FIGL1 coordinates with dosage-sensitive BRCA2 in modulating meiotic recombination in maize

J Integr Plant Biol. 2023 Sep;65(9):2107-2121. doi: 10.1111/jipb.13541. Epub 2023 Jul 27.

Abstract

Meiotic crossover (CO) formation between homologous chromosomes ensures their subsequent proper segregation and generates genetic diversity among offspring. In maize, however, the mechanisms that modulate CO formation remain poorly characterized. Here, we found that both maize BREAST CANCER SUSCEPTIBILITY PROTEIN 2 (BRCA2) and AAA-ATPase FIDGETIN-LIKE-1 (FIGL1) act as positive factors of CO formation by controlling the assembly or/and stability of two conserved DNA recombinases RAD51 and DMC1 filaments. Our results revealed that ZmBRCA2 is not only involved in the repair of DNA double-stranded breaks (DSBs), but also regulates CO formation in a dosage-dependent manner. In addition, ZmFIGL1 interacts with RAD51 and DMC1, and Zmfigl1 mutants had a significantly reduced number of RAD51/DMC1 foci and COs. Further, simultaneous loss of ZmFIGL1 and ZmBRCA2 abolished RAD51/DMC1 foci and exacerbated meiotic defects compared with the single mutant Zmbrca2 or Zmfigl1. Together, our data demonstrate that ZmBRCA2 and ZmFIGL1 act coordinately to regulate the dynamics of RAD51/DMC1-dependent DSB repair to promote CO formation in maize. This conclusion is surprisingly different from the antagonistic roles of BRCA2 and FIGL1 in Arabidopsis, implying that, although key factors that control CO formation are evolutionarily conserved, specific characteristics have been adopted in diverse plant species.

Keywords: BRCA2; FIGL1; crossover; maize; meiosis.

MeSH terms

  • ATPases Associated with Diverse Cellular Activities / genetics
  • ATPases Associated with Diverse Cellular Activities / metabolism
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • DNA / metabolism
  • DNA Repair
  • Meiosis / genetics
  • Microtubule-Associated Proteins / metabolism
  • Rad51 Recombinase / genetics
  • Rad51 Recombinase / metabolism
  • Rec A Recombinases / genetics
  • Rec A Recombinases / metabolism
  • Zea mays / genetics
  • Zea mays / metabolism

Substances

  • Rad51 Recombinase
  • Rec A Recombinases
  • DNA
  • Cell Cycle Proteins
  • FIGL1 protein, Arabidopsis
  • ATPases Associated with Diverse Cellular Activities
  • Microtubule-Associated Proteins
  • Arabidopsis Proteins