Molecular Determinants of Sporulation in <i>Ashbya gossypii</i>

Wasserstrom, Lisa; Lengeler, Klaus B.; Walther, Andrea; Wendland, Jürgen

doi:10.1534/genetics.113.151019

Cited by 22 publications

(33 citation statements)

References 41 publications

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“…The transcription of the A. gossypii ortholog of IRC10, AFR221w, was recently reported to be increased in sporulating cells, suggesting that it may similarly function in sporulation (52). In contrast, ADY3 arose from the whole-genome duplication as a second copy of the CNM67 gene, encoding a constitutive SPB component (50,51,53).…”

Section: Discussionmentioning

confidence: 99%

A Visual Screen of Protein Localization during Sporulation Identifies New Components of Prospore Membrane-Associated Complexes in Budding Yeast

et al. 2014

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During ascospore formation in Saccharomyces cerevisiae, the secretory pathway is reorganized to create new intracellular compartments, termed prospore membranes. Prospore membranes engulf the nuclei produced by the meiotic divisions, giving rise to individual spores. The shape and growth of prospore membranes are constrained by cytoskeletal structures, such as septin proteins, that associate with the membranes. Green fluorescent protein (GFP) fusions to various proteins that associate with septins at the bud neck during vegetative growth as well as to proteins encoded by genes that are transcriptionally induced during sporulation were examined for their cellular localization during prospore membrane growth. We report localizations for over 100 different GFP fusions, including over 30 proteins localized to the prospore membrane compartment. In particular, the screen identified IRC10 as a new component of the leading-edge protein complex (LEP), a ring structure localized to the lip of the prospore membrane. Localization of Irc10 to the leading edge is dependent on SSP1, but not ADY3. Loss of IRC10 caused no obvious phenotype, but an ady3 irc10 mutant was completely defective in sporulation and displayed prospore membrane morphologies similar to those of an ssp1 strain. These results reveal the architecture of the LEP and provide insight into the evolution of this membrane-organizing complex.C omprehensive localization studies have provided a wealth of information about the functions of different Saccharomyces cerevisiae proteins (1, 2). To date, most studies have examined protein localization only during mitotic growth in rich medium. The localization of proteins that are expressed only under specific conditions has not been systematically examined. Moreover, constitutively expressed proteins can also be relocalized under different conditions. Many examples of such changes in distribution occur when yeast cells undergo sporulation (3-6).When diploid yeast cells are starved for nitrogen in the presence of a nonfermentable carbon source, they exit the mitotic cycle and enter the developmental program of meiosis and sporulation (7). Spores are created in an unusual cell division in which membranes are formed de novo in the cytosol and enclose each of the daughter nuclei produced by meiosis. These prospore membranes initially form on the cytoplasmic face of each of the four spindle pole bodies (SPBs) present in meiosis II. The membranes then expand beyond the SPBs to engulf the nuclei. As they do so, their shape is constrained by membrane-associated protein complexes.One of these membrane-associated complexes, the leadingedge protein complex (LEP), composed of the proteins Ssp1, Ady3, and Don1, forms a ring structure at the lip of the prospore membrane (8-10). The LEP is organized in a stratified fashion, with SSP1 being required for the localization of Ady3 and Don1 and ADY3 being required for the localization of Don1. The LEP helps to control the shape of the prospore membrane and is proposed to exert an outward for...

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Section: Discussionmentioning

confidence: 99%

A Visual Screen of Protein Localization during Sporulation Identifies New Components of Prospore Membrane-Associated Complexes in Budding Yeast

et al. 2014

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“…A. gossypii spores are haploid and uninucleate, suggesting that the resulting mycelium formed by a single spore is homothallic since it is itself able to sporulate (29,30). Previous RNA-seq analyses focused on a comparison of the transcriptomes of nonsporulating A. gossypii mutants, e.g., ime1 and ime2 strains, with the wild type (24).…”

Section: Resultsmentioning

confidence: 99%

“…Reads were aligned, and read counts were generated for each annotated gene (using TopHat 2.0.4) based on the published A. gossypii genome. Differential expression based on the RNAseq data was analyzed as described previously using edgeR, DESeq, and cufflinks, and a false discovery rate of Ͻ0.05 was indicative of differential expression (24). RNA-seq was performed by LGC Genomics (Berlin, Germany).…”

Section: Strains and Mediamentioning

confidence: 99%

“…We have previously studied regulation of sporulation in A. gossypii and described a sporulation defect of ime1 and ime2 mutants (24). To address whether MSN2/4 could establish a link between PKA signaling and IME1 expression, we generated MSN2/4 deletion strains.…”

