Distribution and regulation of stochasticity and plasticity in Saccharomyces cerevisiae

Dar, Roy D.; Karig, David K; Cooke, John F; Cox, Chris D.; Simpson, Michael L

doi:10.1063/1.3486800

Distribution and regulation of stochasticity and plasticity in Saccharomyces cerevisiae

Journal Article · Fri Jan 01 04:00:00 EST 2010 · Chaos: An Interdisciplinary Journal of Nonlinear Science

DOI:https://doi.org/10.1063/1.3486800· OSTI ID:989716

Dar, Roy D. ^[1]; Karig, David K ^[2]; Cooke, John F ^[2]; Cox, Chris D. ^[1]; Simpson, Michael L ^[2]

University of Tennessee, Knoxville (UTK)
ORNL

Stochasticity is an inherent feature of complex systems with nanoscale structure. In such systems information is represented by small collections of elements (e.g. a few electrons on a quantum dot), and small variations in the populations of these elements may lead to big uncertainties in the information. Unfortunately, little is known about how to work within this inherently noisy environment to design robust functionality into complex nanoscale systems. Here, we look to the biological cell as an intriguing model system where evolution has mediated the trade-offs between fluctuations and function, and in particular we look at the relationships and trade-offs between stochastic and deterministic responses in the gene expression of budding yeast (Saccharomyces cerevisiae). We find gene regulatory arrangements that control the stochastic and deterministic components of expression, and show that genes that have evolved to respond to stimuli (stress) in the most strongly deterministic way exhibit the most noise in the absence of the stimuli. We show that this relationship is consistent with a bursty 2-state model of gene expression, and demonstrate that this regulatory motif generates the most uncertainty in gene expression when there is the greatest uncertainty in the optimal level of gene expression.

Research Organization:: Oak Ridge National Laboratory (ORNL); Center for Nanophase Materials Sciences

Sponsoring Organization:: SC USDOE - Office of Science (SC)

DOE Contract Number:: AC05-00OR22725

OSTI ID:: 989716

Journal Information:: Chaos: An Interdisciplinary Journal of Nonlinear Science, Journal Name: Chaos: An Interdisciplinary Journal of Nonlinear Science Journal Issue: 3 Vol. 20; ISSN 1054-1500

Country of Publication:: United States

Language:: English

References (49)

