scholarly journals Landscape and evolution of cis- and trans-regulation in chicken genome between two contrasted breeds analyzed in three tissues at one day of age

2019 ◽  
Author(s):  
Qiong Wang ◽  
Yaxiong Jia ◽  
Yuan Wang ◽  
Zhihua Jiang ◽  
Xiang Zhou ◽  
...  

Abstract Background Gene expression variation is an important mechanism underlying phenotypic variation, and can occur via cis- and trans-regulation. In order to understand the role of cis- and trans-regulatory variation on population divergence of chicken, we developed reciprocal crosses of two chicken breeds, White Leghorn and Cornish Game, with major differences in size and reproductive traits, and used them to identify the degree of cis versus trans variation in brain, liver and muscle of both male and female samples at 1-day age. Results We provided a landscape about how the transcriptomes are regulated between two contrasted breeds by allele specific expression analysis. Our results showed that compared with the cis-regulated genes, trans-acted genes existed more extensively in the chicken genome. Furthermore, a widespread compensatory tendency exists in chicken genome. Most importantly, we found the evidence of stronger purifying selection for trans-regulatory variation than the cis-elements. Conclusions Our research performed the first study to describe the transcriptome regulation between White Leghorn and Cornish Game breeds and suggests that artificial selection associated with domestication in chicken may have more often acted on trans-regulatory variation.

2019 ◽  
Author(s):  
Qiong Wang ◽  
Yaxiong Jia ◽  
Yuan Wang ◽  
Zhihua Jiang ◽  
Xiang Zhou ◽  
...  

Abstract Background: Gene expression variation is an important mechanism underlying phenotypic variation, and can occur via cis- and trans-regulation. In order to understand the role of cis- and trans-regulatory variation on population divergence of chicken, we developed reciprocal crosses of two chicken breeds, White Leghorn and Cornish Game, with major differences in body size and reproductive traits, and used them to identify the degree of cis versus trans variation in brain, liver and muscle of both male and female samples at 1 day age. Results: We provided a landscape about how the transcriptomes are regulated in the hybrid progenies of two contrasted breeds by allele specific expression analysis. Our results showed that compared with the cis-regulatory divergence, trans-acted genes existed more extensively in the chicken genome. Furthermore, a widespread tendency of compensatory regulation exists in chicken genome. Most importantly, we found the evidence of stronger purifying selection on genes regulated by trans variations than the cis elements. Conclusions: We demonstrated a pipeline to explore the allele-specific expression in the hybrid progenies of inbred lines without specific reference genome. Our research performed the first study to describe the regulatory divergence between two contrasted breeds. The results suggested that artificial selection associated with domestication in chicken may have more often acted on trans-regulatory divergence than cis.


BMC Genomics ◽  
2019 ◽  
Vol 20 (1) ◽  
Author(s):  
Qiong Wang ◽  
Yaxiong Jia ◽  
Yuan Wang ◽  
Zhihua Jiang ◽  
Xiang Zhou ◽  
...  

Abstract Background Gene expression variation is a key underlying factor influencing phenotypic variation, and can occur via cis- or trans-regulation. To understand the role of cis- and trans-regulatory variation on population divergence in chicken, we developed reciprocal crosses of two chicken breeds, White Leghorn and Cornish Game, which exhibit major differences in body size and reproductive traits, and used them to determine the degree of cis versus trans variation in the brain, liver, and muscle tissue of male and female 1-day-old specimens. Results We provided an overview of how transcriptomes are regulated in hybrid progenies of two contrasting breeds based on allele specific expression analysis. Compared with cis-regulatory divergence, trans-acting genes were more extensive in the chicken genome. In addition, considerable compensatory cis- and trans-regulatory changes exist in the chicken genome. Most importantly, stronger purifying selection was observed on genes regulated by trans-variations than in genes regulated by the cis elements. Conclusions We present a pipeline to explore allele-specific expression in hybrid progenies of inbred lines without a specific reference genome. Our research is the first study to describe the regulatory divergence between two contrasting breeds. The results suggest that artificial selection associated with domestication in chicken could have acted more on trans-regulatory divergence than on cis-regulatory divergence.


2019 ◽  
Author(s):  
Qiong Wang ◽  
Yaxiong Jia ◽  
Yuan Wang ◽  
Zhihua Jiang ◽  
Xiang Zhou ◽  
...  

Abstract Background: Gene expression variation is a key underlying factor influencing phenotypic variation, and can occur via cis- or trans-regulation. To understand the role of cis- and trans-regulatory variation on population divergence in chicken, we developed reciprocal crosses of two chicken breeds, White Leghorn and Cornish Game, which exhibit major differences in body size and reproductive traits, and used them to determine the degree of cis versus trans variation in the brain, liver, and muscle tissue of male and female 1-day-old specimens.Results: We provided an overview of how transcriptomes are regulated in hybrid progenies of two contrasting breeds based on allele specific expression analysis. Compared with cis-regulatory divergence, trans-acting genes were more extensive in the chicken genome. In addition, considerable compensatory cis- and trans-regulatory changes exist in the chicken genome. Most importantly, stronger purifying selection was observed on genes regulated by trans-variations than in genes regulated by the cis elements.Conclusions: We present a pipeline to explore allele-specific expression in hybrid progenies of inbred lines without a specific reference genome. Our research is the first study to describe the regulatory divergence between two contrasting breeds. The results suggest that artificial selection associated with domestication in chicken could have acted more on trans-regulatory divergence than on cis-regulatory divergence.