Section: Figmentioning

confidence: 99%

“…Upon nutrient limitation, A. gossypii mycelia initiate developmental events leading to the formation of sporangia, hyphal fragmentation, sporulation, and riboflavin overproduction (22,23). Previously, conserved roles of key S. cerevisiae genes regulating meiosis, e.g., IME1, IME2, IME4, and NDT80, for the sporulation in A. gossypii were identified (24). Similar to bcy1 mutants in yeast, exogenous addition of cAMP to the growth medium promoting constitutive activation of PKA blocks sporulation in A. gossypii (25).…”

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Developmental Growth Control Exerted via the Protein A Kinase Tpk2 in Ashbya gossypii

et al. 2015

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Sporulation in Ashbya gossypii is induced by nutrient-limited conditions and leads to the formation of haploid spores. Using RNA-seq, we have determined a gene set induced upon sporulation, which bears considerable overlap with that of Saccharomyces cerevisiae but also contains A. gossypii-specific genes. Addition of cyclic AMP (cAMP) to nutrient-limited media blocks sporulation and represses the induction of sporulation specific genes. Deletion of the protein kinase A (PKA) catalytic subunits encoded by TPK1 and TPK2 showed reduced growth in tpk1 but enhanced growth in the tpk2 strain; however, both mutants sporulated well. Sporulation can be blocked by cAMP in tpk1 but not in tpk2 strains. Similarly, TPK2 acts at a second developmental switch promoting the break in spore dormancy. In S. cerevisiae, PKA phosphorylates and inhibits Msn2/4. The transcript profiles of the tpk1 and msn2/4 mutants were very similar to that of the wild type under sporulation conditions. However, deletion of the single A. gossypii MSN2/4 homolog generated a specific sporulation defect. We identified a set of genes involved in spore wall assembly that was downregulated in the msn2/4 mutant, particularly DIT2, suggesting that poor spore viability may be due to lysis of spores. Our results reveal specific functional differences between the two catalytic PKA subunits in A. gossypii and identified Tpk2 as the key A kinase that transduces developmental decisions of growth. Our data also suggest that Msn2/4 is involved only at a late step of sporulation in A. gossypii and is not a major regulator of IME1.

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Insights into the identification and evolutionary conservation of key genes in the transcriptional circuits of meiosis initiation and commitment in budding yeast

Das,

Chaudhary,

Ali

et al. 2023

FEBS Open Bio

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Initiation of meiosis in budding yeast does not commit the cells for meiosis. Thus, two distinct signaling cascades may differentially regulate meiosis initiation and commitment in budding yeast. To distinguish between the role of these signaling cascades, we reconstructed protein–protein interaction networks and gene regulatory networks with upregulated genes in meiosis initiation and commitment. Analyzing the integrated networks, we identified four master regulators (MRs) [Ume6p, Msn2p, Met31p, Ino2p], three transcription factors (TFs), and 279 target genes (TGs) unique for meiosis initiation, and three MRs [Ndt80p, Aro80p, Rds2p], 11 TFs, and 948 TGs unique for meiosis commitment. Functional enrichment analysis of these distinct members from the transcriptional cascades for meiosis initiation and commitment revealed that nutritional cues rewire gene expression for initiating meiosis and chromosomal recombination commits cells to meiosis. As meiotic chromosomal recombination is highly conserved in eukaryotes, we compared the evolutionary rate of unique members in the transcriptional cascade of two meiotic phases of Saccharomyces cerevisiae with members of the phylum Ascomycota, revealing that the transcriptional cascade governing chromosomal recombination during meiosis commitment has experienced greater purifying selection pressure (P value = 0.0013, 0.0382, 0.0448, 0.0369, 0.02967, 0.04937, 0.03046, 0.03357 and < 0.00001 for Ashbya gossypii, Yarrowia lipolytica, Debaryomyces hansenii, Aspergillus fumigatus, Neurospora crassa, Kluyveromyces lactis, Schizosaccharomyces pombe, Schizosaccharomyces cryophilus, and Schizosaccharomyces octosporus, respectively). This study demarcates crucial players driving meiosis initiation and commitment and demonstrates their differential rate of evolution in budding yeast.

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Molecular Determinants of Sporulation in Ashbya gossypii

Cited by 22 publications

References 41 publications

A Visual Screen of Protein Localization during Sporulation Identifies New Components of Prospore Membrane-Associated Complexes in Budding Yeast

A Visual Screen of Protein Localization during Sporulation Identifies New Components of Prospore Membrane-Associated Complexes in Budding Yeast

Developmental Growth Control Exerted via the Protein A Kinase Tpk2 in Ashbya gossypii

Insights into the identification and evolutionary conservation of key genes in the transcriptional circuits of meiosis initiation and commitment in budding yeast

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