Tunability and Noise Dependence in Differentiation Dynamics Suel, G. M.; Kulkarni, R. P.; Dworkin, J. Science, Vol. 315, Issue 5819 https://doi.org/10.1126/science.1137455	journal	March 2007
Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters Yang, Chuhu; Bolotin, Eugene; Jiang, Tao Gene, Vol. 389, Issue 1 https://doi.org/10.1016/j.gene.2006.09.029	journal	March 2007
Phenotypic Diversity, Population Growth, and Information in Fluctuating Environments Kussell, E. Science, Vol. 309, Issue 5743 https://doi.org/10.1126/science.1114383	journal	September 2005
Genetic Properties Influencing the Evolvability of Gene Expression Landry, C. R.; Lemos, B.; Rifkin, S. A. Science, Vol. 317, Issue 5834 https://doi.org/10.1126/science.1140247	journal	July 2007
Genomic Expression Programs in the Response of Yeast Cells to Environmental Changes Gasch, Audrey P.; Spellman, Paul T.; Kao, Camilla M. Molecular Biology of the Cell, Vol. 11, Issue 12 https://doi.org/10.1091/mbc.11.12.4241	journal	December 2000
Non-genetic individuality: chance in the single cell Spudich, John L.; Koshland, D. E. Nature, Vol. 262, Issue 5568 https://doi.org/10.1038/262467a0	journal	August 1976
Noise in protein expression scales with natural protein abundance Bar-Even, Arren; Paulsson, Johan; Maheshri, Narendra Nature Genetics, Vol. 38, Issue 6 https://doi.org/10.1038/ng1807	journal	May 2006
Stochasticity in Transcriptional Regulation: Origins, Consequences, and Mathematical Representations Kepler, Thomas B.; Elston, Timothy C. Biophysical Journal, Vol. 81, Issue 6 https://doi.org/10.1016/s0006-3495(01)75949-8	journal	December 2001
Microbial cell individuality and the underlying sources of heterogeneity Avery, Simon V. Nature Reviews Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/nrmicro1460	journal	August 2006
Noise in biological circuits Simpson, Michael L.; Cox, Chris D.; Allen, Michael S. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, Vol. 1, Issue 2 https://doi.org/10.1002/wnan.22	journal	February 2009
Engineering stability in gene networks by autoregulation Becskei, Attila; Serrano, Luis Nature, Vol. 405, Issue 6786 https://doi.org/10.1038/35014651	journal	June 2000
Noise in eukaryotic gene expression Blake, William J.; KÆrn, Mads; Cantor, Charles R. Nature, Vol. 422, Issue 6932 https://doi.org/10.1038/nature01546	journal	April 2003
A Regulatory Network Analysis of Phenotypic Plasticity in Yeast Promislow, Daniel The American Naturalist, Vol. 165, Issue 5 https://doi.org/10.1086/429161	journal	May 2005
Noise Propagation in Gene Networks Pedraza, J. M. Science, Vol. 307, Issue 5717 https://doi.org/10.1126/science.1109090	journal	March 2005
Stochasticity in Transcriptional Regulation: Origins, Consequences, and Mathematical Representations Kepler, Thomas B.; Elston, Timothy C. Biophysical Journal, Vol. 81, Issue 6 https://doi.org/10.1016/S0006-3495(01)75949-8	journal	December 2001
Stochastic Gene Expression in a Single Cell Elowitz, M. B. Science, Vol. 297, Issue 5584 https://doi.org/10.1126/science.1070919	journal	August 2002
Two strategies for gene regulation by promoter nucleosomes Tirosh, I.; Barkai, N. Genome Research, Vol. 18, Issue 7 https://doi.org/10.1101/gr.076059.108	journal	July 2008
Network Inference, Analysis, and Modeling in Systems Biology Albert, Réka The Plant Cell, Vol. 19, Issue 11 https://doi.org/10.1105/tpc.107.054700	journal	November 2007
Regulated cell-to-cell variation in a cell-fate decision system Colman-Lerner, Alejandro; Gordon, Andrew; Serra, Eduard Nature, Vol. 437, Issue 7059 https://doi.org/10.1038/nature03998	journal	September 2005
Control of Stochasticity in Eukaryotic Gene Expression Raser, J. M. Science, Vol. 304, Issue 5678 https://doi.org/10.1126/science.1098641	journal	June 2004
Statistical indicators of collective behavior and functional clusters in gene networks of yeast Živković, J.; Tadić, B.; Wick, N. The European Physical Journal B, Vol. 50, Issue 1-2 https://doi.org/10.1140/epjb/e2006-00103-4	journal	March 2006
Regulation of noise in the expression of a single gene Ozbudak, Ertugrul M.; Thattai, Mukund; Kurtser, Iren Nature Genetics, Vol. 31, Issue 1 https://doi.org/10.1038/ng869	journal	April 2002
Phenotypic Consequences of Promoter-Mediated Transcriptional Noise Blake, William J.; Balázsi, Gábor; Kohanski, Michael A. Molecular Cell, Vol. 24, Issue 6 https://doi.org/10.1016/j.molcel.2006.11.003	journal	December 2006
Stochastic switching as a survival strategy in fluctuating environments Acar, Murat; Mettetal, Jerome T.; van Oudenaarden, Alexander Nature Genetics, Vol. 40, Issue 4 https://doi.org/10.1038/ng.110	journal	March 2008
Gene Regulation at the Single-Cell Level Rosenfeld, N. Science, Vol. 307, Issue 5717 https://doi.org/10.1126/science.1106914	journal	March 2005
