RAD51 supports DMC1 by inhibiting the SMC5/6 complex during meiosis

Plant Cell. 2021 Aug 31;33(8):2869-2882. doi: 10.1093/plcell/koab136.

Abstract

Meiosis is a fundamental process for sexual reproduction in most eukaryotes and the evolutionarily conserved recombinases RADiation sensitive51 (RAD51) and Disrupted Meiotic cDNA1 (DMC1) are essential for meiosis and thus fertility. The mitotic function of RAD51 is clear, but the meiotic function of RAD51 remains largely unknown. Here we show that RAD51 functions as an interacting protein to restrain the Structural Maintenance of Chromosomes5/6 (SMC5/6) complex from inhibiting DMC1. We unexpectedly found that loss of the SMC5/6 partially suppresses the rad51 knockout mutant in terms of sterility, pollen inviability, and meiotic chromosome fragmentation in a DMC1-dependent manner in Arabidopsis thaliana. Biochemical and cytological studies revealed that the DMC1 localization in meiotic chromosomes is inhibited by the SMC5/6 complex, which is attenuated by RAD51 through physical interactions. This study not only identified the long-sought-after function of RAD51 in meiosis but also discovered the inhibition of SMC5/6 on DMC1 as a control mechanism during meiotic recombination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Chromosome Pairing
  • Chromosomes, Plant
  • Gene Expression Regulation, Plant
  • Loss of Function Mutation
  • Meiosis
  • Multiprotein Complexes / metabolism
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Plant Infertility / genetics
  • Pollen / genetics
  • Rad51 Recombinase / genetics*
  • Rad51 Recombinase / metabolism
  • Rec A Recombinases / genetics
  • Rec A Recombinases / metabolism*

Substances

  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Multiprotein Complexes
  • Nuclear Proteins
  • SMC5 protein, Arabidopsis
  • SNI1 protein, Arabidopsis
  • ATDMC1 protein, Arabidopsis
  • ATRAD51 protein, Arabidopsis
  • Rad51 Recombinase
  • Rec A Recombinases