Evolutionary Genetics of Gene Expression

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (31 January 2019) | Viewed by 44262

Special Issue Editors

Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universitat Munchen, Munich, Germany
Interests: evolutionary genomics; population genetics; gene expression; sex chromosome evolution
Department of Ecology and Evolutionary Biology, School of Biological Sciences, University of California Irvine, Irvine, CA 92697, USA
Interests: functional and comparative genomics; evolution of the expression network; speciation
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Special Issue Information

Dear Colleagues,

Changes in gene expression can generate phenotypic diversity within and between species and, thus, play an important role in evolution. The expression of a gene may be influenced by various genetic events, including point mutations, insertions/deletions, transposable element mobilizations, gene duplications, and chromosomal rearrangements. Furthermore, mutations altering gene expression may be linked to the affected gene, such as changes to transcriptional enhancers (cis-regulation), or may occur elsewhere in the genome and exert their effects through gene regulatory networks (trans-regulation). In this Special Issue, we aim to publish review and original research papers that address the evolution of gene regulation using molecular evolutionary, population genetic, or functional genomic methods. In particular, we encourage submissions that address the genetic basis of gene expression variation, how it influences an organismal phenotype, and how it responds to natural selection.

Dr. John Parsch
Dr. José Ranz
Guest Editors

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Keywords

  • molecular evolution
  • adaptation
  • mutation
  • gene expression
  • gene regulation

Published Papers (9 papers)

