A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes

The respiratory metabolic cycle in budding yeast (Saccharomyces cerevisiae) consists of two phases most simply defined phenomenologically: low oxygen consumption (LOC) and high oxygen consumption (HOC). Each phase is associated with the periodic expression of thousands of genes, producing oscillatin...

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Main Authors: Airoldi, Edoardo M., van Oudenaarden, Alexander, Botstein, David, Slavov, Nikolai G
Other Authors: MIT Materials Research Laboratory
Format: Article
Language:en_US
Published: American Society for Cell Biology 2012
Online Access:http://hdl.handle.net/1721.1/70512
https://orcid.org/0000-0003-2035-1820
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author Airoldi, Edoardo M.
van Oudenaarden, Alexander
Botstein, David
Slavov, Nikolai G
author2 MIT Materials Research Laboratory
author_facet MIT Materials Research Laboratory
Airoldi, Edoardo M.
van Oudenaarden, Alexander
Botstein, David
Slavov, Nikolai G
author_sort Airoldi, Edoardo M.
collection MIT
description The respiratory metabolic cycle in budding yeast (Saccharomyces cerevisiae) consists of two phases most simply defined phenomenologically: low oxygen consumption (LOC) and high oxygen consumption (HOC). Each phase is associated with the periodic expression of thousands of genes, producing oscillating patterns of gene-expression found in synchronized cultures and in single cells of slowly growing unsynchronized cultures. Systematic variation in the durations of the HOC and LOC phases can account quantitatively for well-studied transcriptional responses to growth rate differences. Here we show that a similar mechanism, transitions from the HOC phase to the LOC phase, can account for much of the common environmental stress response (ESR) and for the cross protection by a preliminary heat stress (or slow growth rate) to subsequent lethal heat-stress. Similar to the budding yeast metabolic cycle, we suggest that a metabolic cycle, coupled in a similar way to the ESR, in the distantly related fission yeast, Schizosaccharomyces pombe, and in human can explain gene-expression and respiratory patterns observed in these organisms. Although metabolic cycling is associated with the G0/G1 phase of the cell division cycle of slowly growing budding yeast, transcriptional cycling was detected in the G2 phase of the division cycle in fission yeast, consistent with the idea that respiratory metabolic cycling occurs during the phases of the cell division cycle associated with mass accumulation in these divergent eukaryotes.
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spelling mit-1721.1/705122022-10-03T09:45:04Z A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes Airoldi, Edoardo M. van Oudenaarden, Alexander Botstein, David Slavov, Nikolai G MIT Materials Research Laboratory MIT Materials Research Laboratory Massachusetts Institute of Technology. Department of Biology van Oudenaarden, Alexander Slavov, Nikolai G. van Oudenaarden, Alexander Botstein, David The respiratory metabolic cycle in budding yeast (Saccharomyces cerevisiae) consists of two phases most simply defined phenomenologically: low oxygen consumption (LOC) and high oxygen consumption (HOC). Each phase is associated with the periodic expression of thousands of genes, producing oscillating patterns of gene-expression found in synchronized cultures and in single cells of slowly growing unsynchronized cultures. Systematic variation in the durations of the HOC and LOC phases can account quantitatively for well-studied transcriptional responses to growth rate differences. Here we show that a similar mechanism, transitions from the HOC phase to the LOC phase, can account for much of the common environmental stress response (ESR) and for the cross protection by a preliminary heat stress (or slow growth rate) to subsequent lethal heat-stress. Similar to the budding yeast metabolic cycle, we suggest that a metabolic cycle, coupled in a similar way to the ESR, in the distantly related fission yeast, Schizosaccharomyces pombe, and in human can explain gene-expression and respiratory patterns observed in these organisms. Although metabolic cycling is associated with the G0/G1 phase of the cell division cycle of slowly growing budding yeast, transcriptional cycling was detected in the G2 phase of the division cycle in fission yeast, consistent with the idea that respiratory metabolic cycling occurs during the phases of the cell division cycle associated with mass accumulation in these divergent eukaryotes. National Institutes of Health (U.S.) (GM046406) National Institutes of Health (U.S.). Pioneer Award (1DP1OD003936) National Science Foundation (U.S.) (ECCS 0835623) National Institutes of Health (U.S.) (GM096193) National Institutes of Health (U.S.) National Institutes of Health (U.S.) (U54CA143874) National Institute of General Medical Sciences (U.S.). Center for Quantitative Biology (GM071508) 2012-05-04T19:02:19Z 2012-05-04T19:02:19Z 2012-03 2012-01 Article http://purl.org/eprint/type/JournalArticle 1059-1524 1939-4586 http://hdl.handle.net/1721.1/70512 Slavov, N. et al. “A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes.” Molecular Biology of the Cell (2012): Web. 4 May 2012. https://orcid.org/0000-0003-2035-1820 en_US http://dx.doi.org/10.1091/mbc.E11-11-0961 Molecular Biology of the Cell Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf American Society for Cell Biology American Society for Cell Biology
spellingShingle Airoldi, Edoardo M.
van Oudenaarden, Alexander
Botstein, David
Slavov, Nikolai G
A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes
title A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes
title_full A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes
title_fullStr A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes
title_full_unstemmed A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes
title_short A Conserved Cell Growth Cycle Can Account for the Environmental Stress Responses of Divergent Eukaryotes
title_sort conserved cell growth cycle can account for the environmental stress responses of divergent eukaryotes
url http://hdl.handle.net/1721.1/70512
https://orcid.org/0000-0003-2035-1820
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