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

• Published in: FEBS open bio Vol. 13; no. 12; pp. 2290 - 2305
• Main Authors: Das, Deepyaman, Chaudhary, Anis Ahmad, Ali, Mohamed A. M., Alawam, Abdullah S., Sarkar, Hironmoy, Podder, Soumita
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01.12.2023; Wiley
• Subjects: Evolutionary conservation; Fungi; Gene expression; gene regulatory network; Gene set enrichment analysis; Genes; Glucose; Kinases; master regulator; Meiosis; Meiosis - genetics; Peptides; Proteins; protein–protein interaction network; Recombination; Saccharomyces cerevisiae; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - metabolism; Saccharomyces cerevisiae Proteins - metabolism; Saccharomycetales - genetics; Saccharomycetales - metabolism; Spermatogenesis; transcription factor; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Yeast; master regulator; transcription factor; protein-protein interaction network; Saccharomyces cerevisiae; gene regulatory network; evolutionary conservation
• ISSN: 2211-5463; 2211-5463
• DOI: 10.1002/2211-5463.13728

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. To distinguish between the roles of signaling cascades for meiosis initiation and commitment in budding yeast, we reconstructed protein–protein interaction networks and gene regulatory networks with upregulated genes in both phases. Analyzing the integrated networks, we identified and performed functional enrichment of unique interactors in both the phases. Lastly, we compared the evolutionary rate for unique members in transcriptional cascade of two meiotic phases.