Noise Minimization in Eukaryotic Gene Expression Fraser, Hunter B.; Hirsh, Aaron E.; Giaever, Guri PLoS Biology, Vol. 2, Issue 6 https://doi.org/10.1371/journal.pbio.0020137	journal	April 2004
Nano‐enabled synthetic biology Doktycz, Mitchel J.; Simpson, Michael L. Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100165	journal	January 2007
Frequency domain chemical Langevin analysis of stochasticity in gene transcriptional regulation Simpson, Michael L.; Cox, Chris D.; Sayler, Gary S. Journal of Theoretical Biology, Vol. 229, Issue 3 https://doi.org/10.1016/j.jtbi.2004.04.017	journal	August 2004
Chance and necessity in cellular response to challenge Koonin, Eugene V. Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100152	journal	January 2007
Transient-mediated fate determination in a transcriptional circuit of HIV Weinberger, Leor S.; Dar, Roy D.; Simpson, Michael L. Nature Genetics, Vol. 40, Issue 4 https://doi.org/10.1038/ng.116	journal	March 2008
Gene network shaping of inherent noise spectra Austin, D.; Allen, M.; Mccollum, J. 2006 Bio Micro and Nanosystems Conference https://doi.org/10.1109/bmn.2006.330897	conference	January 2006
Exact stochastic simulation of coupled chemical reactions Gillespie, Daniel T. The Journal of Physical Chemistry, Vol. 81, Issue 25 https://doi.org/10.1021/j100540a008	journal	December 1977
A Regulatory Network Analysis of Phenotypic Plasticity in Yeast No authors listed The American Naturalist, Vol. 165, Issue 5 https://doi.org/10.2307/3473383	journal	January 2005
A Genome-Wide Housekeeping Role for TFIID and a Highly Regulated Stress-Related Role for SAGA in Saccharomyces cerevisiae Huisinga, Kathryn L.; Pugh, B. Franklin Molecular Cell, Vol. 13, Issue 4 https://doi.org/10.1016/S1097-2765(04)00087-5	journal	February 2004
A high-resolution atlas of nucleosome occupancy in yeast Lee, William; Tillo, Desiree; Bray, Nicolas Nature Genetics, Vol. 39, Issue 10 https://doi.org/10.1038/ng2117	journal	September 2007
Origins of extrinsic variability in eukaryotic gene expression Volfson, Dmitri; Marciniak, Jennifer; Blake, William J. Nature, Vol. 439, Issue 7078 https://doi.org/10.1038/nature04281	journal	December 2005
A Genome-Wide Housekeeping Role for TFIID and a Highly Regulated Stress-Related Role for SAGA in Saccharomyces cerevisiae Huisinga, Kathryn L.; Pugh, B. Franklin Molecular Cell, Vol. 13, Issue 4 https://doi.org/10.1016/s1097-2765(04)00087-5	journal	February 2004
Correlation Patterns in Gene Expressions along the Cell Cycle of Yeast Živković, Jelena; Mitrović, Marija; Tadić, Bosiljka Complex Networks https://doi.org/10.1007/978-3-642-01206-8_3	book	January 2009
Identification and Distinct Regulation of Yeast TATA Box-Containing Genes Basehoar, Andrew D.; Zanton, Sara J.; Pugh, B. Franklin Cell, Vol. 116, Issue 5 https://doi.org/10.1016/S0092-8674(04)00205-3	journal	March 2004
Genome‐wide transcriptional plasticity underlies cellular adaptation to novel challenge Stern, Shay; Dror, Tali; Stolovicki, Elad Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100147	journal	January 2007
Dynamic proteomics in individual human cells uncovers widespread cell-cycle dependence of nuclear proteins Sigal, Alex; Milo, Ron; Cohen, Ariel Nature Methods, Vol. 3, Issue 7 https://doi.org/10.1038/nmeth892	journal	June 2006
Using noise to probe and characterize gene circuits Cox, C. D.; McCollum, J. M.; Allen, M. S. Proceedings of the National Academy of Sciences, Vol. 105, Issue 31 https://doi.org/10.1073/pnas.0804829105	journal	July 2008
Variability and memory of protein levels in human cells Sigal, Alex; Milo, Ron; Cohen, Ariel Nature, Vol. 444, Issue 7119 https://doi.org/10.1038/nature05316	journal	November 2006
Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise Newman, John R. S.; Ghaemmaghami, Sina; Ihmels, Jan Nature, Vol. 441, Issue 7095 https://doi.org/10.1038/nature04785	journal	May 2006
Origins of extrinsic variability in eukaryotic gene expression Hasty, Jeff 2006 Bio Micro and Nanosystems Conference https://doi.org/10.1109/bmn.2006.330878	conference	January 2006
Transcriptional Bursting from the HIV-1 Promoter Is a Significant Source of Stochastic Noise in HIV-1 Gene Expression Singh, Abhyudai; Razooky, Brandon; Cox, Chris D. Biophysical Journal, Vol. 98, Issue 8 https://doi.org/10.1016/j.bpj.2010.03.001	journal	April 2010
Gene network shaping of inherent noise spectra Austin, D. W.; Allen, M. S.; McCollum, J. M. Nature, Vol. 439, Issue 7076 https://doi.org/10.1038/nature04194	journal	February 2006
Stochastic Gene Expression in Fluctuating Environments Thattai, Mukund; van Oudenaarden, Alexander Genetics, Vol. 167, Issue 1 https://doi.org/10.1534/genetics.167.1.523	journal	May 2004
Identification and Distinct Regulation of Yeast TATA Box-Containing Genes Basehoar, Andrew D.; Zanton, Sara J.; Pugh, B. Franklin Cell, Vol. 116, Issue 5 https://doi.org/10.1016/s0092-8674(04)00205-3	journal	March 2004

