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Allele-specific gene expression inferred by a Bayesian negative binomial approach indicates abundant cis-regulatory variation in natural flycatcher populations
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.ORCID-id: 0000-0003-2439-6946
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
(engelsk)Manuskript (preprint) (Annet vitenskapelig)
Abstract [en]

Polymorphisms in cis-regulatory sequences can make the two alleles of a gene be expressed at different levels, providing a starting point for the evolution of divergence in gene expression. However, little is known about the genome-wide abundance of regulatory variation in natural populations. We performed RNA-seq of multiple tissues from population samples of two closely related flycatcher species and developed a Bayesian algorithm that maximises data usage by borrowing overdispersion estimates over the whole dataset and combines several SNPs per transcript to detect allele-specific expression (ASE). Of 2,576 transcripts analysed in collared flycatcher, ASE was detected in 185 (7.2%). A similar frequency was seen in the pied flycatcher but these frequencies are likely to be underestimates for several reasons. The proportion of ASE transcripts varied among tissues, being lowest in testis and highest in muscle. Often, ASE was seen in several tissues for particular gene-individual combinations. This is one of only very few large-scale studies investigating the incidence of ASE in the wild. The results suggest that genetic variation in regulatory sequences commonly affect gene expression in natural populations and that it provides a seedbed for phenotypic evolution via divergence in gene expression.

Emneord [en]
regulatory sequences, gene expression evolution, ASE, RNA-seq
HSV kategori
Forskningsprogram
Biologi med inriktning mot evolutionär genetik
Identifikatorer
URN: urn:nbn:se:uu:diva-258797OAI: oai:DiVA.org:uu-258797DiVA, id: diva2:844360
Tilgjengelig fra: 2015-08-05 Laget: 2015-07-20 Sist oppdatert: 2015-10-01
Inngår i avhandling
1. On the Evolution of the Avian Transcriptome
Åpne denne publikasjonen i ny fane eller vindu >>On the Evolution of the Avian Transcriptome
2015 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
Abstract [en]

Change in gene expression is a powerful tool for evolution, because seemingly small expression changes can contribute important steps towards adaptation without necessarily affecting the whole organism. There is still much to learn about how gene expression evolves on genome- and population-wide levels, especially in non-model organisms. This thesis addresses some important questions in gene expression evolution via the quantitative measurement of RNA and protein levels in birds.

First, I confirmed the state of incomplete dosage compensation in birds by sequencing the transcriptome of collared flycatchers (Ficedula albicollis). I showed that pleiotropy governs the evolution of expression male-bias from the Z chromosome. Sex-linked genes in females were more highly expressed than half the male expression level, indicative of a partial up-regulation. A comparison with data from ostrich (Struthio camelus), a bird with non-degenerated sex chromosomes, showed that sex-linked expression male-bias evolved following sex chromosome degradation.

Second, using a combination of RNA sequencing and proteome mass spectrometry in chicken (Gallus gallus), I asked whether complete dosage compensation was achieved through regulation at translation. I showed that this was not the case and that incomplete dosage compensation extends to the protein level in birds. In addition, sex-linked genes showed more often an increased amount of regulation at translational level than autosomal genes.

Third, I investigated gene expression divergence between collared and pied flycatchers (Ficedula hypoleuca) using RNA sequencing in multiple tissues and individuals. Tissues differed in the degree of expression variance and in the number of divergent genes, which I identified using expression QST. Variance within species was negatively correlated with expression breadth and protein interactivity, indicating that evolutionary constraints act predominantly within interbreeding populations. Among genes unique to one of the species, I identified one gene, DPP7, falling into a large genomic deletion fixed in pied flycatchers.

Fourth, I investigated allele-specific expression (ASE) in the two flycatcher populations. ASE was identified from genetic variants within transcripts using RNA sequencing reads. We developed a Bayesian negative binomial approach that gained statistical power by estimating expression variance from combined SNPs within a transcript and overdispersion from the whole dataset.

sted, utgiver, år, opplag, sider
Uppsala: Acta Universitatis Upsaliensis, 2015. s. 42
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1270
Emneord
evolution, gene expression, regulation, RNA-seq, transcriptomics, proteomics, sex chromosome, dosage compensation, divergence, ASE, birds, Ficedula, flycatcher, chicken
HSV kategori
Forskningsprogram
Biologi med inriktning mot evolutionär genetik
Identifikatorer
urn:nbn:se:uu:diva-259487 (URN)978-91-554-9292-2 (ISBN)
Disputas
2015-09-24, Ekmansalen, Norbyvägen 14, Uppsala, 13:15 (engelsk)
Veileder
Tilgjengelig fra: 2015-09-02 Laget: 2015-08-05 Sist oppdatert: 2015-10-01

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