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Eukaryotic Cell, September 2006, p. 1468-1489, Vol. 5, No. 9
1535-9778/06/$08.00+0     doi:10.1128/EC.00107-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

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

Liang-Chuan Lai,1 Alexander L. Kosorukoff,2 Patricia V. Burke,1 and Kurt E. Kwast1*

Department of Molecular and Integrative Physiology,1 Department of Computer Science, University of Illinois, Urbana, Illinois 618012

Received 13 April 2006/ Accepted 8 June 2006

We conducted a comprehensive genomic analysis of the temporal response of yeast to anaerobiosis (six generations) and subsequent aerobic recovery ({approx}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 O2 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 {approx}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.

* Corresponding author. Mailing address: Department of Molecular and Integrative Physiology, University of Illinois, 524 Burrill Hall, 407 S. Goodwin Ave., Urbana, IL 61801. Phone: (217) 244-3122. Fax: (217) 333-1133. E-mail: kwast{at}uiuc.edu.

{dagger} Supplemental material for this article may be found at http://ec.asm.org/.

Eukaryotic Cell, September 2006, p. 1468-1489, Vol. 5, No. 9
1535-9778/06/$08.00+0     doi:10.1128/EC.00107-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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