FIGL1 attenuates meiotic interhomolog repair and is counteracted by the RAD51 paralog XRCC2 and the chromosome axis protein ASY1 during meiosis

New Phytol. 2024 Dec;244(6):2442-2457. doi: 10.1111/nph.20181. Epub 2024 Oct 17.

Abstract

Two recombinases, RAD51 and DMC1, catalyze meiotic break repair to ensure crossovers (COs) between homologous chromosomes (interhomolog) rather than between sisters (intersister). FIDGETIN-LIKE-1 (FIGL1) downregulates both recombinases. However, the understanding of how FIGL1 functions in meiotic repair remains limited. Here, we discover new genetic interactions of Arabidopsis thaliana FIGL1 that are important in vivo determinants of meiotic repair outcome. In figl1 mutants, compromising RAD51-dependent repair, either through the loss of RAD51 paralogs (RAD51B or XRCC2) or RAD54 or by inhibiting RAD51 catalytic activity, results in either unrepaired breaks or meiotic CO defects. Further, XRCC2 physically interacts with FIGL1 and partially counteracts FIGL1 activity for RAD51 focus formation. Our data indicate that RAD51-mediated repair mechanisms compensate FIGL1 dysfunction. FIGL1 is not necessary for intersister repair in dmc1 but is essential for the completion of meiotic repair in mutants such as asy1 that have impaired DMC1 functions and interhomolog bias. We show that FIGL1 attenuates interhomolog repair, and ASY1 counteracts FIGL1 to promote interhomolog recombination. Altogether, this study underlines that multiple factors can counteract FIGL1 activity to promote accurate meiotic repair.

Keywords: DMC1; FIGL1; RAD51; chromosome axis; crossovers; meiotic DNA repair.

MeSH terms

  • ATPases Associated with Diverse Cellular Activities
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Chromosomes, Plant / genetics
  • DNA Repair*
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Meiosis* / genetics
  • Microtubule-Associated Proteins
  • Mutation* / genetics
  • Protein Binding
  • Rad51 Recombinase* / genetics
  • Rad51 Recombinase* / metabolism

Substances

  • Arabidopsis Proteins
  • DNA-Binding Proteins
  • Rad51 Recombinase
  • ASY1 protein, Arabidopsis
  • XRCC2 protein, Arabidopsis
  • FIGL1 protein, Arabidopsis
  • Cell Cycle Proteins
  • ATPases Associated with Diverse Cellular Activities
  • Microtubule-Associated Proteins