Together Yes But Not Coupled: New Insights in RAD51 and DMC1 Roles in Plant Meiotic Recombination

The eukaryotic recombinases Rad51 and Dmc1 are essential for DNA strand-exchange between homologous chromosomes during meiosis. Rad51 is also expressed during mitosis and mediates homologous recombination (HR) between sister-chromatids. It has been suggested that Dmc1 might be involved in the switch from inter-sister chromatid recombination in somatic cells to inter-homolog meiotic recombination. At meiosis, the Arabidopsis Atrad51 null mutant fails to synapse and has extensive chromosome fragmentation. The Atdmc1 null mutant is also asynaptic but in this case chromosome fragmentation is absent. Thus in plants, AtDMC1 appears to be indispensable for the inter-homolog homologous recombination, whereas AtRAD51 seems to be more involved in inter-sister recombination. In this work, we have studied a new AtRAD51 knockdown mutant: Atrad51-2, which expresses only a small amount of RAD51 protein. Atrad51-2 mutant plants are sterile and hypersensitive to DNA double-strand break induction, but their vegetative development is apparently normal. The meiotic phenotype of the mutant consists of partial synapsis, an elevated frequency of univalents, a low incidence of chromosome fragmentation and multivalent chromosome associations. Surprisingly, non-homologous chromosomes are involved in 51% of bivalents. The depletion of AtDMC1 in the Atrad51-2 background results in the loss of bivalents and in an increase of chromosome fragmentation. Our results suggest that a critical level of AtRAD51 is required to ensure fidelity of HR during inter-chromosomal exchanges. Assuming the existence of asymmetrical DNA strand invasion during the initial steps of recombination, we have developed a working model in which the initial step in strand invasion is mediated by AtDMC1 with AtRAD51 required to check the fidelity of this process. © 2011 The Authors. The Plant Journal© 2011 Blackwell Publishing Ltd.