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Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0003-2439-6946
Uppsala University, Disciplinary Domain of Science and Technology, Chemistry, Department of Chemistry - BMC, Analytical Chemistry. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
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2015 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 32, no 10, 2716-2725 p.Article in journal (Refereed) Published
Abstract [en]

There is increasing evidence that dosage compensation is not a ubiquitous feature following sex chromosome evolution, especially not in organisms where females are the heterogametic sex, like in birds. Even when it occurs, compensation can be incomplete and limited to dosage-sensitive genes. However, previous work has mainly studied transcriptional regulation of sex-linked genes, which may not reflect expression at the protein level. Here, we used liquid chromatography–tandem mass spectrometry to detect and quantify expressed levels of more than 2,400 proteins in ten different tissues of male and female chicken embryos. For comparison, transcriptome sequencing was performed in the same individuals, five of each sex. The proteomic analysis revealed that dosage compensation was incomplete, with a mean male-to-female (M:F) expression ratio of Z-linked genes of 1.32 across tissues, similar to that at the RNA level (1.29). The mean Z chromosome-to-autosome expression ratio was close to 1 in males and lower than 1 in females, consistent with partly reduced Z chromosome expression in females. Although our results exclude a general mechanism for chromosome-wide dosage compensation at translation, 30% of all proteins encoded from Z-linked genes showed a significant change in the M:F ratio compared with the corresponding ratio at the RNA level. This resulted in a pattern where some genes showed balanced expression between sexes and some close to 2-fold higher expression in males. This suggests that proteomic analyses will be necessary to reveal a more complete picture of gene regulation and sex chromosome evolution.

Place, publisher, year, edition, pages
2015. Vol. 32, no 10, 2716-2725 p.
Keyword [en]
sex chromosome evolution, dosage compensation, chicken, proteomics, mass spectrometry
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
URN: urn:nbn:se:uu:diva-258796DOI: 10.1093/molbev/msv147ISI: 000361987100019PubMedID: 26108680OAI: oai:DiVA.org:uu-258796DiVA: diva2:842445
Swedish Research Council, 2010-5650, 2013-8271, 2011-4423EU, European Research Council, AdG 249976Knut and Alice Wallenberg Foundation
Available from: 2015-07-20 Created: 2015-07-20 Last updated: 2015-11-10Bibliographically approved
In thesis
1. On the Evolution of the Avian Transcriptome
Open this publication in new window or tab >>On the Evolution of the Avian Transcriptome
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
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.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. 42 p.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1270
evolution, gene expression, regulation, RNA-seq, transcriptomics, proteomics, sex chromosome, dosage compensation, divergence, ASE, birds, Ficedula, flycatcher, chicken
National Category
Biological Sciences Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
urn:nbn:se:uu:diva-259487 (URN)978-91-554-9292-2 (ISBN)
Public defence
2015-09-24, Ekmansalen, Norbyvägen 14, Uppsala, 13:15 (English)
Available from: 2015-09-02 Created: 2015-08-05 Last updated: 2015-10-01

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