Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression

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Abstract

Evolutionary changes in transcription networks are an important source of diversity across species, yet the quantitative consequences of network evolution have rarely been studied. Here we consider the transcriptional 'rewiring' of the three GAL genes that encode the enzymes needed for cells to convert galactose to glucose. In Saccharomyces cerevisiae, the transcriptional regulator Gal4 binds and activates these genes. In the human pathogen Candida albicans (which last shared a common ancestor with S. cerevisiae some 300 million years ago), we show that different regulators, Rtg1 and Rtg3, activate the three GAL genes. Using single-cell dynamics and RNA-sequencing, we demonstrate that although the overall logic of regulation is the same in both species-the GAL genes are induced by galactose-there are major differences in both the quantitative response of these genes to galactose and in the position of these genes in the overall transcription network structure of the two species.

Data availability

The following data sets were generated

1. Dalal CK
2. Zuleta IA
3. Mitchell KF
4. Andes DR
5. El-Samad H
6. Johnson AD
(2016) Transcriptional Response of S. cerevisiae to Glucose and Galactose
Publicly available at the NCBI Short Read Archive (accession no: SRP083773).

http://www.ncbi.nlm.nih.gov/sra/SRP083773
1. Dalal CK
2. Zuleta IA
3. Mitchell KF
4. Andes DR
5. El-Samad H
6. Johnson AD
(2016) Transcriptional Response of C. albicans to Glucose and Galactose
Publicly available at the NCBI Short Read Archive (accession no: SRP083777).

http://www.ncbi.nlm.nih.gov/sra/SRP083777

Article and author information

Author details

Chiraj K Dalal

Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States

For correspondence
chirajdalal.ucsf@gmail.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3624-8409
Ignacio A Zuleta

Department of Biochemistry and Biophysics, California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Kaitlin F Mitchell

Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, United States

Competing interests
The authors declare that no competing interests exist.
David R Andes

Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, United States

Competing interests
The authors declare that no competing interests exist.
Hana El-Samad

Department of Biochemistry and Biophysics, California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Alexander D Johnson

Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States

For correspondence
ajohnson@cgl.ucsf.edu

Competing interests
The authors declare that no competing interests exist.

Funding

Paul G. Allen Family Foundation

Ignacio A Zuleta
Hana El-Samad

National Institute of General Medical Sciences (P50 GM081879)

Ignacio A Zuleta
Hana El-Samad

National Institutes of Health (R01AI073289)

Kaitlin F Mitchell
David R Andes

National Institutes of Health (R01AI049187)

Chiraj K Dalal
Alexander D Johnson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures in this study were approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Wisconsin (protocol number MV1947) according to the guidelines of the Animal Welfare Act, and The Institute of Laboratory Animal Resources Guide for the Care and Use of Laboratory Animals and Public Health Service Policy.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.