Cited By (6)

Perspective: Engineering noise in biological systems towards predictive stochastic design Dar, Roy D.; Weiss, Ron APL Bioengineering, Vol. 2, Issue 2 https://doi.org/10.1063/1.5025033	journal	June 2018
Computational Investigation of Environment-Noise Interaction in Single-Cell Organisms: The Merit of Expression Stochasticity Depends on the Quality of Environmental Fluctuations Lück, Anja; Klimmasch, Lukas; Großmann, Peter Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-17441-8	journal	January 2018
The Low Noise Limit in Gene Expression Dar, Roy D.; Razooky, Brandon S.; Weinberger, Leor S. PLOS ONE, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pone.0140969	journal	October 2015
High-Throughput Yeast Aging Analysis for Cryptococcus (HYAAC) microfluidic device streamlines aging studies in Cryptococcus neoformans Orner, Erika P.; Zhang, Pengchao; Jo, Myeong C. Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0504-5	journal	July 2019
Screening for noise in gene expression identifies drug synergies Dar, R. D.; Hosmane, N. N.; Arkin, M. R. Science, Vol. 344, Issue 6190 https://doi.org/10.1126/science.1250220	journal	June 2014
Fine-tuning of noise in gene expression with nucleosome remodeling Megaridis, Melina R.; Lu, Yiyang; Tevonian, Erin N. APL Bioengineering, Vol. 2, Issue 2 https://doi.org/10.1063/1.5021183	journal	June 2018

Similar Records

Distribution and regulation of stochasticity and plasticity in Saccharomyces cerevisiae

Journal Article · Tue Aug 31 20:00:00 EDT 2010 · Chaos: An Interdisciplinary Journal of Nonlinear Science · OSTI ID:1076448

Mutations in Ran system affected telomere silencing in Saccharomyces cerevisiae

Journal Article · Thu Nov 22 23:00:00 EST 2007 · Biochemical and Biophysical Research Communications · OSTI ID:21032986

Genetic approaches for identifying kinetochore components in Saccharomyces cerevisiae

Conference · Thu Dec 30 23:00:00 EST 1993 · OSTI ID:28434

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
99 GENERAL AND MISCELLANEOUS
DESIGN
DISTRIBUTION
ELECTRONS
FLUCTUATIONS
GENES
PLASTICITY
REGULATIONS
SACCHAROMYCES
SACCHAROMYCES CEREVISIAE
STIMULI
Stochasticity
YEASTS
complex systems
emergent behavior

Distribution and regulation of stochasticity and plasticity in Saccharomyces cerevisiae

Citation Formats

References (49)

Cited By (6)

Similar Records

Related Subjects