Cited by 97Fungal and yeast genetics researchRedox biology and oxidative stressBacterial Genetics and Biotechnology

Metabolic-State-Dependent Remodeling of the Transcriptome in Response to Anoxia and Subsequent Reoxygenation in Saccharomyces cerevisiae

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Lai, Liang-Chuan, Kosorukoff, Alexander L., Burke, Patricia V., Kwast, Kurt E.·2006·Eukaryotic Cell

Abstract

ABSTRACT We conducted a comprehensive genomic analysis of the temporal response of yeast to anaerobiosis (six generations) and subsequent aerobic recovery (≈2 generations) to reveal metabolic-state (galactose versus glucose)-dependent differences in gene network activity and function. Analysis of variance showed that far fewer genes responded (raw P value of ≤10 −8 ) to the O 2 shifts in glucose (1,603 genes) than in galactose (2,388 genes). Gene network analysis reveals that this difference is due largely to the failure of “stress”-activated networks controlled by Msn2/4, Fhl1, MCB, SCB, PAC, and RRPE to transiently respond to the shift to anaerobiosis in glucose as they did in galactose. After ≈1 generation of anaerobiosis, the response was similar in both media, beginning with the deactivation of Hap1 and Hap2/3/4/5 networks involved in mitochondrial functions and the concomitant derepression of Rox1-regulated networks for carbohydrate catabolism and redox regulation and ending (≥2 generations) with the activation of Upc2- and Mot3-regulated networks involved in sterol and cell wall homeostasis. The response to reoxygenation was rapid (<5 min) and similar in both media, dominated by Yap1 networks involved in oxidative stress/redox regulation and the concomitant activation of heme-regulated ones. Our analyses revealed extensive networks of genes subject to combinatorial regulation by both heme-dependent (e.g., Hap1, Hap2/3/4/5, Rox1, Mot3, and Upc2) and heme-independent (e.g., Yap1, Skn7, and Puf3) factors under these conditions. We also uncover novel functions for several cis -regulatory sites and trans -acting factors and define functional regulons involved in the physiological acclimatization to changes in oxygen availability.

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  • Some of the genes that are most strongly induced upon reoxygenation are involved in the two first modules of ergosterol synthesis.

    “In accordance with this hypothesis, some of the genes that are most strongly induced upon reoxygenation are involved in the two first modules of ergosterol synthesis [103].”
  • 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].”

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  1. [59]59. Laabs, T. L., D. D. Markwardt, M. G. Slattery, L. L. Newcomb, D. J. Stillman, and W. Heideman. 2003. ACE2 is required for daughter cellspecific G1 delay in Saccharomyces cerevisiae . Proc. Natl. Acad. Sci. USA 100: 10275-10280.

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Authors
Lai, L.-C., Kosorukoff, A. L., Burke, P. V., & Kwast, K. E.
Affiliations
  • Department of Molecular and Integrative Physiology
  • University of Illinois Urbana-Champaign (US)
Corresponding author
Kwast, Kurt E.
Venue
Eukaryotic Cell
Published
2006-09
Volume
5
Issue
9
Pages
1468-1489
ISSN
  • 1535-9778 (ISSN-L)
  • 1535-9786
OpenAlex
W2162295516
Cited by
97
References
113
Citations by year
2026: 3 · 2025: 2 · 2024: 1 · 2022: 1 · 2021: 6 · 2020: 3 · 2019: 1 · 2018: 3 · 2017: 7 · 2016: 4 · 2015: 1 · 2014: 8 · 2013: 5 · 2012: 9
FWCI
4.03
Type
journal article
Language
en
Open access
Locations
  • Eukaryotic Cell (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM059826)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
anaerobic conditions, reoxygenation, Saccharomyces cerevisiae, transcriptome dynamics, oxygen availability, YAP, HAP1, roX1, UPC2, Skn7, heme regulation, redox regulation, oxidative stress, carbohydrate catabolism, metabolic status
MeSH terms
Anaerobiosis, Galactose, Glucose, Oxygen, Saccharomyces cerevisiae, Down-Regulation, Up-Regulation, Gene Expression Regulation, Fungal, Cluster Analysis, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling

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