scholarly journals Contributions of cis- and trans-Regulatory Evolution to Transcriptomic Divergence across Populations in the Drosophila mojavensis Larval Brain

2020 ◽  
Vol 12 (8) ◽  
pp. 1407-1418
Author(s):  
Kyle M Benowitz ◽  
Joshua M Coleman ◽  
Carson W Allan ◽  
Luciano M Matzkin
Keyword(s):  
Gene Expression ◽  
Population Level ◽  
F1 Hybrids ◽  
Evolutionary Divergence ◽  
Drosophila Mojavensis ◽  
Regulatory Evolution ◽  
Larval Brain ◽  
Expression Evolution ◽  
Trans Regulation ◽  
In Cis

Abstract Natural selection on gene expression was originally predicted to result primarily in cis- rather than trans-regulatory evolution, due to the expectation of reduced pleiotropy. Despite this, numerous studies have ascribed recent evolutionary divergence in gene expression predominantly to trans-regulation. Performing RNA-seq on single isofemale lines from genetically distinct populations of the cactophilic fly Drosophila mojavensis and their F1 hybrids, we recapitulated this pattern in both larval brains and whole bodies. However, we demonstrate that improving the measurement of brain expression divergence between populations by using seven additional genotypes considerably reduces the estimate of trans-regulatory contributions to expression evolution. We argue that the finding of trans-regulatory predominance can result from biases due to environmental variation in expression or other sources of noise, and that cis-regulation is likely a greater contributor to transcriptional evolution across D. mojavensis populations. Lastly, we merge these lines of data to identify several previously hypothesized and intriguing novel candidate genes, and suggest that the integration of regulatory and population-level transcriptomic data can provide useful filters for the identification of potentially adaptive genes.

scholarly journals Evolution of Gene Expression and Splicing in Parallel Cold-Adapted Fly Populations

2019 ◽  
Author(s):  
Yuheng Huang ◽  
Justin B. Lack ◽  
Grant T. Hoppel ◽  
John E. Pool
Keyword(s):  
Gene Expression ◽  
Adaptive Evolution ◽  
Parallel Evolution ◽  
Population Variation ◽  
Regulatory Evolution ◽  
Cold Adapted ◽  
Mitochondrial Functions ◽  
Expression Evolution ◽  
Gene Regulatory ◽  
Trans Regulation

AbstractChanges in gene regulation at multiple levels may comprise an important share of the molecular changes underlying adaptive evolution in nature. However, few studies have assayed within- and between-population variation in gene regulatory traits at a transcriptomic scale, and therefore inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. The cold-adapted populations were known to show population genetic evidence for parallel evolution at the SNP level, and here we find significant although somewhat limited evidence for parallel expression evolution between them, and less evidence for parallel splicing evolution. We find that genes with mitochondrial functions are particularly enriched among candidates for adaptive expression evolution. We also develop a method to estimate cis-versus trans-encoded contributions to expression or splicing differences that does not rely on the presence of fixed differences between parental strains. Applying this method, we infer important roles of both cis-and trans-regulation among our putatively adaptive expression and splicing differences. The apparent contributions of cis-versus trans-regulation to adaptive evolution vary substantially among population pairs, with an Ethiopian pair showing pervasive trans-effects, suggesting that basic characteristics of regulatory evolution may depend on biological context. These findings expand our knowledge of adaptive gene regulatory evolution and our ability to make inferences about this important and widespread process.

scholarly journals Modeling gene expression evolution with EvoGeneX uncovers differences in evolution of species, organs and sexes

2020 ◽  
Author(s):  
Soumitra Pal ◽  
Brian Oliver ◽  
Teresa M. Przytycka
Keyword(s):  
Gene Expression ◽  
Evolutionary Dynamics ◽  
Computational Method ◽  
Specific Gene ◽  
Species Variation ◽  
Evolutionary Divergence ◽  
Sequence Evolution ◽  
Study Gene Expression ◽  
Expression Evolution ◽  
Gene Expression Evolution

