Dosage Compensation and Gene Expression of the X Chromosome in Sheep

Ohno’s hypothesis predicts that the expression of the single X chromosome in males needs compensatory upregulation to balance its dosage with that of the diploid autosomes. Additionally, X chromosome inactivation ensures that quadruple expression of the two X chromosomes is avoided in females. These...

Full description

Bibliographic Details
Main Authors: Jingyue (Ellie) Duan, Kaleigh Flock, Nathanial Jue, Mingyuan Zhang, Amanda Jones, Sahar Al Seesi, Ion Mandoiu, Sambhu Pillai, Maria Hoffman, Rachel O’Neill, Steven Zinn, Kristen Govoni, Sarah Reed, Hesheng Jiang, Zongliang (Carl) Jiang, Xiuchun (Cindy) Tian
Format: Article
Language:English
Published: Oxford University Press 2019-01-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.118.200815
_version_ 1818657345298759680
author Jingyue (Ellie) Duan
Kaleigh Flock
Nathanial Jue
Mingyuan Zhang
Amanda Jones
Sahar Al Seesi
Ion Mandoiu
Sambhu Pillai
Maria Hoffman
Rachel O’Neill
Steven Zinn
Kristen Govoni
Sarah Reed
Hesheng Jiang
Zongliang (Carl) Jiang
Xiuchun (Cindy) Tian
author_facet Jingyue (Ellie) Duan
Kaleigh Flock
Nathanial Jue
Mingyuan Zhang
Amanda Jones
Sahar Al Seesi
Ion Mandoiu
Sambhu Pillai
Maria Hoffman
Rachel O’Neill
Steven Zinn
Kristen Govoni
Sarah Reed
Hesheng Jiang
Zongliang (Carl) Jiang
Xiuchun (Cindy) Tian
author_sort Jingyue (Ellie) Duan
collection DOAJ
description Ohno’s hypothesis predicts that the expression of the single X chromosome in males needs compensatory upregulation to balance its dosage with that of the diploid autosomes. Additionally, X chromosome inactivation ensures that quadruple expression of the two X chromosomes is avoided in females. These mechanisms have been actively studied in mice and humans but lag behind in domestic species. Using RNA sequencing data, we analyzed the X chromosome upregulation in sheep fetal tissues from day 135 of gestation under control, over or restricted maternal diets (100%, 140% and 60% of National Research Council Total Digestible Nutrients), and in conceptuses, juvenile, and adult somatic tissues. By computing the mean expression ratio of all X-linked genes to all autosomal genes (X:A), we found that all samples displayed some levels of X chromosome upregulation. The degrees of X upregulation were not significant (P-value = 0.74) between ovine females and males in the same somatic tissues. Brain, however, displayed complete X upregulation. Interestingly, the male and female reproduction-related tissues exhibited divergent X dosage upregulation. Moreover, expression upregulation of the X chromosome in fetal tissues was not affected by maternal diets. Maternal nutrition, however, did change expression levels of several X-linked genes, such as sex determination genes SOX3 and NR0B1. In summary, our results showed that X chromosome upregulation occurred in nearly all sheep somatic tissues analyzed, thus support Ohno’s hypothesis in a new species. However, the levels of upregulation differed by different subgroups of genes such as those that are house-keeping and “dosage-sensitive”.
first_indexed 2024-12-17T03:40:00Z
format Article
id doaj.art-864b5ffcf0614b31a7f65df7c0eed917
institution Directory Open Access Journal
issn 2160-1836
language English
last_indexed 2024-12-17T03:40:00Z
publishDate 2019-01-01
publisher Oxford University Press
record_format Article
series G3: Genes, Genomes, Genetics
spelling doaj.art-864b5ffcf0614b31a7f65df7c0eed9172022-12-21T22:05:02ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362019-01-019130531410.1534/g3.118.20081528Dosage Compensation and Gene Expression of the X Chromosome in SheepJingyue (Ellie) DuanKaleigh FlockNathanial JueMingyuan ZhangAmanda JonesSahar Al SeesiIon MandoiuSambhu PillaiMaria HoffmanRachel O’NeillSteven ZinnKristen GovoniSarah ReedHesheng JiangZongliang (Carl) JiangXiuchun (Cindy) TianOhno’s hypothesis predicts that the expression of the single X chromosome in males needs compensatory upregulation to balance its dosage with that of the diploid autosomes. Additionally, X chromosome inactivation ensures that quadruple expression of the two X chromosomes is avoided in females. These mechanisms have been actively studied in mice and humans but lag behind in domestic species. Using RNA sequencing data, we analyzed the X chromosome upregulation in sheep fetal tissues from day 135 of gestation under control, over or restricted maternal diets (100%, 140% and 60% of National Research Council Total Digestible Nutrients), and in conceptuses, juvenile, and adult somatic tissues. By computing the mean expression ratio of all X-linked genes to all autosomal genes (X:A), we found that all samples displayed some levels of X chromosome upregulation. The degrees of X upregulation were not significant (P-value = 0.74) between ovine females and males in the same somatic tissues. Brain, however, displayed complete X upregulation. Interestingly, the male and female reproduction-related tissues exhibited divergent X dosage upregulation. Moreover, expression upregulation of the X chromosome in fetal tissues was not affected by maternal diets. Maternal nutrition, however, did change expression levels of several X-linked genes, such as sex determination genes SOX3 and NR0B1. In summary, our results showed that X chromosome upregulation occurred in nearly all sheep somatic tissues analyzed, thus support Ohno’s hypothesis in a new species. However, the levels of upregulation differed by different subgroups of genes such as those that are house-keeping and “dosage-sensitive”.http://g3journal.org/lookup/doi/10.1534/g3.118.200815Ohno’s hypothesisX chromosome upregulationMaternal nutritionOvine
spellingShingle Jingyue (Ellie) Duan
Kaleigh Flock
Nathanial Jue
Mingyuan Zhang
Amanda Jones
Sahar Al Seesi
Ion Mandoiu
Sambhu Pillai
Maria Hoffman
Rachel O’Neill
Steven Zinn
Kristen Govoni
Sarah Reed
Hesheng Jiang
Zongliang (Carl) Jiang
Xiuchun (Cindy) Tian
Dosage Compensation and Gene Expression of the X Chromosome in Sheep
G3: Genes, Genomes, Genetics
Ohno’s hypothesis
X chromosome upregulation
Maternal nutrition
Ovine
title Dosage Compensation and Gene Expression of the X Chromosome in Sheep
title_full Dosage Compensation and Gene Expression of the X Chromosome in Sheep
title_fullStr Dosage Compensation and Gene Expression of the X Chromosome in Sheep
title_full_unstemmed Dosage Compensation and Gene Expression of the X Chromosome in Sheep
title_short Dosage Compensation and Gene Expression of the X Chromosome in Sheep
title_sort dosage compensation and gene expression of the x chromosome in sheep
topic Ohno’s hypothesis
X chromosome upregulation
Maternal nutrition
Ovine
url http://g3journal.org/lookup/doi/10.1534/g3.118.200815
work_keys_str_mv AT jingyueellieduan dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT kaleighflock dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT nathanialjue dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT mingyuanzhang dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT amandajones dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT saharalseesi dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT ionmandoiu dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT sambhupillai dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT mariahoffman dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT racheloneill dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT stevenzinn dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT kristengovoni dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT sarahreed dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT heshengjiang dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT zongliangcarljiang dosagecompensationandgeneexpressionofthexchromosomeinsheep
AT xiuchuncindytian dosagecompensationandgeneexpressionofthexchromosomeinsheep