2019 ◽  
Author(s):  
Qiong Wang ◽  
Yaxiong Jia ◽  
Yuan Wang ◽  
Zhihua Jiang ◽  
Xiang Zhou ◽  
...  

Abstract Background: Gene expression variation is a key underlying factor influencing phenotypic variation, and can occur via cis- or trans-regulation. To understand the role of cis- and trans-regulatory variation on population divergence in chicken, we developed reciprocal crosses of two chicken breeds, White Leghorn and Cornish Game, which exhibit major differences in body size and reproductive traits, and used them to determine the degree of cis versus trans variation in the brain, liver, and muscle tissue of male and female 1-day-old specimens.Results: We provided an overview of how transcriptomes are regulated in hybrid progenies of two contrasting breeds based on allele specific expression analysis. Compared with cis-regulatory divergence, trans-acting genes were more extensive in the chicken genome. In addition, considerable compensatory cis- and trans-regulatory changes exist in the chicken genome. Most importantly, stronger purifying selection was observed on genes regulated by trans-variations than in genes regulated by the cis elements.Conclusions: We present a pipeline to explore allele-specific expression in hybrid progenies of inbred lines without a specific reference genome. Our research is the first study to describe the regulatory divergence between two contrasting breeds. The results suggest that artificial selection associated with domestication in chicken could have acted more on trans-regulatory divergence than on cis-regulatory divergence.


2015 ◽  
Author(s):  
Kim A. Steige ◽  
Benjamin Laenen ◽  
Johan Reimegård ◽  
Douglas Scofield ◽  
Tanja Slotte

Understanding the causes of cis-regulatory variation is a long-standing aim in evolutionary biology. Although cis-regulatory variation has long been considered important for adaptation, we still have a limited understanding of the selective importance and genomic determinants of standing cis-regulatory variation. To address these questions, we studied the prevalence, genomic determinants and selective forces shaping cis-regulatory variation in the outcrossing plant Capsella grandiflora. We first identified a set of 1,010 genes with common cis-regulatory variation using analyses of allele-specific expression (ASE). Population genomic analyses of whole-genome sequences from 32 individuals showed that genes with common cis-regulatory variation are 1) under weaker purifying selection and 2) undergo less frequent positive selection than other genes. We further identified genomic determinants of cis-regulatory variation. Gene-body methylation (gbM) was a major factor constraining cis-regulatory variation, whereas presence of nearby TEs and tissue specificity of expression increased the odds of ASE. Our results suggest that most common cis-regulatory variation in C. grandiflora is under weak purifying selection, and that gene-specific functional constraints are more important for the maintenance of cis-regulatory variation than genome-scale variation in the intensity of selection. Our results agree with previous findings that suggest TE silencing affects nearby gene expression, and provide novel evidence for a link between gbM and cis-regulatory constraint, possibly reflecting greater dosage-sensitivity of body-methylated genes. Given the extensive conservation of gene-body methylation in flowering plants, this suggests that gene-body methylation could be an important predictor of cis-regulatory variation in a wide range of plant species.


2017 ◽  
Vol 114 (5) ◽  
pp. 1087-1092 ◽  
Author(s):  
Kim A. Steige ◽  
Benjamin Laenen ◽  
Johan Reimegård ◽  
Douglas G. Scofield ◽  
Tanja Slotte

Understanding the causes ofcis-regulatory variation is a long-standing aim in evolutionary biology. Althoughcis-regulatory variation has long been considered important for adaptation, we still have a limited understanding of the selective importance and genomic determinants of standingcis-regulatory variation. To address these questions, we studied the prevalence, genomic determinants, and selective forces shapingcis-regulatory variation in the outcrossing plantCapsella grandiflora. We first identified a set of 1,010 genes with commoncis-regulatory variation using analyses of allele-specific expression (ASE). Population genomic analyses of whole-genome sequences from 32 individuals showed that genes with commoncis-regulatory variation (i) are under weaker purifying selection and (ii) undergo less frequent positive selection than other genes. We further identified genomic determinants ofcis-regulatory variation. Gene body methylation (gbM) was a major factor constrainingcis-regulatory variation, whereas presence of nearby transposable elements (TEs) and tissue specificity of expression increased the odds of ASE. Our results suggest that most commoncis-regulatory variation inC. grandiflorais under weak purifying selection, and that gene-specific functional constraints are more important for the maintenance ofcis-regulatory variation than genome-scale variation in the intensity of selection. Our results agree with previous findings that suggest TE silencing affects nearby gene expression, and provide evidence for a link between gbM andcis-regulatory constraint, possibly reflecting greater dosage sensitivity of body-methylated genes. Given the extensive conservation of gbM in flowering plants, this suggests that gbM could be an important predictor ofcis-regulatory variation in a wide range of plant species.


