Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination

Alexander Lorenz; Alizée Mehats; Fekret Osman; Matthew C Whitby

doi:10.1093/nar/gku1219

Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination

Alexander Lorenz, Alizée Mehats, Fekret Osman, Matthew C Whitby

Medical Sciences

University of Oxford

Research output: Contribution to journal › Article › peer-review

19 Citations (Scopus)

10 Downloads (Pure)

Abstract

During meiosis programmed DNA double-strand breaks (DSBs) are repaired by homologous recombination using the sister chromatid or the homologous chromosome (homolog) as a template. This repair results in crossover (CO) and non-crossover (NCO) recombinants. Only CO formation between homologs provides the physical linkages guiding correct chromosome segregation, which are essential to produce healthy gametes. The factors that determine the CO/NCO decision are still poorly understood. Using Schizosaccharomyces pombe as a model we show that the Rad51/Dmc1-paralog complexes Rad55-Rad57 and Rdl1-Rlp1-Sws1 together with Swi5-Sfr1 play a major role in antagonizing both the FANCM-family DNA helicase/translocase Fml1 and the RecQ-type DNA helicase Rqh1 to limit hybrid DNA formation and promote Mus81-Eme1-dependent COs. A common attribute of these protein complexes is an ability to stabilize the Rad51/Dmc1 nucleoprotein filament, and we propose that it is this property that imposes constraints on which enzymes gain access to the recombination intermediate, thereby controlling the manner in which it is processed and resolved.

Original language	English
Pages (from-to)	13723-13735
Number of pages	13
Journal	Nucleic Acids Research
Volume	42
Issue number	22
Early online date	20 Nov 2014
DOIs	https://doi.org/10.1093/nar/gku1219
Publication status	Published - 16 Dec 2014

Bibliographical note

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

ACKNOWLEDGMENTS
We are grateful to J ¨urg Kohli, Ramsay J. McFarlane, Paul Russell, Gerald R. Smith, Walter W. Steiner and the National BioResource Project (NBRP) Japan for providing strains and to C. Bryer for technical assistance.

FUNDING
Wellcome Trust [090767/Z/09/Z to M.C.W.]; College of Life Sciences and Medicine, University of Aberdeen [to A.L., in part]. Funding for open access charge: Wellcome Trust

Keywords

meiosis
homologous recombination
Schizosaccharomyces pombe
Rad51
Dmc1
DNA helicases

Access to Document

10.1093/nar/gku1219Licence: CC BY

Lorenz&al2014(NAR42)plusSUPPL
C The Author(s) 2014. Published by Oxford University Press on behalf of Nucleic Acids Research. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Final published version, 5.13 MBLicence: CC BY

Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination
Lorenz, A. (Creator), Figshare, 15 Oct 2014
DOI: 10.6084/m9.figshare.1197171
Dataset

Alexander Lorenz
Person: Academic

Cite this

@article{f1b462ef13894fe8b5922839c818291d,

title = "Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination",

abstract = "During meiosis programmed DNA double-strand breaks (DSBs) are repaired by homologous recombination using the sister chromatid or the homologous chromosome (homolog) as a template. This repair results in crossover (CO) and non-crossover (NCO) recombinants. Only CO formation between homologs provides the physical linkages guiding correct chromosome segregation, which are essential to produce healthy gametes. The factors that determine the CO/NCO decision are still poorly understood. Using Schizosaccharomyces pombe as a model we show that the Rad51/Dmc1-paralog complexes Rad55-Rad57 and Rdl1-Rlp1-Sws1 together with Swi5-Sfr1 play a major role in antagonizing both the FANCM-family DNA helicase/translocase Fml1 and the RecQ-type DNA helicase Rqh1 to limit hybrid DNA formation and promote Mus81-Eme1-dependent COs. A common attribute of these protein complexes is an ability to stabilize the Rad51/Dmc1 nucleoprotein filament, and we propose that it is this property that imposes constraints on which enzymes gain access to the recombination intermediate, thereby controlling the manner in which it is processed and resolved.",

keywords = "meiosis, homologous recombination, Schizosaccharomyces pombe, Rad51, Dmc1, DNA helicases",

author = "Alexander Lorenz and Aliz{\'e}e Mehats and Fekret Osman and Whitby, {Matthew C}",

