Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression
- University of California, San Francisco, United States
- University of Wisconsin, United States
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
-
Transcriptional Response of S. cerevisiae to Glucose and GalactosePublicly available at the NCBI Short Read Archive (accession no: SRP083773).
-
Transcriptional Response of C. albicans to Glucose and GalactosePublicly available at the NCBI Short Read Archive (accession no: SRP083777).
Article and author information
Author details
Alexander D Johnson
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
© 2016, Dalal et al.
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.
Metrics
-
- 4,207
- views
-
- 904
- downloads
-
- 52
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression
eLife 5:e18981.
https://doi.org/10.7554/eLife.18981
Further reading
-
- Evolutionary Biology
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than ten alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognized.
-
- Evolutionary Biology
Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation by distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60km2 per generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.
