AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms

Meiotic crossovers (COs) generate genetic diversity and are critical for the correct completion of meiosis in most species. Their occurrence is tightly constrained but the mechanisms underlying this limitation remain poorly understood. Here we identified the conserved AAA-ATPase FIDGETIN-LIKE-1 (FIGL1) as a negative regulator of meiotic CO formation. We show that Arabidopsis FIGL1 limits CO formation genome-wide, that FIGL1 controls dynamics of the two conserved recombinases DMC1 and RAD51 and that FIGL1 hinders the interaction between homologous chromosomes, suggesting that FIGL1 counteracts DMC1/RAD51-mediated inter-homologue strand invasion to limit CO formation. Further, depleting both FIGL1 and the previously identified anti-CO helicase FANCM synergistically increases crossover frequency. Additionally, we showed that the effect of mutating FANCM on recombination is much lower in F1 hybrids contrasting from the phenotype of inbred lines, while figl1 mutation equally increases crossovers in both contexts. This shows that the modes of action of FIGL1 and FANCM are differently affected by genomic contexts. We propose that FIGL1 and FANCM represent two successive barriers to CO formation, one limiting strand invasion, the other disassembling D-loops to promote SDSA, which when both lifted, leads to a large increase of crossovers, without impairing meiotic progression.Author Summary: Sexually reproducing species produce offspring that are genetically unique from one another, despite having the same parents. This uniqueness is created by meiosis, which is a specialized cell division. After meiosis each parent transmits half of their DNA, but each time this occurs, the 'half portion' of DNA transmitted to offspring is different from the previous. The differences are due to resorting the parental chromosomes, but also recombining them. Here we describe a gene—FIDGETIN-LIKE 1—which limits the amount of recombination that occurs during meiosis. Previously we identified a gene with a similar function, FANCM. FIGL1 and FANCM operate through distinct mechanisms. This discovery will be useful to understand more, from an evolutionary perspective, why recombination is naturally limited. Also this has potentially significant applications for plant breeding which is largely about sampling many 'recombinants' to find individuals that have heritable advantages compared to their parents.