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Single-cell RNA-seq reveals intrinsic and extrinsic regulatory heterogeneity in yeast responding to stress

View ORCID ProfileAudrey P. Gasch, Feiqiao Brian Yu, James Hose, Leah E. Escalante, Mike Place, Rhonda Bacher, Jad Kanbar, Doina Ciobanu, Laura Sandor, Igor V. Grigoriev, Christina Kendziorski, Stephen R. Quake, Megan N. McClean
doi: https://doi.org/10.1101/179093
Audrey P. Gasch
1Laboratory of Genetics, University of Wisconsin-Madison, Madison WI, 53706
2Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison WI, 53706
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  • ORCID record for Audrey P. Gasch
  • For correspondence: agasch@wisc.edu
Feiqiao Brian Yu
3Department of Bioengineering, Stanford University, Stanford, CA 94305
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James Hose
1Laboratory of Genetics, University of Wisconsin-Madison, Madison WI, 53706
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Leah E. Escalante
1Laboratory of Genetics, University of Wisconsin-Madison, Madison WI, 53706
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Mike Place
2Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison WI, 53706
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Rhonda Bacher
4Department of Biostatistics and Medical Informatics, University of Wisconsin-Madison, Madison WI 53706
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Jad Kanbar
3Department of Bioengineering, Stanford University, Stanford, CA 94305
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Doina Ciobanu
5Department of Energy Joint Genome Institute, Walnut Creek, CA 94598
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Laura Sandor
5Department of Energy Joint Genome Institute, Walnut Creek, CA 94598
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Igor V. Grigoriev
5Department of Energy Joint Genome Institute, Walnut Creek, CA 94598
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Christina Kendziorski
4Department of Biostatistics and Medical Informatics, University of Wisconsin-Madison, Madison WI 53706
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Stephen R. Quake
3Department of Bioengineering, Stanford University, Stanford, CA 94305
6Chan Zuckerberg Biohub, San Francisco, CA, 94518
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Megan N. McClean
7Department of Biomedical Engineering, University of Wisconsin-Madison, Madison WI 53706
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ABSTRACT

From bacteria to humans, individual cells within isogenic populations can show significant variation in stress tolerance, but the nature of this heterogeneity is not clear. To investigate this, we used single-cell RNA sequencing to quantify transcript heterogeneity in single S. cerevisiae cells treated with and without salt stress, to explore population variation and identify cellular covariates that influence the stress-responsive transcriptome. Leveraging the extensive knowledge of yeast transcriptional regulation, we uncovered significant regulatory variation in individual yeast cells, both before and after stress. We also discovered that a subset of cells decouple expression of ribosomal protein genes from the environmental stress response, in a manner partly correlated with the cell cycle but unrelated to the yeast ultradian metabolic cycle. Live-cell imaging of cells expressing pairs of fluorescent regulators, including the transcription factor Msn2 with Dot6, Sfp1, or MAP kinase Hog1, revealed both coordinated and decoupled nucleocytoplasmic shuttling. Together with transcriptomic analysis, our results reveal that cells maintain a cellular filter against decoupled bursts of transcription-factor activation but mount a stress response upon coordinated regulation, even in a subset of unstressed cells.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted August 26, 2017.
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Single-cell RNA-seq reveals intrinsic and extrinsic regulatory heterogeneity in yeast responding to stress
Audrey P. Gasch, Feiqiao Brian Yu, James Hose, Leah E. Escalante, Mike Place, Rhonda Bacher, Jad Kanbar, Doina Ciobanu, Laura Sandor, Igor V. Grigoriev, Christina Kendziorski, Stephen R. Quake, Megan N. McClean
bioRxiv 179093; doi: https://doi.org/10.1101/179093
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Single-cell RNA-seq reveals intrinsic and extrinsic regulatory heterogeneity in yeast responding to stress
Audrey P. Gasch, Feiqiao Brian Yu, James Hose, Leah E. Escalante, Mike Place, Rhonda Bacher, Jad Kanbar, Doina Ciobanu, Laura Sandor, Igor V. Grigoriev, Christina Kendziorski, Stephen R. Quake, Megan N. McClean
bioRxiv 179093; doi: https://doi.org/10.1101/179093

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