RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.

An essential component of the homologous recombination machinery in eukaryotes, the RAD54 protein is a member of the SWI2/SNF2 family of helicases with dsDNA-dependent ATPase, DNA translocase, DNA supercoiling and chromatin remodelling activities. It is a motor protein that translocates along dsDNA...

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Main Authors: Miguel Hernandez Sanchez-Rebato, Alida M Bouatta, Maria E Gallego, Charles I White, Olivier Da Ines
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-05-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1008919&type=printable
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author Miguel Hernandez Sanchez-Rebato
Alida M Bouatta
Maria E Gallego
Charles I White
Olivier Da Ines
author_facet Miguel Hernandez Sanchez-Rebato
Alida M Bouatta
Maria E Gallego
Charles I White
Olivier Da Ines
author_sort Miguel Hernandez Sanchez-Rebato
collection DOAJ
description An essential component of the homologous recombination machinery in eukaryotes, the RAD54 protein is a member of the SWI2/SNF2 family of helicases with dsDNA-dependent ATPase, DNA translocase, DNA supercoiling and chromatin remodelling activities. It is a motor protein that translocates along dsDNA and performs multiple functions in homologous recombination. In particular, RAD54 is an essential cofactor for regulating RAD51 activity. It stabilizes the RAD51 nucleofilament, remodels nucleosomes, and stimulates the homology search and strand invasion activities of RAD51. Accordingly, deletion of RAD54 has dramatic consequences on DNA damage repair in mitotic cells. In contrast, its role in meiotic recombination is less clear. RAD54 is essential for meiotic recombination in Drosophila and C. elegans, but plays minor roles in yeast and mammals. We present here characterization of the roles of RAD54 in meiotic recombination in the model plant Arabidopsis thaliana. Absence of RAD54 has no detectable effect on meiotic recombination in otherwise wild-type plants but RAD54 becomes essential for meiotic DSB repair in absence of DMC1. In Arabidopsis, dmc1 mutants have an achiasmate meiosis, in which RAD51 repairs meiotic DSBs. Lack of RAD54 leads to meiotic chromosomal fragmentation in absence of DMC1. The action of RAD54 in meiotic RAD51 activity is thus mainly downstream of the role of RAD51 in supporting the activity of DMC1. Equivalent analyses show no effect on meiosis of combining dmc1 with the mutants of the RAD51-mediators RAD51B, RAD51D and XRCC2. RAD54 is thus required for repair of meiotic DSBs by RAD51 and the absence of meiotic phenotype in rad54 plants is a consequence of RAD51 playing a RAD54-independent supporting role to DMC1 in meiotic recombination.
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spelling doaj.art-6d91ceedaaa244b980cd4eae8823c1cc2025-03-03T05:32:50ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-05-01175e100891910.1371/journal.pgen.1008919RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.Miguel Hernandez Sanchez-RebatoAlida M BouattaMaria E GallegoCharles I WhiteOlivier Da InesAn essential component of the homologous recombination machinery in eukaryotes, the RAD54 protein is a member of the SWI2/SNF2 family of helicases with dsDNA-dependent ATPase, DNA translocase, DNA supercoiling and chromatin remodelling activities. It is a motor protein that translocates along dsDNA and performs multiple functions in homologous recombination. In particular, RAD54 is an essential cofactor for regulating RAD51 activity. It stabilizes the RAD51 nucleofilament, remodels nucleosomes, and stimulates the homology search and strand invasion activities of RAD51. Accordingly, deletion of RAD54 has dramatic consequences on DNA damage repair in mitotic cells. In contrast, its role in meiotic recombination is less clear. RAD54 is essential for meiotic recombination in Drosophila and C. elegans, but plays minor roles in yeast and mammals. We present here characterization of the roles of RAD54 in meiotic recombination in the model plant Arabidopsis thaliana. Absence of RAD54 has no detectable effect on meiotic recombination in otherwise wild-type plants but RAD54 becomes essential for meiotic DSB repair in absence of DMC1. In Arabidopsis, dmc1 mutants have an achiasmate meiosis, in which RAD51 repairs meiotic DSBs. Lack of RAD54 leads to meiotic chromosomal fragmentation in absence of DMC1. The action of RAD54 in meiotic RAD51 activity is thus mainly downstream of the role of RAD51 in supporting the activity of DMC1. Equivalent analyses show no effect on meiosis of combining dmc1 with the mutants of the RAD51-mediators RAD51B, RAD51D and XRCC2. RAD54 is thus required for repair of meiotic DSBs by RAD51 and the absence of meiotic phenotype in rad54 plants is a consequence of RAD51 playing a RAD54-independent supporting role to DMC1 in meiotic recombination.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1008919&type=printable
spellingShingle Miguel Hernandez Sanchez-Rebato
Alida M Bouatta
Maria E Gallego
Charles I White
Olivier Da Ines
RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.
PLoS Genetics
title RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.
title_full RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.
title_fullStr RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.
title_full_unstemmed RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.
title_short RAD54 is essential for RAD51-mediated repair of meiotic DSB in Arabidopsis.
title_sort rad54 is essential for rad51 mediated repair of meiotic dsb in arabidopsis
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1008919&type=printable
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