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Research

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10 pages, 3518 KiB  
Article
Decreased Temperature Sensitivity of Vestigial Gene Expression in Temperate Populations of Drosophila melanogaster
by Susanne Voigt, Anna Christina Erpf and Wolfgang Stephan
Genes 2019, 10(7), 498; https://doi.org/10.3390/genes10070498 - 28 Jun 2019
Cited by 4 | Viewed by 4194
Abstract
Drosophila melanogaster recently spread from its tropical origin in Africa and became a cosmopolitan species that has adapted to a wide range of different thermal environments, including temperate climates. An important limiting factor of temperate climates has probably been their low and varying [...] Read more.
Drosophila melanogaster recently spread from its tropical origin in Africa and became a cosmopolitan species that has adapted to a wide range of different thermal environments, including temperate climates. An important limiting factor of temperate climates has probably been their low and varying temperatures. The transcriptional output of genes can vary across temperatures, which might have been detrimental while settling in temperate environments. The reduction of temperature-sensitive expression of functionally important genes to ensure consistent levels of gene expression might have been relevant while adapting to such environments. In this study, we focus on the gene vestigial (vg) whose product is a key factor in wing development. We provide evidence that temperature-sensitivity of vg has been buffered in populations from temperate climates. We investigated temperature-sensitivity of vg gene expression in six natural populations, including four temperate populations (three from Europe and one from high-altitude Africa), and two tropical populations from the ancestral species range. All temperate populations exhibited a lower degree of temperature-induced expression plasticity than the tropical populations. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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13 pages, 1243 KiB  
Article
Gene Expression Networks Across Multiple Tissues Are Associated with Rates of Molecular Evolution in Wild House Mice
by Katya L. Mack, Megan Phifer-Rixey, Bettina Harr and Michael W. Nachman
Genes 2019, 10(3), 225; https://doi.org/10.3390/genes10030225 - 18 Mar 2019
Cited by 8 | Viewed by 4328
Abstract
Interactions between genes can influence how selection acts on sequence variation. In gene regulatory networks, genes that affect the expression of many other genes may be under stronger evolutionary constraint than genes whose expression affects fewer partners. While this has been studied for [...] Read more.
Interactions between genes can influence how selection acts on sequence variation. In gene regulatory networks, genes that affect the expression of many other genes may be under stronger evolutionary constraint than genes whose expression affects fewer partners. While this has been studied for individual tissue types, we know less about the effects of regulatory networks on gene evolution across different tissue types. We use RNA-sequencing and genomic data collected from Mus musculus domesticus to construct and compare gene co-expression networks for 10 tissue types. We identify tissue-specific expression and local regulatory variation, and we associate these components of gene expression variation with sequence polymorphism and divergence. We found that genes with higher connectivity across tissues and genes associated with a greater number of cross-tissue modules showed significantly lower genetic diversity and lower rates of protein evolution. Consistent with this pattern, “hub” genes across multiple tissues also showed evidence of greater evolutionary constraint. Using allele-specific expression, we found that genes with cis-regulatory variation had lower average connectivity and higher levels of tissue specificity. Taken together, these results are consistent with strong purifying selection acting on genes with high connectivity within and across tissues. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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12 pages, 1462 KiB  
Article
Population Genetic and Functional Analysis of a cis-Regulatory Polymorphism in the Drosophila melanogaster Metallothionein A gene
by Timothy J. S. Ramnarine, Amanda Glaser-Schmitt, Ana Catalán and John Parsch
Genes 2019, 10(2), 147; https://doi.org/10.3390/genes10020147 - 14 Feb 2019
Cited by 5 | Viewed by 3531
Abstract
Although gene expression can vary extensively within and among populations, the genetic basis of this variation and the evolutionary forces that maintain it are largely unknown. In Drosophila melanogaster, a 49-bp insertion/deletion (indel) polymorphism in the Metallothionein A (MtnA) gene [...] Read more.
Although gene expression can vary extensively within and among populations, the genetic basis of this variation and the evolutionary forces that maintain it are largely unknown. In Drosophila melanogaster, a 49-bp insertion/deletion (indel) polymorphism in the Metallothionein A (MtnA) gene is associated with variation in MtnA expression and oxidative stress tolerance. To better understand the functional and evolutionary significance of this polymorphism, we investigated it in several worldwide populations. In a German population, the deletion was present at a high and stable frequency over multiple seasons and years, and was associated with increased MtnA expression. There was, however, no evidence that the polymorphism was maintained by overdominant, seasonally fluctuating, or sexually antagonistic selection. The deletion was rare in a population from the species’ ancestral range in sub-Saharan Africa and is likely the result of non-African admixture, suggesting that it spread to high frequency following the species’ out-of-Africa expansion. Using data from a North American population, we found that the deletion was associated with MtnA expression and tolerance to oxidative stress induced by menadione sodium bisulfite. Our results are consistent with the deletion being selectively favored in temperate populations due to the increased MtnA expression and oxidative stress tolerance that it confers. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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12 pages, 1939 KiB  
