Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length

Displacement loops (D-loops) are critical intermediates formed during homologous recombination. Rdh54 (a.k.a. Tid1), a Rad54 paralog in Saccharomyces cerevisiae, is well-known for its role with Dmc1 recombinase during meiotic recombination. Yet contrary to Dmc1, Rdh54/Tid1 is also present in somatic...

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Main Authors: Shanaya Shital Shah, Stella Hartono, Aurèle Piazza, Vanessa Som, William Wright, Frédéric Chédin, Wolf-Dietrich Heyer
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/59112
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author Shanaya Shital Shah
Stella Hartono
Aurèle Piazza
Vanessa Som
William Wright
Frédéric Chédin
Wolf-Dietrich Heyer
author_facet Shanaya Shital Shah
Stella Hartono
Aurèle Piazza
Vanessa Som
William Wright
Frédéric Chédin
Wolf-Dietrich Heyer
author_sort Shanaya Shital Shah
collection DOAJ
description Displacement loops (D-loops) are critical intermediates formed during homologous recombination. Rdh54 (a.k.a. Tid1), a Rad54 paralog in Saccharomyces cerevisiae, is well-known for its role with Dmc1 recombinase during meiotic recombination. Yet contrary to Dmc1, Rdh54/Tid1 is also present in somatic cells where its function is less understood. While Rdh54/Tid1 enhances the Rad51 DNA strand invasion activity in vitro, it is unclear how it interplays with Rad54. Here, we show that Rdh54/Tid1 inhibits D-loop formation by Rad51 and Rad54 in an ATPase-independent manner. Using a novel D-loop Mapping Assay, we further demonstrate that Rdh54/Tid1 uniquely restricts the length of Rad51-Rad54-mediated D-loops. The alterations in D-loop properties appear to be important for cell survival and mating-type switch in haploid yeast. We propose that Rdh54/Tid1 and Rad54 compete for potential binding sites within the Rad51 filament, where Rdh54/Tid1 acts as a physical roadblock to Rad54 translocation, limiting D-loop formation and D-loop length.
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spelling doaj.art-b733ef15e04c47d69371f47d2ccc9a962022-12-22T03:51:16ZengeLife Sciences Publications LtdeLife2050-084X2020-11-01910.7554/eLife.59112Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop lengthShanaya Shital Shah0https://orcid.org/0000-0002-2881-2794Stella Hartono1Aurèle Piazza2https://orcid.org/0000-0002-7722-0955Vanessa Som3William Wright4Frédéric Chédin5Wolf-Dietrich Heyer6https://orcid.org/0000-0002-7774-1953Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, United StatesDepartment of Molecular and Cellular Biology, University of California, Davis, Davis, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States; CR CNRS UMR5239, Team Genome Mechanics, Laboratory of Biology and Modelling of the Cell, Ecole Normale Supérieure de Lyon 46, Lyon, FranceDepartment of Microbiology and Molecular Genetics, University of California, Davis, Davis, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States; Mammoth Biosciences, South San Francisco, United StatesDepartment of Molecular and Cellular Biology, University of California, Davis, Davis, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Davis, Davis, United States; Department of Molecular and Cellular Biology, University of California, Davis, Davis, United StatesDisplacement loops (D-loops) are critical intermediates formed during homologous recombination. Rdh54 (a.k.a. Tid1), a Rad54 paralog in Saccharomyces cerevisiae, is well-known for its role with Dmc1 recombinase during meiotic recombination. Yet contrary to Dmc1, Rdh54/Tid1 is also present in somatic cells where its function is less understood. While Rdh54/Tid1 enhances the Rad51 DNA strand invasion activity in vitro, it is unclear how it interplays with Rad54. Here, we show that Rdh54/Tid1 inhibits D-loop formation by Rad51 and Rad54 in an ATPase-independent manner. Using a novel D-loop Mapping Assay, we further demonstrate that Rdh54/Tid1 uniquely restricts the length of Rad51-Rad54-mediated D-loops. The alterations in D-loop properties appear to be important for cell survival and mating-type switch in haploid yeast. We propose that Rdh54/Tid1 and Rad54 compete for potential binding sites within the Rad51 filament, where Rdh54/Tid1 acts as a physical roadblock to Rad54 translocation, limiting D-loop formation and D-loop length.https://elifesciences.org/articles/59112recombinationgenome stabilitydsb repair
spellingShingle Shanaya Shital Shah
Stella Hartono
Aurèle Piazza
Vanessa Som
William Wright
Frédéric Chédin
Wolf-Dietrich Heyer
Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length
eLife
recombination
genome stability
dsb repair
title Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length
title_full Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length
title_fullStr Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length
title_full_unstemmed Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length
title_short Rdh54/Tid1 inhibits Rad51-Rad54-mediated D-loop formation and limits D-loop length
title_sort rdh54 tid1 inhibits rad51 rad54 mediated d loop formation and limits d loop length
topic recombination
genome stability
dsb repair
url https://elifesciences.org/articles/59112
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