Reduced Mismatch Repair of Heteroduplexes Reveals “Non”-interfering Crossing Over in Wild-Type Saccharomyces cerevisiae

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Abstract
Using small palindromes to monitor meiotic double-strand-break-repair (DSBr) events, we demonstrate that two distinct classes of crossovers occur during meiosis in wild-type yeast. We found that crossovers accompanying 5:3 segregation of a palindrome show no conventional (i.e., positive) interference, while crossovers with 6:2 or normal 4:4 segregation for the same palindrome, in the same cross, do manifest interference. Our observations support the concept of a “non”-interference class and an interference class of meiotic double-strand-break-repair events, each with its own rules for mismatch repair of heteroduplexes. We further show that deletion of MSH4 reduces crossover tetrads with 6:2 or normal 4:4 segregation more than it does those with 5:3 segregation, consistent with Msh4p specifically promoting formation of crossovers in the interference class. Additionally, we present evidence that an ndj1 mutation causes a shift of noncrossovers to crossovers specifically within the “non”-interference class of DSBr events. We use these and other data in support of a model in which meiotic recombination occurs in two phases—one specializing in homolog pairing, the other in disjunction—and each producing both noncrossovers and crossovers.