Article
A 24 h Age Difference Causes Twice as Much Gene Expression Divergence as 100 Generations of Adaptation to a Novel Environment
by Sheng-Kai Hsu, Ana Marija Jakšić, Viola Nolte, Neda Barghi, François Mallard, Kathrin A. Otte and Christian Schlötterer
Genes 2019, 10(2), 89; https://doi.org/10.3390/genes10020089 - 28 Jan 2019
Cited by 6 | Viewed by 5062
Abstract
Gene expression profiling is one of the most reliable high-throughput phenotyping methods, allowing researchers to quantify the transcript abundance of expressed genes. Because many biotic and abiotic factors influence gene expression, it is recommended to control them as tightly as possible. Here, we [...] Read more.
Gene expression profiling is one of the most reliable high-throughput phenotyping methods, allowing researchers to quantify the transcript abundance of expressed genes. Because many biotic and abiotic factors influence gene expression, it is recommended to control them as tightly as possible. Here, we show that a 24 h age difference of Drosophila simulans females that were subjected to RNA sequencing (RNA-Seq) five and six days after eclosure resulted in more than 2000 differentially expressed genes. This is twice the number of genes that changed expression during 100 generations of evolution in a novel hot laboratory environment. Importantly, most of the genes differing in expression due to age introduce false positives or negatives if an adaptive gene expression analysis is not controlled for age. Our results indicate that tightly controlled experimental conditions, including precise developmental staging, are needed for reliable gene expression analyses, in particular in an evolutionary framework. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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13 pages, 3672 KiB  
Article
Comparative Analysis of Developmental Transcriptome Maps of Arabidopsis thaliana and Solanum lycopersicum
by Aleksey A. Penin, Anna V. Klepikova, Artem S. Kasianov, Evgeny S. Gerasimov and Maria D. Logacheva
Genes 2019, 10(1), 50; https://doi.org/10.3390/genes10010050 - 15 Jan 2019
Cited by 14 | Viewed by 4546
Abstract
The knowledge of gene functions in model organisms is the starting point for the analysis of gene function in non-model species, including economically important ones. Usually, the assignment of gene functions is based on sequence similarity. In plants, due to a highly intricate [...] Read more.
The knowledge of gene functions in model organisms is the starting point for the analysis of gene function in non-model species, including economically important ones. Usually, the assignment of gene functions is based on sequence similarity. In plants, due to a highly intricate gene landscape, this approach has some limitations. It is often impossible to directly match gene sets from one plant species to another species based only on their sequences. Thus, it is necessary to use additional information to identify functionally similar genes. Expression patterns have great potential to serve as a source of such information. An important prerequisite for the comparative analysis of transcriptomes is the existence of high-resolution expression maps consisting of comparable samples. Here, we present a transcriptome atlas of tomato (Solanum lycopersicum) consisting of 30 samples of different organs and developmental stages. The samples were selected in a way that allowed for side-by-side comparison with the Arabidopsis thaliana transcriptome map. Newly obtained data are integrated in the TraVA database and are available online, together with tools for their analysis. In this paper, we demonstrate the potential of comparing transcriptome maps for inferring shifts in the expression of paralogous genes. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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22 pages, 4195 KiB  
Article
Transcriptome Analysis Reveals Candidate Genes for Cold Tolerance in Drosophila ananassae
by Annabella Königer and Sonja Grath
Genes 2018, 9(12), 624; https://doi.org/10.3390/genes9120624 - 12 Dec 2018
Cited by 16 | Viewed by 4732
Abstract
Coping with daily and seasonal temperature fluctuations is a key adaptive process for species to colonize temperate regions all over the globe. Over the past 18,000 years, the tropical species Drosophila ananassae expanded its home range from tropical regions in Southeast Asia to [...] Read more.
Coping with daily and seasonal temperature fluctuations is a key adaptive process for species to colonize temperate regions all over the globe. Over the past 18,000 years, the tropical species Drosophila ananassae expanded its home range from tropical regions in Southeast Asia to more temperate regions. Phenotypic assays of chill coma recovery time (CCRT) together with previously published population genetic data suggest that only a small number of genes underlie improved cold hardiness in the cold-adapted populations. We used high-throughput RNA sequencing to analyze differential gene expression before and after exposure to a cold shock in coldtolerant lines (those with fast chill coma recovery, CCR) and cold-sensitive lines (slow CCR) from a population originating from Bangkok, Thailand (the ancestral species range). We identified two candidate genes with a significant interaction between cold tolerance and cold shock treatment: GF14647 and GF15058. Further, our data suggest that selection for increased cold tolerance did not operate through the increased activity of heat shock proteins, but more likely through the stabilization of the actin cytoskeleton and a delayed onset of apoptosis. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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Review

