Dynamical Remodeling of the Transcriptome during Short-Term Anaerobiosis in Saccharomyces cerevisiae : Differential Response and Role of Msn2 and/or Msn4 and Other Factors in Galactose and Glucose Media

Lai, Liang-Chuan; Kosorukoff, Alexander L.; Burke, Patricia V.; Kwast, Kurt E.

doi:10.1128/mcb.25.10.4075-4091.2005

Cited by 84Fungal and yeast genetics researchBacterial Genetics and BiotechnologyGene Regulatory Network Analysis

Dynamical Remodeling of the Transcriptome during Short-Term Anaerobiosis in Saccharomyces cerevisiae : Differential Response and Role of Msn2 and/or Msn4 and Other Factors in Galactose and Glucose Media

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Lai, Liang-Chuan, Kosorukoff, Alexander L., Burke, Patricia V., Kwast, Kurt E.·2005·Molecular and Cellular Biology

DOI 10.1128/mcb.25.10.4075-4091.2005PMC PMC1087712

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Abstract

In contrast to previous steady-state analyses of the O(2)-responsive transcriptome, here we examined the dynamics of the response to short-term anaerobiosis (2 generations) in both catabolite-repressed (glucose) and derepressed (galactose) cells, assessed the specific role that Msn2 and Msn4 play in mediating the response, and identified gene networks using a novel clustering approach. Upon shifting cells to anaerobic conditions in galactose medium, there was an acute ( approximately 10 min) yet transient (<45 min) induction of Msn2- and/or Msn4-regulated genes associated with the remodeling of reserve energy and catabolic pathways during the switch from mixed respiro-fermentative to strictly fermentative growth. Concomitantly, MCB- and SCB-regulated networks associated with the G(1)/S transition of the cell cycle were transiently down-regulated along with rRNA processing genes containing PAC and RRPE motifs. Remarkably, none of these gene networks were differentially expressed when cells were shifted in glucose, suggesting that a metabolically derived signal arising from the abrupt cessation of respiration, rather than O(2) deprivation per se, elicits this "stress response." By approximately 0.2 generation of anaerobiosis in both media, more chronic, heme-dependent effects were observed, including the down-regulation of Hap1-regulated networks, derepression of Rox1-regulated networks, and activation of Upc2-regulated ones. Changes in these networks result in the functional remodeling of the cell wall, sterol and sphingolipid metabolism, and dissimilatory pathways required for long-term anaerobiosis. Overall, this study reveals that the acute withdrawal of oxygen can invoke a metabolic state-dependent "stress response" but that acclimatization to oxygen deprivation is a relatively slow process involving complex changes primarily in heme-regulated gene networks.

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Several genome-wide expression studies under low oxygen conditions have reflected that the pattern of expression differs among ERG genes, although some general trends can be extracted.
“Several genome-wide expression studies based on microarray and RNA-Seq analyses under low oxygen conditions have reflected that the pattern of expression differs among ERG genes, although some general trends can be extracted [94,96,98,100,101,102,103].”
From Regulation of Ergosterol Biosynthesis in Saccharomyces cerevisiae (2020) · cites this paper as [102]

