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Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues

Dosage compensation of the mammalian X chromosome (X) was proposed by Susumu Ohno as a mechanism wherein the inactivation of one X in females would lead to doubling the expression of the other. This would resolve the dosage imbalance between eutherian females (XX) versus male (XY) and between a sing...

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Autores principales: Duan, Jingyue (Ellie), Shi, Wei, Jue, Nathaniel K, Jiang, Zongliang, Kuo, Lynn, O’Neill, Rachel, Wolf, Eckhard, Dong, Hong, Zheng, Xinbao, Chen, Jingbo, Tian, Xiuchun (Cindy)
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354180/
https://www.ncbi.nlm.nih.gov/pubmed/30566637
http://dx.doi.org/10.1093/gbe/evy270
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author Duan, Jingyue (Ellie)
Shi, Wei
Jue, Nathaniel K
Jiang, Zongliang
Kuo, Lynn
O’Neill, Rachel
Wolf, Eckhard
Dong, Hong
Zheng, Xinbao
Chen, Jingbo
Tian, Xiuchun (Cindy)
author_facet Duan, Jingyue (Ellie)
Shi, Wei
Jue, Nathaniel K
Jiang, Zongliang
Kuo, Lynn
O’Neill, Rachel
Wolf, Eckhard
Dong, Hong
Zheng, Xinbao
Chen, Jingbo
Tian, Xiuchun (Cindy)
author_sort Duan, Jingyue (Ellie)
collection PubMed
description Dosage compensation of the mammalian X chromosome (X) was proposed by Susumu Ohno as a mechanism wherein the inactivation of one X in females would lead to doubling the expression of the other. This would resolve the dosage imbalance between eutherian females (XX) versus male (XY) and between a single active X versus autosome pairs (A). Expression ratio of X- and A-linked genes has been relatively well studied in humans and mice, despite controversial results over the existence of upregulation of X-linked genes. Here we report the first comprehensive test of Ohno’s hypothesis in bovine preattachment embryos, germline, and somatic tissues. Overall an incomplete dosage compensation (0.5 < X:A < 1) of expressed genes and an excess X dosage compensation (X:A > 1) of ubiquitously expressed “dosage-sensitive” genes were seen. No significant differences in X:A ratios were observed between bovine female and male somatic tissues, further supporting Ohno’s hypothesis. Interestingly, preimplantation embryos manifested a unique pattern of X dosage compensation dynamics. Specifically, X dosage decreased after fertilization, indicating that the sperm brings in an inactive X to the matured oocyte. Subsequently, the activation of the bovine embryonic genome enhanced expression of X-linked genes and increased the X dosage. As a result, an excess compensation was exhibited from the 8-cell stage to the compact morula stage. The X dosage peaked at the 16-cell stage and stabilized after the blastocyst stage. Together, our findings confirm Ohno’s hypothesis of X dosage compensation in the bovine and extend it by showing incomplete and over-compensation for expressed and “dosage-sensitive” genes, respectively.
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spelling pubmed-63541802019-02-08 Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues Duan, Jingyue (Ellie) Shi, Wei Jue, Nathaniel K Jiang, Zongliang Kuo, Lynn O’Neill, Rachel Wolf, Eckhard Dong, Hong Zheng, Xinbao Chen, Jingbo Tian, Xiuchun (Cindy) Genome Biol Evol Original Article Dosage compensation of the mammalian X chromosome (X) was proposed by Susumu Ohno as a mechanism wherein the inactivation of one X in females would lead to doubling the expression of the other. This would resolve the dosage imbalance between eutherian females (XX) versus male (XY) and between a single active X versus autosome pairs (A). Expression ratio of X- and A-linked genes has been relatively well studied in humans and mice, despite controversial results over the existence of upregulation of X-linked genes. Here we report the first comprehensive test of Ohno’s hypothesis in bovine preattachment embryos, germline, and somatic tissues. Overall an incomplete dosage compensation (0.5 < X:A < 1) of expressed genes and an excess X dosage compensation (X:A > 1) of ubiquitously expressed “dosage-sensitive” genes were seen. No significant differences in X:A ratios were observed between bovine female and male somatic tissues, further supporting Ohno’s hypothesis. Interestingly, preimplantation embryos manifested a unique pattern of X dosage compensation dynamics. Specifically, X dosage decreased after fertilization, indicating that the sperm brings in an inactive X to the matured oocyte. Subsequently, the activation of the bovine embryonic genome enhanced expression of X-linked genes and increased the X dosage. As a result, an excess compensation was exhibited from the 8-cell stage to the compact morula stage. The X dosage peaked at the 16-cell stage and stabilized after the blastocyst stage. Together, our findings confirm Ohno’s hypothesis of X dosage compensation in the bovine and extend it by showing incomplete and over-compensation for expressed and “dosage-sensitive” genes, respectively. Oxford University Press 2018-12-19 /pmc/articles/PMC6354180/ /pubmed/30566637 http://dx.doi.org/10.1093/gbe/evy270 Text en © The Author(s) 2018. 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 Original Article
Duan, Jingyue (Ellie)
Shi, Wei
Jue, Nathaniel K
Jiang, Zongliang
Kuo, Lynn
O’Neill, Rachel
Wolf, Eckhard
Dong, Hong
Zheng, Xinbao
Chen, Jingbo
Tian, Xiuchun (Cindy)
Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues
title Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues
title_full Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues
title_fullStr Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues
title_full_unstemmed Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues
title_short Dosage Compensation of the X Chromosomes in Bovine Germline, Early Embryos, and Somatic Tissues
title_sort dosage compensation of the x chromosomes in bovine germline, early embryos, and somatic tissues
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354180/
https://www.ncbi.nlm.nih.gov/pubmed/30566637
http://dx.doi.org/10.1093/gbe/evy270
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