Role of DNA Replication Factor C1 in Meiotic Recombination

During meiotic recombination, induced double strand breaks (DSBs) are processed into crossovers (COs) and non-COs (NCO). COs are required for proper chromosome segregation and fertility. DNA synthesis is essential for meiotic DSB repair, but current models of meiotic recombination pathways only include leading strand DNA synthesis, while lagging strand synthesis has been assumed to be unnecessary. Here we show that the Arabidopsis DNA REPLICATION FACTOR C1 (RFC1) important for lagging strand synthesis is necessary for fertility, meiotic bivalent formation and homolog segregation. Loss of meiotic RFC1 function caused abnormal meiotic chromosome association and other cytological defects; genetic analyses with other meiotic mutations indicate that RFC1 acts in the MSH4-dependent interference-sensitive pathway for CO formation. In a rfc1 mutant, residual pollen viability is MUS81 dependent and COs exhibit essentially no interference, indicating that these COs form via the MUS81-dependent interference-insensitive pathway. Further analysis of the tomato RFC1 homolog and anther lagging strand synthetic factor in Arabidopsis show that they are also required for meiotic recombination. Taken together, we hypothesize that lagging strand DNA synthesis is important for the formation of double Holliday junctions, but not alternative recombination intermediates. That RFC1 is found in divergent eukaryotes suggests a previously unrecognized and highly conserved role for DNA synthesis in discriminating between recombination pathways.