note = "This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. ACKNOWLEDGMENTS We are grateful to J ¨urg Kohli, Ramsay J. McFarlane, Paul Russell, Gerald R. Smith, Walter W. Steiner and the National BioResource Project (NBRP) Japan for providing strains and to C. Bryer for technical assistance. FUNDING Wellcome Trust [090767/Z/09/Z to M.C.W.]; College of Life Sciences and Medicine, University of Aberdeen [to A.L., in part]. Funding for open access charge: Wellcome Trust",

year = "2014",

month = dec,

day = "16",

doi = "10.1093/nar/gku1219",

language = "English",

volume = "42",

pages = "13723--13735",

journal = "Nucleic Acids Research",

issn = "0305-1048",

publisher = "Oxford University Press",

number = "22",

}

TY - JOUR

T1 - Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination

AU - Lorenz, Alexander

AU - Mehats, Alizée

AU - Osman, Fekret

AU - Whitby, Matthew C

N1 - This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. ACKNOWLEDGMENTS We are grateful to J ¨urg Kohli, Ramsay J. McFarlane, Paul Russell, Gerald R. Smith, Walter W. Steiner and the National BioResource Project (NBRP) Japan for providing strains and to C. Bryer for technical assistance. FUNDING Wellcome Trust [090767/Z/09/Z to M.C.W.]; College of Life Sciences and Medicine, University of Aberdeen [to A.L., in part]. Funding for open access charge: Wellcome Trust

PY - 2014/12/16

Y1 - 2014/12/16

N2 - During meiosis programmed DNA double-strand breaks (DSBs) are repaired by homologous recombination using the sister chromatid or the homologous chromosome (homolog) as a template. This repair results in crossover (CO) and non-crossover (NCO) recombinants. Only CO formation between homologs provides the physical linkages guiding correct chromosome segregation, which are essential to produce healthy gametes. The factors that determine the CO/NCO decision are still poorly understood. Using Schizosaccharomyces pombe as a model we show that the Rad51/Dmc1-paralog complexes Rad55-Rad57 and Rdl1-Rlp1-Sws1 together with Swi5-Sfr1 play a major role in antagonizing both the FANCM-family DNA helicase/translocase Fml1 and the RecQ-type DNA helicase Rqh1 to limit hybrid DNA formation and promote Mus81-Eme1-dependent COs. A common attribute of these protein complexes is an ability to stabilize the Rad51/Dmc1 nucleoprotein filament, and we propose that it is this property that imposes constraints on which enzymes gain access to the recombination intermediate, thereby controlling the manner in which it is processed and resolved.

AB - During meiosis programmed DNA double-strand breaks (DSBs) are repaired by homologous recombination using the sister chromatid or the homologous chromosome (homolog) as a template. This repair results in crossover (CO) and non-crossover (NCO) recombinants. Only CO formation between homologs provides the physical linkages guiding correct chromosome segregation, which are essential to produce healthy gametes. The factors that determine the CO/NCO decision are still poorly understood. Using Schizosaccharomyces pombe as a model we show that the Rad51/Dmc1-paralog complexes Rad55-Rad57 and Rdl1-Rlp1-Sws1 together with Swi5-Sfr1 play a major role in antagonizing both the FANCM-family DNA helicase/translocase Fml1 and the RecQ-type DNA helicase Rqh1 to limit hybrid DNA formation and promote Mus81-Eme1-dependent COs. A common attribute of these protein complexes is an ability to stabilize the Rad51/Dmc1 nucleoprotein filament, and we propose that it is this property that imposes constraints on which enzymes gain access to the recombination intermediate, thereby controlling the manner in which it is processed and resolved.

KW - meiosis

KW - homologous recombination

KW - Schizosaccharomyces pombe

KW - Rad51

KW - Dmc1

KW - DNA helicases

U2 - 10.1093/nar/gku1219

DO - 10.1093/nar/gku1219

M3 - Article

C2 - 25414342

SN - 0305-1048

VL - 42

SP - 13723

EP - 13735

JO - Nucleic Acids Research

JF - Nucleic Acids Research

IS - 22

ER -

Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination

Abstract

Bibliographical note

Keywords

Access to Document

Fingerprint

Datasets

Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination

Profiles

Alexander Lorenz

Cite this