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Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken

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...

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Autores principales: Uebbing, Severin, Konzer, Anne, Xu, Luohao, Backström, Niclas, Brunström, Björn, Bergquist, Jonas, Ellegren, Hans
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4576709/
https://www.ncbi.nlm.nih.gov/pubmed/26108680
http://dx.doi.org/10.1093/molbev/msv147
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author Uebbing, Severin
Konzer, Anne
Xu, Luohao
Backström, Niclas
Brunström, Björn
Bergquist, Jonas
Ellegren, Hans
author_facet Uebbing, Severin
Konzer, Anne
Xu, Luohao
Backström, Niclas
Brunström, Björn
Bergquist, Jonas
Ellegren, Hans
author_sort Uebbing, Severin
collection PubMed
description 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.
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spelling pubmed-45767092015-09-25 Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken Uebbing, Severin Konzer, Anne Xu, Luohao Backström, Niclas Brunström, Björn Bergquist, Jonas Ellegren, Hans Mol Biol Evol Discoveries 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. Oxford University Press 2015-10 2015-06-24 /pmc/articles/PMC4576709/ /pubmed/26108680 http://dx.doi.org/10.1093/molbev/msv147 Text en © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Uebbing, Severin
Konzer, Anne
Xu, Luohao
Backström, Niclas
Brunström, Björn
Bergquist, Jonas
Ellegren, Hans
Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
title Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
title_full Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
title_fullStr Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
title_full_unstemmed Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
title_short Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
title_sort quantitative mass spectrometry reveals partial translational regulation for dosage compensation in chicken
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4576709/
https://www.ncbi.nlm.nih.gov/pubmed/26108680
http://dx.doi.org/10.1093/molbev/msv147
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