Genes ◽  
2019 ◽  
Vol 10 (3) ◽  
pp. 225 ◽  
Author(s):  
Katya Mack ◽  
Megan Phifer-Rixey ◽  
Bettina Harr ◽  
Michael Nachman

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.


2020 ◽  
Author(s):  
Brecca Miller ◽  
Alison Morse ◽  
Jacqueline E. Borgert ◽  
Zihao Liu ◽  
Kelsey Sinclair ◽  
...  

ABSTRACTAllelic imbalance (AI) occurs when alleles in a diploid individual are differentially expressed and indicates cis acting regulatory variation. What is the distribution of allelic effects in a natural population? Are all alleles the same? Are all alleles distinct? Tests of allelic effect are performed by crossing individuals and comparing expression between alleles directly in the F1. However, a crossing scheme that compares alleles pairwise is a prohibitive cost for more than a handful of alleles as the number of crosses is at least (n2-n)/2 where n is the number of alleles. We show here that a testcross design followed by a hypothesis test of AI between testcrosses can be used to infer differences between non-tester alleles, allowing n alleles to be compared with n crosses. Using a mouse dataset where both testcrosses and direct comparisons have been performed, we show that ∼75% of the predicted differences between non-tester alleles are validated in a background of ∼10% differences in AI. The testing for AI involves several complex bioinformatics steps. BASE is a complete bioinformatics pipeline that incorporates state-of-the-art error reduction techniques and a flexible Bayesian approach to estimating AI and formally comparing levels of AI between conditions. The modular structure of BASE has been packaged in Galaxy, made available in Nextflow and sbatch. (https://github.com/McIntyre-Lab/BASE_2020). In the mouse data, the direct test identifies more cis effects than the testcross. Cis-by-trans interactions with trans-acting factors on the X contributing to observed cis effects in autosomal genes in the direct cross remains a possible explanation for the discrepancy.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3737 ◽  
Author(s):  
M. Rocío Aguilar-Rangel ◽  
Ricardo A. Chávez Montes ◽  
Eric González-Segovia ◽  
Jeffrey Ross-Ibarra ◽  
June K. Simpson ◽  
...  

BackgroundGene regulatory variation has been proposed to play an important role in the adaptation of plants to environmental stress. In the central highlands of Mexico, farmer selection has generated a unique group of maize landraces adapted to the challenges of the highland niche. In this study, gene expression in Mexican highland maize and a reference maize breeding line were compared to identify evidence of regulatory variation in stress-related genes. It was hypothesised that local adaptation in Mexican highland maize would be associated with a transcriptional signature observable even under benign conditions.MethodsAllele specific expression analysis was performed using the seedling-leaf transcriptome of an F1individual generated from the cross between the highland adapted Mexican landrace Palomero Toluqueño and the reference line B73, grown under benign conditions. Results were compared with a published dataset describing the transcriptional response of B73 seedlings to cold, heat, salt and UV treatments.ResultsA total of 2,386 genes were identified to show allele specific expression. Of these, 277 showed an expression difference between Palomero Toluqueño and B73 alleles under benign conditions that anticipated the response of B73 cold, heat, salt and/or UV treatments, and, as such, were considered to display a prior stress response. Prior stress response candidates included genes associated with plant hormone signaling and a number of transcription factors. Construction of a gene co-expression network revealed further signaling and stress-related genes to be among the potential targets of the transcription factors candidates.DiscussionPrior activation of responses may represent the best strategy when stresses are severe but predictable. Expression differences observed here between Palomero Toluqueño and B73 alleles indicate the presence ofcis-acting regulatory variation linked to stress-related genes in Palomero Toluqueño. Considered alongside gene annotation and population data, allele specific expression analysis of plants grown under benign conditions provides an attractive strategy to identify functional variation potentially linked to local adaptation.


2017 ◽  
Author(s):  
Peter A. Combs ◽  
Hunter B. Fraser

AbstractSpatial patterning of gene expression is a key process in development—responsible for the incredible diversity of animal body plans—yet how it evolves is still poorly understood. Both cis- and trans-acting changes could accumulate and participate in complex interactions, so to isolate the cis-regulatory component of patterning evolution, we measured allele-specific spatial gene expression patterns inD. melanogaster×D. simulanshybrid embryos. RNA-seq of cryosectioned slices revealed 55 genes with strong spatially varying allele-specific expression, and several hundred more with weaker but significant spatial divergence. For example, we found thathunchback (hb), a major regulator of developmental patterning, had reduced expression specifically in the anterior tip ofD. simulansembryos. Mathematical modeling ofhbcis-regulation suggested that a mutation in a Bicoid binding site was responsible, which we verified using CRISPR-Cas9 genome editing. In sum, even comparing morphologically near-identical species we identified a substantial amount of spatial variation in gene expression, suggesting that development is robust to many such changes, but also that natural selection may have ample raw material for evolving new body plans via cis-regulatory divergence.


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