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

PLoS Genet. 2021 May 18;17(5):e1008919. doi: 10.1371/journal.pgen.1008919. eCollection 2021 May.


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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / cytology*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Cycle Proteins / deficiency
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • DNA Breaks, Double-Stranded*
  • DNA Helicases / deficiency
  • DNA Helicases / genetics
  • DNA Helicases / metabolism*
  • DNA-Binding Proteins
  • Genes, Essential
  • Meiosis* / genetics
  • Mutation
  • Rad51 Recombinase / genetics
  • Rad51 Recombinase / metabolism*
  • Rec A Recombinases / genetics
  • Rec A Recombinases / metabolism
  • Recombinational DNA Repair*
  • Repressor Proteins


  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • RAD51B protein, Arabidopsis
  • RAD51D protein, Arabidopsis
  • RAD54 protein, Arabidopsis
  • Repressor Proteins
  • XRCC2 protein, Arabidopsis
  • ATDMC1 protein, Arabidopsis
  • ATRAD51 protein, Arabidopsis
  • Rad51 Recombinase
  • Rec A Recombinases
  • DNA Helicases

Grants and funding

This work was supported by the CNRS, INSERM, Université Clermont Auvergne, a grant from the French government through the IDEX-ISITE-CAP20-25 initiative (16-IDEX-0001-CAP20-25 to O.D.I) and the European Union (H2020-MSCA-ITN-2017:765212-MEICOM to C.I.W). The doctoral fellowship of MH is financed by the European H2020-MSCA-ITN-2017:765212-MEICOM contract. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.