AbstractWhile DNA sequence evolution has been well studied, the expression of genes is also subject to evolution. Yet the evolution of gene expression is currently not well understood. In recent years, new tissue/organ specific gene expression datasets spanning several organisms across the tree of life, have become available providing the opportunity to study gene expression evolution in more detail. However, while a theoretical model to study evolution of continuous traits exist, in practice computational methods often cannot distinguish, with confidence, between alternative evolutionary scenarios. This lack of power has been attributed to the modest number of species with available expression data.To solve this challenge, we introduce EvoGeneX, a computationally efficient method to uncover the mode of gene expression evolution based on the Ornstein-Uhlenbeck process. Importantly, EvoGeneX in addition to modelling expression variations between species, models within species variation. To estimate the within species variation, EvoGeneX formally incorporates the data from biological replicates as a part of the mathematical model. We show that by modelling the within species diversity EvoGeneX significantly outperforms the currently available computational method. In addition, to facilitate comparative analysis of gene expression evolution, we introduce a new approach to measure the dynamics of evolutionary divergence of a group of genes.We used EvoGeneX to analyse the evolution of expression across different organs, species and sexes of the Drosophila genus. Our analysis revealed differences in the evolutionary dynamics of male and female gonads, and uncovered examples of adaptive evolution of genes expressed in the head and in the thorax.

scholarly journals Gene and Transposable Element Expression Evolution Following Recent and Past Polyploidy Events in Spartina (Poaceae)

2021 ◽  
Vol 12 ◽  
Author(s):  
Delphine Giraud ◽  
Oscar Lima ◽  
Mathieu Rousseau-Gueutin ◽  
Armel Salmon ◽  
Malika Aïnouche
Keyword(s):  
Gene Expression ◽  
Transposable Element ◽  
Divergence Time ◽  
Reticulate Evolution ◽  
F1 Hybrids ◽  
Polyploid Evolution ◽  
Gene Expression Dynamics ◽  
Expression Evolution ◽  
Weak Expression ◽  
Spartina Versicolor

Gene expression dynamics is a key component of polyploid evolution, varying in nature, intensity, and temporal scales, most particularly in allopolyploids, where two or more sub-genomes from differentiated parental species and different repeat contents are merged. Here, we investigated transcriptome evolution at different evolutionary time scales among tetraploid, hexaploid, and neododecaploid Spartina species (Poaceae, Chloridoideae) that successively diverged in the last 6–10 my, at the origin of differential phenotypic and ecological traits. Of particular interest are the recent (19th century) hybridizations between the two hexaploids Spartina alterniflora (2n = 6x = 62) and S. maritima (2n = 6x = 60) that resulted in two sterile F1 hybrids: Spartina × townsendii (2n = 6x = 62) in England and Spartina × neyrautii (2n = 6x = 62) in France. Whole genome duplication of S. × townsendii gave rise to the invasive neo-allododecaploid species Spartina anglica (2n = 12x = 124). New transcriptome assemblies and annotations for tetraploids and the enrichment of previously published reference transcriptomes for hexaploids and the allododecaploid allowed identifying 42,423 clusters of orthologs and distinguishing 21 transcribed transposable element (TE) lineages across the seven investigated Spartina species. In 4x and 6x mesopolyploids, gene and TE expression changes were consistent with phylogenetic relationships and divergence, revealing weak expression differences in the tetraploid sister species Spartina bakeri and Spartina versicolor (<2 my divergence time) compared to marked transcriptome divergence between the hexaploids S. alterniflora and S. maritima that diverged 2–4 mya. Differentially expressed genes were involved in glycolysis, post-transcriptional protein modifications, epidermis development, biosynthesis of carotenoids. Most detected TE lineages (except SINE elements) were found more expressed in hexaploids than in tetraploids, in line with their abundance in the corresponding genomes. Comparatively, an astonishing (52%) expression repatterning and deviation from parental additivity were observed following recent reticulate evolution (involving the F1 hybrids and the neo-allododecaploid S. anglica), with various patterns of biased homoeologous gene expression, including genes involved in epigenetic regulation. Downregulation of TEs was observed in both hybrids and accentuated in the neo-allopolyploid. Our results reinforce the view that allopolyploidy represents springboards to new regulatory patterns, offering to worldwide invasive species, such as S. anglica, the opportunity to colonize stressful and fluctuating environments on saltmarshes.

scholarly journals Evolved Differences in cis and trans Regulation Between the Maternal and Zygotic mRNA Complements in the Drosophila Embryo

Genetics ◽  
2020 ◽  
Vol 216 (3) ◽  
pp. 805-821
Author(s):  
Emily L. Cartwright ◽  
Susan E. Lott
Keyword(s):  
Gene Expression ◽  
Developmental Stages ◽  
Transcript Level ◽  
Drosophila Embryo ◽  
Gene Products ◽  
Regulatory Evolution ◽  
Transcript Levels ◽  
Maternal Transcript ◽  
Zygotic Transcription ◽  
Trans Regulation

