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Mlh1-Mlh3 is an endonuclease hypothesized to act in meiosis to resolve double Holliday junctions into crossovers. It also plays a minor role in eukaryotic DNA mismatch repair (MMR). To understand how Mlh1-Mlh3 functions in both meiosis and MMR, we analyzed in baker’s yeast 60 new  mlh3  alleles. Five alleles specifically disrupted MMR, whereas one ( mlh3-32 ) specifically disrupted meiotic crossing over. Mlh1-mlh3 representatives for each class were purified and characterized. Both Mlh1-mlh3-32 (MMR + , crossover - ) and Mlh1-mlh3-45 (MMR - , crossover + ) displayed wild-type endonuclease activities  in vitro . Msh2-Msh3, an MSH complex that acts with Mlh1-Mlh3 in MMR, stimulated the endonuclease activity of Mlh1-mlh3-32 but not Mlh1-mlh3-45, suggesting that Mlh1-mlh3-45 is defective in MSH interactions. Whole genome recombination maps were constructed for wild-type and MMR +  crossover - , MMR -  crossover + , endonuclease defective and null  mlh3  mutants in an S288c/YJM789 hybrid background. Compared to wild-type, all of the  mlh3  mutants showed increases in the number of noncrossover events, consistent with recombination intermediates being resolved through alternative recombination pathways. Our observations provide a structure-function map for Mlh3 that reveals the importance of protein-protein interactions in regulating Mlh1-Mlh3’s enzymatic activity. They also illustrate how defective meiotic components can alter the fate of meiotic recombination intermediates, providing new insights for how meiotic recombination pathways are regulated.

mlh3 mutations in baker’s yeast alter meiotic recombination outcomes by increasing noncrossover events genome-wide