FIDGETIN-LIKE 1 Limits Non-Interfering Meiotic Crossovers, Independently of FANCM, by Regulating the Invasion Step of Homologous Recombination

Most species only have an average of one to four meiotic crossovers (COs) per chromosome irrespective of their physical size and despite an excess of recombination precursors. However, the underlying mechanisms constraining CO frequency remain largely unknown. CO-deficient mutants (e.g. zmm) of Arabidopsis thaliana display a reduced fertility, easily noticeable by their manifest reduced fruit length. To find factors that could limit CO formation, a genetic suppressor screen was performed, exploiting Arabidopsis fruit length as a measure of fertility, hence of CO level compared to zmm mutant plants.

We have now identified FIDGETIN-LIKE-1 (FIGL), a conserved AAA-ATPase unfoldase, as a negative regulator of meiotic CO formation: the Arabidopsis figl1 mutation provokes a general increase of non-interfering CO, a minor class in wild type Arabidopsis. Our data show that FIGL1 regulates the homologous template invasion step of meiotic recombination, through regulation of recombinases dynamic.

The FANCM-MHF1-MHF2 helicase complex was previously shown to also limit non-interfering CO, but presumably by promoting non-crossover formation at a later step of meiotic recombination (Crismani et al., 2012; Lorenz et al., 2012; Girard et al., 2014). Consistently, the effects of figl1 and fancm mutations on recombination are cumulative, demonstrating that they act through two different mechanisms. Interestingly, while figl1 and fancm mutations increase largely recombination, the length of the synaptonemal complex is not affected by either mutation.

This work reveals that FIGL1 and FANCM represent two distinct barriers to CO formation which, when both lifted, leads to a large increase of recombination, without impairing chromosome segregation.

- Crismani, W., Girard, C., Froger, N., Pradillo, M., Santos, J. L., Chelysheva, L., et al. (2012). FANCM limits meiotic crossovers. Science, 336(6088), 1588–1590.

- Lorenz, A., Osman, F., Sun, W., Nandi, S., Steinacher, R., & Whitby, M. C. (2012). The Fission Yeast FANCM Ortholog Directs Non-Crossover Recombination During Meiosis. Science, 336(6088), 1585–1588.

- Girard, C., Crismani, W., Froger, N., Mazel, J., Lemhemdi, A., Horlow, C., & Mercier, R. (2014). FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Research, 42(14), 9087–9095.