How gene expression can evolve depends on the mechanisms driving gene expression. Gene expression is controlled in different ways in different developmental stages; here we ask whether different developmental stages show different patterns of regulatory evolution. To explore the mode of regulatory evolution, we used the early stages of embryonic development controlled by two different genomes, that of the mother and that of the zygote. During embryogenesis in all animals, initial developmental processes are driven entirely by maternally provided gene products deposited into the oocyte. The zygotic genome is activated later, when developmental control is handed off from maternal gene products to the zygote during the maternal-to-zygotic transition. Using hybrid crosses between sister species of Drosophila (D. simulans, D. sechellia, and D. mauritiana) and transcriptomics, we find that the regulation of maternal transcript deposition and zygotic transcription evolve through different mechanisms. We find that patterns of transcript level inheritance in hybrids, relative to parental species, differ between maternal and zygotic transcripts, and maternal transcript levels are more likely to be conserved. Changes in transcript levels occur predominantly through differences in trans regulation for maternal genes, while changes in zygotic transcription occur through a combination of both cis and trans regulatory changes. Differences in the underlying regulatory landscape in the mother and the zygote are likely the primary determinants for how maternal and zygotic transcripts evolve.

scholarly journals Gene Regulatory Evolution During Speciation in a Songbird

2015 ◽  
Author(s):  
Christopher N. Balakrishnan ◽  
John H. Davidson
Keyword(s):  
High Rate ◽  
F1 Hybrids ◽  
Rna Seq ◽  
Comprehensive Understanding ◽  
Regulatory Evolution ◽  
Tremendous Progress ◽  
Postzygotic Reproductive Isolation ◽  
Gene Regulatory ◽  
Slow Evolution ◽  
In Cis

Over the last decade tremendous progress has been made towards a comparative understanding of gene regulatory evolution. However, we know little about how gene regulation evolves in birds, and how divergent genomes interact in their hybrids. Because of unique features of birds - female heterogamety, a highly conserved karyotype, and the slow evolution of reproductive incompatibilities - an understanding of regulatory evolution in birds is critical to a comprehensive understanding of regulatory evolution and its implications for speciation. Using a novel complement of analyses of replicated RNA-seq libraries, we demonstrate abundant divergence in gene expression between subspecies of zebra finches Taeniopygia guttata. By comparing parental populations and their F1 hybrids, we also show that gene misexpression is relatively rare, a pattern that may partially explain the slow buildup of postzygotic reproductive isolation observed in birds relative to other taxa. Although we expected that the action of genetic drift on the island-dwelling zebra finch subspecies would be manifested in a high rate of trans regulatory divergence, we found that most divergence was in cis regulation, following a pattern commonly observed in other taxa. Thus our study highlights both unique and shared features of avian regulatory evolution.

scholarly journals Evolved differences in cis and trans regulation between the maternal and zygotic mRNA complements in the Drosophila embryo

2019 ◽  
Author(s):  
Emily L. Cartwright ◽  
Susan E. Lott
Keyword(s):  
Gene Expression ◽  
Developmental Stages ◽  
Transcript Level ◽  
Drosophila Embryo ◽  
Gene Products ◽  
Regulatory Evolution ◽  
Transcript Levels ◽  
Maternal Transcript ◽  
Zygotic Transcription ◽  
Trans Regulation

ABSTRACTHow gene expression can evolve depends on the mechanisms driving gene expression. Gene expression is controlled in different ways in different developmental stages; here we ask whether different developmental stages show different patterns of regulatory evolution. To explore the mode of regulatory evolution, we used the early stages of embryonic development controlled by two different genomes, that of the mother and that of the zygote. During embryogenesis in all animals, initial developmental processes are driven entirely by maternally provided gene products deposited into the oocyte. The zygotic genome is activated later, when developmental control is handed off from maternal gene products to the zygote during the maternal-to-zygotic transition. Using hybrid crosses between sister species of Drosophila (D. simulans, D. sechellia, and D. mauritiana) and transcriptomics, we find that the regulation of maternal transcript deposition and zygotic transcription evolve through different mechanisms. We find that patterns of transcript level inheritance in hybrids, relative to parental species, differ between maternal and zygotic transcripts, and maternal transcript levels are more likely to be conserved. Changes in transcript levels occur predominantly through differences in trans regulation for maternal genes, while changes in zygotic transcription occur through a combination of both cis and trans regulatory changes. Differences in the underlying regulatory landscape in the mother and the zygote are likely the primary determinants for how maternal and zygotic transcripts evolve.