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Transcription factors and ABC transporters: from pleiotropic drug resistance to cellular signaling in yeast
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The Hog1 Mitogen-Activated Protein Kinase Mediates a Hypoxic Response inSaccharomyces cerevisiae
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Time-Course Analysis of Gene Expression During theSaccharomyces cerevisiaeHypoxic Response
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Direct Role for the Rpd3 Complex in Transcriptional Induction of the Anaerobic DAN/TIR Genes in Yeast
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Function of Protein Phosphatase-1, Glc7, in Saccharomyces cerevisiae
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The oxygen level determines the fermentation pattern inKluyveromyces lactis
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A Predictive Model of the Oxygen and Heme Regulatory Network in Yeast
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Transcriptional Responses of Saccharomyces cerevisiae to Shift from Respiratory and Respirofermentative to Fully Fermentative Metabolism
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New insights into the Saccharomyces cerevisiae fermentation switch: Dynamic transcriptional response to anaerobicity and glucose-excess
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Quantitative Global Proteomics of Yeast PBP1 Deletion Mutants and Their Stress Responses Identifies Glucose Metabolism, Mitochondrial, and Stress Granule Changes
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The Regulation of Coenzyme Q Biosynthesis in Eukaryotic Cells: All That Yeast Can Tell Us
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Comparison of the transcriptomic "stress response" evoked by antimycin A and oxygen deprivation in saccharomyces cerevisiae
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Impact of assimilable nitrogen availability in glucose uptake kinetics in Saccharomyces cerevisiae during alcoholic fermentation
Palma, M., Madeira, S. C., Mendes‐Ferreira, A., & Sá‐Correia, I. (2012) · Microbial Cell Factories · doi:10.1186/1475-2859-11-99 · Cited by 27 · see citing works
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Foam-stabilizing properties of the yeast protein PAU5 and evaluation of factors that can influence its concentration in must and wine
Kupfer, V. M., Vogt, E. I., Siebert, A., Meyer, M., Vogel, R. F., & Niessen, L. (2017) · Food Research International · doi:10.1016/j.foodres.2017.09.060 · Cited by 22 · see citing works
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Metabolic and transcriptomic response of the wine yeast Saccharomyces cerevisiae strain EC1118 after an oxygen impulse under carbon-sufficient, nitrogen-limited fermentative conditions
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The Saccharomyces cerevisiae flavodoxin-like proteins Ycp4 and Rfs1 play a role in stress response and in the regulation of genes related to metabolism
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The adaptive response of anaerobically grownSaccharomyces cerevisiaeto hydrogen peroxide is mediated by the Yap1 and Skn7 transcription factors
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Loss of the Thioredoxin Reductase Trr1 Suppresses the Genomic Instability of Peroxiredoxin tsa1 Mutants
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Anoxia-Induced Suspended Animation in Budding Yeast as an Experimental Paradigm for Studying Oxygen-Regulated Gene Expression
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Essential Role of One-carbon Metabolism and Gcn4p and Bas1p Transcriptional Regulators during Adaptation to Anaerobic Growth of Saccharomyces cerevisiae
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Heart of the Matter: Discovering the Consensus of Multiple Clustering Results
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Expression in Fission Yeast Is a Principal Regulator of Anaerobic Gene Sterol Regulatory Element Binding Protein
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Regulation of Cytochrome C Oxidase Composition by Oxygen and Oxidative Stress
Liu, J. (2012)
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Dynamical Remodeling of the Transcriptome during Short-Term Anaerobiosis in Saccharomyces cerevisiae: Differential Response and Role of Msn2 and/or Msn4 and Other Factors
Galactose, I., Media, G., Lai, L.-C., Kosorukoff, E. L., Burke, P. V., & Kwast, K. E. (2005)
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Metabolic-State-Dependent Remodeling of the Transcriptome in Response to Anoxia and Subsequent Reoxygenation in Saccharomyces cerevisiae
Lai, L.-C., Kosorukoff, A. L., Burke, P. V., & Kwast, K. E. (2006) · Eukaryotic Cell · doi:10.1128/ec.00107-06 · Cited by 97 · see citing works
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Comparison of the transcriptomic "stress response" evoked by antimycin A and oxygen deprivation in saccharomyces cerevisiae
Lai, L., Kissinger, M. T., Burke, P. V., & Kwast, K. E. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-627 · Cited by 27 · see citing works
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New insights into the Saccharomyces cerevisiae fermentation switch: Dynamic transcriptional response to anaerobicity and glucose-excess
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Authors: Lai, L.-C., Kosorukoff, A. L., Burke, P. V., & Kwast, K. E.
Affiliations: Department of Molecular & Integrative Physiology
University of Illinois Urbana-Champaign (US)
Corresponding author: Kwast, Kurt E.
ORCID: Lai, Liang-Chuan
Venue: Molecular and Cellular Biology
Publisher: Informa UK Limited
Published: 2005-05
Volume: 25
Issue: 10
Pages: 4075-4091
ISSN: 0270-7306 (ISSN-L)
1098-5549
DOI: 10.1128/mcb.25.10.4075-4091.2005
PMC: PMC1087712
OpenAlex: W2158583828
Cited by: 84
References: 94
Citations by year: 2026: 1 · 2025: 1 · 2024: 3 · 2020: 2 · 2019: 2 · 2018: 1 · 2017: 4 · 2016: 3 · 2015: 3 · 2014: 7 · 2013: 3 · 2012: 4
FWCI: 3.76
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Molecular and Cellular Biology (publishedVersion)
PubMed Central (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of General Medical Sciences (R01GM059826, R01-GM59826)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords: anaerobic conditions, oxygen deprivation, Saccharomyces cerevisiae, transcriptome dynamics, Msn2, Msn4, galactose medium, glucose medium, catabolite repression, fermentative growth, G1/S transition, rRNA processing, heme regulation, HAP1, roX1, UPC2, sterol metabolism, cell wall remodeling
MeSH terms: Algorithms, Anaerobiosis, Cell Cycle, Culture Media, DNA, DNA Repair, DNA-Binding Proteins, Energy Metabolism, Galactose, Genes, Fungal, Glucose, Oxygen, RNA, Fungal, RNA, Messenger, Saccharomyces cerevisiae, Time Factors, Transcription Factors, Transcription, Genetic, Gene Expression Regulation, Fungal, Computational Biology, Amino Acid Motifs, Saccharomyces cerevisiae Proteins

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Dynamical Remodeling of the Transcriptome during Short-Term Anaerobiosis in Saccharomyces cerevisiae : Differential Response and Role of Msn2 and/or Msn4 and Other Factors in Galactose and Glucose Media

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