Jump to: Research

21 pages, 1454 KiB  
Review
Cloudy with a Chance of Insights: Context Dependent Gene Regulation and Implications for Evolutionary Studies
by Elisa Buchberger, Micael Reis, Ting-Hsuan Lu and Nico Posnien
Genes 2019, 10(7), 492; https://doi.org/10.3390/genes10070492 - 28 Jun 2019
Cited by 14 | Viewed by 7580
Abstract
Research in various fields of evolutionary biology has shown that divergence in gene expression is a key driver for phenotypic evolution. An exceptional contribution of cis-regulatory divergence has been found to contribute to morphological diversification. In the light of these findings, the [...] Read more.
Research in various fields of evolutionary biology has shown that divergence in gene expression is a key driver for phenotypic evolution. An exceptional contribution of cis-regulatory divergence has been found to contribute to morphological diversification. In the light of these findings, the analysis of genome-wide expression data has become one of the central tools to link genotype and phenotype information on a more mechanistic level. However, in many studies, especially if general conclusions are drawn from such data, a key feature of gene regulation is often neglected. With our article, we want to raise awareness that gene regulation and thus gene expression is highly context dependent. Genes show tissue- and stage-specific expression. We argue that the regulatory context must be considered in comparative expression studies. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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10 pages, 879 KiB  
Review
Modulation and Evolution of Animal Development through microRNA Regulation of Gene Expression
by Sebastian Kittelmann and Alistair P. McGregor
Genes 2019, 10(4), 321; https://doi.org/10.3390/genes10040321 - 25 Apr 2019
Cited by 30 | Viewed by 4862
Abstract
microRNAs regulate gene expression by blocking the translation of mRNAs and/or promoting their degradation. They, therefore, play important roles in gene regulatory networks (GRNs) by modulating the expression levels of specific genes and can tune GRN outputs more broadly as part of feedback [...] Read more.
microRNAs regulate gene expression by blocking the translation of mRNAs and/or promoting their degradation. They, therefore, play important roles in gene regulatory networks (GRNs) by modulating the expression levels of specific genes and can tune GRN outputs more broadly as part of feedback loops. These roles for microRNAs provide developmental buffering on one hand but can facilitate evolution of development on the other. Here we review how microRNAs can modulate GRNs during animal development as part of feedback loops and through their individual or combinatorial targeting of multiple different genes in the same network. We then explore how changes in the expression of microRNAs and consequently targets can facilitate changes in GRNs that alter development and lead to phenotypic evolution. The reviewed studies exemplify the key roles played by microRNAs in the regulation and evolution of gene expression during developmental processes in animals. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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13 pages, 8850 KiB  
Review
The Elaboration of miRNA Regulation and Gene Regulatory Networks in Plant–Microbe Interactions
by Sophie de Vries, Jan de Vries and Laura E. Rose
Genes 2019, 10(4), 310; https://doi.org/10.3390/genes10040310 - 21 Apr 2019
Cited by 14 | Viewed by 4795
Abstract
Plants are exposed to diverse abiotic and biotic stimuli. These require fast and specific integrated responses. Such responses are coordinated at the protein and transcript levels and are incorporated into larger regulatory networks. Here, we focus on the evolution of transcriptional regulatory networks [...] Read more.
Plants are exposed to diverse abiotic and biotic stimuli. These require fast and specific integrated responses. Such responses are coordinated at the protein and transcript levels and are incorporated into larger regulatory networks. Here, we focus on the evolution of transcriptional regulatory networks involved in plant–pathogen interactions. We discuss the evolution of regulatory networks and their role in fine-tuning plant defense responses. Based on the observation that many of the cornerstones of immune signaling in angiosperms are also present in streptophyte algae, it is likely that some regulatory components also predate the origin of land plants. The degree of functional conservation of many of these ancient components has not been elucidated. However, ongoing functional analyses in bryophytes show that some components are conserved. Hence, some of these regulatory components and how they are wired may also trace back to the last common ancestor of land plants or earlier. Of course, an understanding of the similarities and differences during the evolution of plant defense networks cannot ignore the lineage-specific coevolution between plants and their pathogens. In this review, we specifically focus on the small RNA regulatory networks involved in fine-tuning of the strength and timing of defense responses and highlight examples of pathogen exploitation of the host RNA silencing system. These examples illustrate well how pathogens frequently target gene regulation and thereby alter immune responses on a larger scale. That this is effective is demonstrated by the diversity of pathogens from distinct kingdoms capable of manipulating the same gene regulatory networks, such as the RNA silencing machinery. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Gene Expression)
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