Abstract
BackgroundThe Saccharomyces cerevisiae RecQ helicase Sgs1 is essential for mitotic and meiotic genome stability. The stage at which Sgs1 acts during meiosis is subject to debate. Cytological experiments showed that a deletion of SGS1 leads to an increase in synapsis initiation complexes and axial associations leading to the proposal that it has an early role in unwinding surplus strand invasion events. Physical studies of recombination intermediates implicate it in the dissolution of double Holliday junctions between sister chromatids.Methodology/Principal FindingsIn this work, we observed an increase in meiotic recombination between diverged sequences (homeologous recombination) and an increase in unequal sister chromatid events when SGS1 is deleted. The first of these observations is most consistent with an early role of Sgs1 in unwinding inappropriate strand invasion events while the second is consistent with unwinding or dissolution of recombination intermediates in an Mlh1- and Top3-dependent manner. We also provide data that suggest that Sgs1 is involved in the rejection of ‘second strand capture’ when sequence divergence is present. Finally, we have identified a novel class of tetrads where non-sister spores (pairs of spores where each contains a centromere marker from a different parent) are inviable. We propose a model for this unusual pattern of viability based on the inability of sgs1 mutants to untangle intertwined chromosomes. Our data suggest that this role of Sgs1 is not dependent on its interaction with Top3. We propose that in the absence of SGS1 chromosomes may sometimes remain entangled at the end of pre-meiotic replication. This, combined with reciprocal crossing over, could lead to physical destruction of the recombined and entangled chromosomes. We hypothesise that Sgs1, acting in concert with the topoisomerase Top2, resolves these structures.ConclusionsThis work provides evidence that Sgs1 interacts with various partner proteins to maintain genome stability throughout meiosis.
Highlights
Meiotic Recombination During meiosis, the process of homologous recombination is critical for ensuring accurate chromosome segregation and in generating genetic diversity
This work provides evidence that Sgs1 interacts with various partner proteins to maintain genome stability throughout meiosis
To investigate the role of Sgs1 in the suppression of meiotic homeologous recombination and sister chromatid exchange, we created a variety of SGS1 mutations in the partial hybrid strain in which chromosome III from S. cerevisiae was replaced with chromosome III from S. paradoxus [24]
Summary
Meiotic Recombination During meiosis, the process of homologous recombination is critical for ensuring accurate chromosome segregation and in generating genetic diversity. Homologous recombination is initiated by a double-strand break (DSB) catalysed by Spo11 [1]. Following the formation of the DSB, 59 strand resection generates 39 single-stranded overhangs that are able to invade the homolog [2]. When breaks are repaired via the crossover pathway, the second single-stranded end is captured by the D-loop following invasion and DNA synthesis. Ligation leads to formation of a double Holliday junction (dHJ) [4,5]. The invading strand is not captured as in the crossover pathway, but is instead displaced. This is followed by strand annealing to complementary sequences on the second DSB end, and DNA synthesis, culminating in the formation of a noncrossover product. Physical studies of recombination intermediates implicate it in the dissolution of double Holliday junctions between sister chromatids
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