Abstract
Eukaryotic organisms employ a variety of mechanisms during meiosis to assess and ensure the quality of their gametes. Defects or delays in successful meiotic recombination activate conserved mechanisms to delay the meiotic divisions, but many multicellular eukaryotes also induce cell death programs to eliminate gametes deemed to have failed during meiosis. It is generally thought that yeasts lack such mechanisms. Here, we show that in the fission yeast Schizosaccharomyces pombe, defects in meiotic recombination lead to the activation of a checkpoint that is linked to ascus wall endolysis – the process by which spores are released in response to nutritional cues for subsequent germination. Defects in meiotic recombination are sensed as unrepaired DNA damage through the canonical ATM and ATR DNA damage response kinases, and this information is communicated to the machinery that stimulates ascus wall breakdown. Viability of spores that undergo endolysis spontaneously is significantly higher than that seen upon chemical endolysis, demonstrating that this checkpoint contributes to a selective mechanism for the germination of high quality progeny. These results provide the first evidence for the existence of a checkpoint linking germination to meiosis and suggest that analysis solely based on artificial, enzymatic endolysis bypasses an important quality control mechanism in this organism and potentially other ascomycota, which are models widely used to study meiosis.
Highlights
Meiosis lies at the heart of sexual reproduction, encompassing programmed recombination between homologous chromosomes followed by two rounds of specialized cell division that gives rise to haploid gametes or spores
We found that approximately 60 percent of wild type (WT) tetrads undergo ascus wall endolysis within 24 hours; this percentage did not appreciably increase at 48 hours (Figure 1B)
Tetrads arising from the mating of kms1D cells had nearly 3-fold less ascus wall endolysis at 24 hours, this increased to about 40% by 48 hours
Summary
Meiosis lies at the heart of sexual reproduction, encompassing programmed recombination between homologous chromosomes followed by two rounds of specialized cell division that gives rise to haploid gametes or spores. Observations in a broad array of eukaryotic models suggests that meiosis is an error-prone process, requiring numerous checkpoints to ensure successful gametogenesis either through delay of the meiotic divisions or, in higher eukaryotes, the removal of failed meiotic products through apoptotic pathways [5]. S. pombe either lack or have a very weak recombination checkpoint response compared to S. cerevisiae [9,10] It is unclear whether yeasts possess mechanisms to cull progeny resulting from a failed meiosis analogous to the apoptotic pathways employed by multicellular eukaryotes
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