scholarly journals Commuting to Work: Nucleolar Long Non-Coding RNA Control Ribosome Biogenesis from Near and Far

2021 ◽  
Vol 7 (3) ◽  
pp. 42
Author(s):  
Victoria Mamontova ◽  
Barbara Trifault ◽  
Lea Boten ◽  
Kaspar Burger
Keyword(s):  
Gene Expression ◽  
Rna Polymerase Ii ◽  
Ribosome Biogenesis ◽  
Intergenic Spacer ◽  
Cellular Growth ◽  
Rrna Synthesis ◽  
Protein Coding ◽  
Non Coding Rna ◽  
And Function ◽  
In Cis

Gene expression is an essential process for cellular growth, proliferation, and differentiation. The transcription of protein-coding genes and non-coding loci depends on RNA polymerases. Interestingly, numerous loci encode long non-coding (lnc)RNA transcripts that are transcribed by RNA polymerase II (RNAPII) and fine-tune the RNA metabolism. The nucleolus is a prime example of how different lncRNA species concomitantly regulate gene expression by facilitating the production and processing of ribosomal (r)RNA for ribosome biogenesis. Here, we summarise the current findings on how RNAPII influences nucleolar structure and function. We describe how RNAPII-dependent lncRNA can both promote nucleolar integrity and inhibit ribosomal (r)RNA synthesis by modulating the availability of rRNA synthesis factors in trans. Surprisingly, some lncRNA transcripts can directly originate from nucleolar loci and function in cis. The nucleolar intergenic spacer (IGS), for example, encodes nucleolar transcripts that counteract spurious rRNA synthesis in unperturbed cells. In response to DNA damage, RNAPII-dependent lncRNA originates directly at broken ribosomal (r)DNA loci and is processed into small ncRNA, possibly to modulate DNA repair. Thus, lncRNA-mediated regulation of nucleolar biology occurs by several modes of action and is more direct than anticipated, pointing to an intimate crosstalk of RNA metabolic events.

Comprehensive Analysis of Differential Expression Profiles of Long Non-coding RNAs with Associated Co-expression and Competing Endogenous RNA Networks in the Hippocampus of Patients with Alzheimer's Disease

2021 ◽  
Vol 18 ◽  
Author(s):  
Jian-Jun Zhang ◽  
Ze-Xuan-Zhu ◽  
Guang-Min-Xu ◽  
Peng Su ◽  
Qian Lei ◽  
...  
Keyword(s):  
Gene Expression ◽  
Alzheimer’S Disease ◽  
Alzheimer's Disease ◽  
Expression Profiles ◽  
Gene Expression Omnibus ◽  
Competing Endogenous Rna ◽  
Pathogenic Genes ◽  
Non Coding Rna ◽  
Using Data ◽  
Trans Regulation

Background: Alzheimer's disease (AD) is still one of the major threats to human health. Although a satisfactory treatment for AD has not yet been discovered, it is necessary to continue to search for novel approaches to deal with this insidious and debilitating disease. Although numerous studies have shown that long non-coding RNA (lncRNA) occupy a significant role in a variety of diseases, their roles in AD remain unclear. Objectives: Using data analysis to explore the role of lncRNA in the course of AD, to further our understanding of AD, and to look forward to finding a new breakthrough for the treatment of AD. Methods: We downloaded and screened expression data of the hippocampal regions of patients with AD from the Gene Expression Omnibus database. We generated lncRNA-miRNA-mRNA networks based on the competing endogenous RNA (ceRNA) hypothesis, and according to gene expression level, we constructed a coding-noncoding co-expression (CNC) network and then executed cis- and trans-regulation analyses. Results: Through comprehensive and systematic analyses, we found that lncRNAs MALAT1, OIP5-AS1, LINC00657, and lnc-NUMB-1 regulated the expression of the key AD pathogenic genes APP, PSEN1, BACE1; and that these lncRNAs may promote the distribution of β-amyloid (Aβ protein) in the brain through exosomes. In addition, lncRNAs were found to adjust viral transcriptional expression, thereby further supporting viral pathogenesis for AD. Conclusions: The lncRNAs MALAT1, OIP5-AS1, LINC00657, and lnc-NUMB-1 that are present in the hippocampus of AD patients exert an important influence on the development of this disease.

