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Meiotic regulators Ndt80 and ime2 have different roles in Saccharomyces and Neurospora.

ABSTRACT: Meiosis is a highly regulated process in eukaryotic species. The filamentous fungus Neurospora crassa has been shown to be missing homologs of a number of meiotic initiation genes conserved in Saccharomyces cerevisiae, but has three homologs of the well-characterized middle meiotic transcriptional regulator NDT80. In this study, we evaluated the role of all three NDT80 homologs in the formation of female reproductive structures, sexual development, and meiosis. We found that none of the NDT80 homologs were required for meiosis and that even the triple mutant was unaffected. However, strains containing mutations in NCU09915 (fsd-1) were defective in female sexual development and ascospore maturation. vib-1 was a major regulator of protoperithecial development in N. crassa, and double mutants carrying deletions of both vib-1 (NCU03725) and fsd-1 exhibited a synergistic effect on the timing of female reproductive structure (protoperithecia) formation. We further evaluated the role of the N. crassa homolog of IME2, a kinase involved in initiation of meiosis in S. cerevisiae. Strains containing mutations in ime-2 showed unregulated development of protoperithecia. Genetic analysis indicated that mutations in vib-1 were epistatic to ime-2, suggesting that IME-2 may negatively regulate VIB-1 activity. Our data indicate that the IME2/NDT80 pathway is not involved in meiosis in N. crassa, but rather regulates the formation of female reproductive structures.

SUBMITTER: Hutchison EA

PROVIDER: S-EPMC2927755 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Meiotic regulators Ndt80 and ime2 have different roles in Saccharomyces and Neurospora.

Hutchison Elizabeth A EA Glass N Louise NL

Genetics 20100602 4

Meiosis is a highly regulated process in eukaryotic species. The filamentous fungus Neurospora crassa has been shown to be missing homologs of a number of meiotic initiation genes conserved in Saccharomyces cerevisiae, but has three homologs of the well-characterized middle meiotic transcriptional regulator NDT80. In this study, we evaluated the role of all three NDT80 homologs in the formation of female reproductive structures, sexual development, and meiosis. We found that none of the NDT80 ho ...[more]

PMID: 20519745

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Project description:In budding yeast, meiotic commitment is the irreversible continuation of the developmental path of meiosis. After reaching meiotic commitment, cells finish meiosis and gametogenesis, even in the absence of the meiosis-inducing signal. In contrast, if the meiosis-inducing signal is removed and the mitosis-inducing signal is provided prior to reaching meiotic commitment, cells exit meiosis and return to mitosis. Previous work has shown that cells commit to meiosis after prophase I but before entering the meiotic divisions. Since the Ndt80 transcription factor induces expression of middle meiosis genes necessary for the meiotic divisions, we examined the role of the NDT80 transcriptional network in meiotic commitment. Using a microfluidic approach to analyze single cells, we found that cells commit to meiosis in prometaphase I, after the induction of the Ndt80-dependent genes. Our results showed that high-level expression of NDT80 is important for the timing and irreversibility of meiotic commitment. A modest reduction in NDT80 levels delayed meiotic commitment based on meiotic stages, although the timing of each meiotic stage was similar to that of wildtype cells. A further reduction of NDT80 resulted in the surprising finding of inappropriately uncommitted cells: withdrawal of the meiosis-inducing signal and addition of the mitosis-inducing signal to cells at stages beyond metaphase I caused return to mitosis, leading to multi-nucleate cells. Since Ndt80 enhances its own transcription through positive feedback, we tested whether positive feedback ensured the irreversibility of meiotic commitment. Ablating positive feedback in NDT80 expression resulted in a complete loss of meiotic commitment. These findings suggest that irreversibility of meiotic commitment is a consequence of the NDT80 transcriptional positive feedback loop, which provides the high-level of Ndt80 required for the developmental switch of meiotic commitment. These results also illustrate the importance of irreversible meiotic commitment for maintaining genome integrity by preventing formation of multi-nucleate cells.

Project description: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.

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Meiotic regulators Ndt80 and ime2 have different roles in Saccharomyces and Neurospora.

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Meiotic regulators Ndt80 and ime2 have different roles in Saccharomyces and Neurospora.

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