Cell. 2012 Sep 14;47(5):722-33
pubmed: 22841486
Nature. 2020 Jun;582(7812):426-431
pubmed: 32461690
Curr Opin Genet Dev. 2013 Apr;23(2):147-55
pubmed: 23313097
Chromosoma. 2007 Oct;116(5):471-86
pubmed: 17558514
Plant J. 2006 Oct;48(2):206-16
pubmed: 17018031
Plant Cell. 2008 Aug;20(8):2146-59
pubmed: 18757558
Proc Natl Acad Sci U S A. 2016 Sep 20;113(38):10577-82
pubmed: 27601671
Plant J. 2020 Sep;103(6):2052-2068
pubmed: 32559326
Plant Cell. 2021 Jul 2;33(5):1633-1656
pubmed: 33659989
Semin Cell Dev Biol. 2016 Jun;54:165-76
pubmed: 26995551
Genetics. 1997 Aug;146(4):1253-64
pubmed: 9258671
Curr Biol. 2020 Nov 2;30(21):4113-4127.e6
pubmed: 32857973
PLoS Genet. 2012 Feb;8(2):e1002507
pubmed: 22319460
Genetics. 2001 Feb;157(2):519-32
pubmed: 11156975
Nature. 2021 Apr;592(7852):144-149
pubmed: 33731927
EMBO J. 2007 Dec 12;26(24):5061-70
pubmed: 18007598
Mol Cell. 2019 Jun 6;74(5):1053-1068.e8
pubmed: 31003867
Life Sci Alliance. 2018 Dec 10;1(6):e201800259
pubmed: 30569039
PLoS Genet. 2013;9(8):e1003679
pubmed: 23990794
Genetics. 1997 Jul;146(3):781-95
pubmed: 9215887
Cell Cycle. 2018;17(10):1155-1172
pubmed: 29963942
Nucleic Acids Res. 2019 Nov 4;47(19):10166-10180
pubmed: 31665745
Plant J. 2007 Oct;52(1):41-52
pubmed: 17672843
Genetics. 1991 May;128(1):79-88
pubmed: 2060778
Sci Rep. 2017 Aug 30;7(1):10007
pubmed: 28855712
Curr Genet. 1993;23(4):295-304
pubmed: 8385581
PLoS Genet. 2015 Jul 16;11(7):e1005372
pubmed: 26182244
J Mol Evol. 2004 Apr;58(4):424-41
pubmed: 15114421
Mol Cell. 2013 Jan 10;49(1):43-54
pubmed: 23246437
Curr Biol. 2013 Nov 4;23(21):2090-9
pubmed: 24206843
Nucleic Acids Res. 2020 Nov 18;48(20):11521-11535
pubmed: 32558910
Nat Cell Biol. 2016 Nov;18(11):1208-1220
pubmed: 27723721
Plant Cell. 2012 May;24(5):2058-70
pubmed: 22589466
Chromosome Res. 1996 Nov;4(7):507-16
pubmed: 8939362
Genetics. 1997 Jul;146(3):797-816
pubmed: 9215888
Plant Cell. 2019 Sep;31(9):2259-2275
pubmed: 31266898
Plant Cell. 2004 Aug;16(8):1968-78
pubmed: 15258261
PLoS Genet. 2018 Apr 2;14(4):e1007317
pubmed: 29608566
Cytogenet Genome Res. 2010 Jul;129(1-3):143-53
pubmed: 20628250
Science. 2004 Jan 2;303(5654):89-92
pubmed: 14704428

Auteurs

Nathalie Vrielynck (N)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Katja Schneider (K)

Department of Chromosome Biology, Max Perutz Labs, University of Vienna, Vienna Biocenter, Dr. Bohr-Gasse 9, 1030 Vienna, Austria.

Marion Rodriguez (M)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Jason Sims (J)

Department of Chromosome Biology, Max Perutz Labs, University of Vienna, Vienna Biocenter, Dr. Bohr-Gasse 9, 1030 Vienna, Austria.

Aurélie Chambon (A)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Aurélie Hurel (A)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Arnaud De Muyt (A)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Arnaud Ronceret (A)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Ondrej Krsicka (O)

Department of Chromosome Biology, Max Perutz Labs, University of Vienna, Vienna Biocenter, Dr. Bohr-Gasse 9, 1030 Vienna, Austria.

Christine Mézard (C)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Peter Schlögelhofer (P)

Department of Chromosome Biology, Max Perutz Labs, University of Vienna, Vienna Biocenter, Dr. Bohr-Gasse 9, 1030 Vienna, Austria.

Mathilde Grelon (M)

Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, France.

Articles similaires

Meiosis Schizosaccharomyces Schizosaccharomyces pombe Proteins Spores, Fungal
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger
Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis
Humans DNA Methylation Female Male Alcohol Oxidoreductases

Classifications MeSH