scholarly journals Gene Variations in Cis-Acting Elements between the Taiwan and Prototype Strains of Porcine Epidemic Diarrhea Virus Alter Viral Gene Expression

Genes ◽  
2018 ◽  
Vol 9 (12) ◽  
pp. 591
Author(s):  
Tsung-Lin Tsai ◽  
Chen-Chang Su ◽  
Ching-Chi Hsieh ◽  
Chao-Nan Lin ◽  
Hui-Wen Chang ◽  
...  
Keyword(s):  
Gene Expression ◽  
Porcine Epidemic Diarrhea Virus ◽  
The Body ◽  
Economic Losses ◽  
Viral Gene ◽  
Sequence Motif ◽  
Cis Acting ◽  
Diarrhea Virus ◽  
Porcine Epidemic Diarrhea ◽  
In Cis

In 2013, the outbreak of porcine epidemic diarrhea (PED) in Taiwan caused serious economic losses. In this study, we examined whether the variations of the cis-acting elements between the porcine epidemic diarrhea virus (PEDV) Taiwan (TW) strain and the prototype strain CV777 alter gene expression. For this aim, we analyzed the variations of the cis-acting elements in the 5’ and 3’ untranslated regions (UTRs) between the PEDV TW, CV777, and other reference strains. We also determined the previously unidentified transcription regulatory sequence (TRS), a sequence motif required for coronavirus transcription, and found that a nucleotide deletion in the TW strain, in comparison with CV777 strain, immediately downstream of the leader core sequence alters the identity between the leader TRS and the body TRS. Functional analyses using coronavirus defective interfering (DI) RNA revealed that such variations in cis-acting elements for the TW strain compared with the CV777 strain have an influence on the efficiency of gene expression. The current data show for the first time the evolution of PEDV in terms of cis-acting elements and their effects on gene expression, and thus may contribute to our understanding of recent PED outbreaks worldwide.

scholarly journals Ecological divergence in sympatry causes gene misregulation in hybrids

2019 ◽  
Author(s):  
Joseph A. McGirr ◽  
Christopher H. Martin
Keyword(s):  
Gene Expression ◽  
Reproductive Isolation ◽  
Differentially Expressed ◽  
F1 Hybrids ◽  
Adaptive Divergence ◽  
Lower Hybrid ◽  
Hybrid Fitness ◽  
Hybrid Gene ◽  
San Salvador ◽  
Ecological Selection

AbstractEcological speciation occurs when reproductive isolation evolves as a byproduct of adaptive divergence between populations. However, it is unknown whether divergent ecological selection on gene regulation can directly cause reproductive isolation. Selection favoring regulatory divergence between species could result in gene misregulation in F1 hybrids and ultimately lower hybrid fitness. We combined 58 resequenced genomes with 124 transcriptomes to test this hypothesis in a young, sympatric radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas, which consists of a dietary generalist and two novel trophic specialists – a molluscivore and a scale-eater. We found more differential gene expression between closely related sympatric specialists than between allopatric generalist populations separated by 1000 km. Intriguingly, 9.6% of genes that were differentially expressed between sympatric species were also misregulated in their F1 hybrids. Consistent with divergent ecological selection causing misregulation, a subset of these genes were in highly differentiated genomic regions and enriched for functions important for trophic specialization, including head, muscle, and brain development. These regions also included genes that showed evidence of hard selective sweeps and were significantly associated with oral jaw length – the most rapidly diversifying skeletal trait in this radiation. Our results indicate that divergent ecological selection in sympatry can cause hybrid gene misregulation which may act as a primary reproductive barrier between nascent species.SignificanceIt is unknown whether the same genes that regulate ecological traits can simultaneously contribute to reproductive barriers between species. We measured gene expression in two trophic specialist species of Cyprinodon pupfishes that rapidly diverged from a generalist ancestor. We found genes differentially expressed between species that also showed extreme expression levels in their hybrid offspring. Many of these genes showed signs of selection and have putative effects on the development of traits that are important for ecological specialization. This suggests that genetic variants contributing to adaptive trait divergence between parental species negatively interact to cause hybrid gene misregulation, potentially producing unfit hybrids. Such loci may be important barriers to gene flow during the early stages of speciation, even in sympatry.

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