High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep

High-altitude stress threatens the survival rate of Tibetan sheep and reduces their fertility. However, the molecular basis of this phenomenon remains elusive. Here, we used RNA-seq to elucidate the transcriptome dynamics of high-altitude stress in Tibetan sheep ovaries. In total, 104 genes were cha...

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Main Authors: Wenhao Li, Weike Zeng, Xiayang Jin, Huiming Xu, Xingyan Fang, Zhijie Ma, Gangjian Cao, Ruizhe Li, Liuyin Ma
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/12/20/2812
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author Wenhao Li
Weike Zeng
Xiayang Jin
Huiming Xu
Xingyan Fang
Zhijie Ma
Gangjian Cao
Ruizhe Li
Liuyin Ma
author_facet Wenhao Li
Weike Zeng
Xiayang Jin
Huiming Xu
Xingyan Fang
Zhijie Ma
Gangjian Cao
Ruizhe Li
Liuyin Ma
author_sort Wenhao Li
collection DOAJ
description High-altitude stress threatens the survival rate of Tibetan sheep and reduces their fertility. However, the molecular basis of this phenomenon remains elusive. Here, we used RNA-seq to elucidate the transcriptome dynamics of high-altitude stress in Tibetan sheep ovaries. In total, 104 genes were characterized as high-altitude stress-related differentially expressed genes (DEGs). In addition, 36 DEGs contributed to ovarian follicle development, and 28 of them were downregulated under high-altitude stress. In particular, high-altitude stress significantly suppressed the expression of two ovarian lymphatic system marker genes: <i>LYVE1</i> and <i>ADAMTS-1</i>. Network analysis revealed that luteinizing hormone (LH)/follicle-stimulating hormone (FSH) signaling-related genes, such as <i>EGR1</i>, <i>FKBP5</i>, <i>DUSP1</i>, and <i>FOS</i>, were central regulators in the DEG network, and these genes were also suppressed under high-altitude stress. As a post-transcriptional regulation mechanism, alternative splicing (AS) is ubiquitous in Tibetan sheep. High-altitude stress induced 917 differentially alternative splicing (DAS) events. High-altitude stress modulated DAS in an AS-type-specific manner: suppressing skipped exon events but increasing retained intron events. C<sub>2</sub>H<sub>2</sub>-type zinc finger transcription factors and RNA processing factors were mainly enriched in DAS. These findings revealed high-altitude stress repressed ovarian development by suppressing the gene expression of LH/FSH hormone signaling genes and inducing intron retention of C<sub>2</sub>H<sub>2</sub>-type zinc finger transcription factors.
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spelling doaj.art-587d127ad39e41d89e54ab46429838472023-11-23T22:32:18ZengMDPI AGAnimals2076-26152022-10-011220281210.3390/ani12202812High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan SheepWenhao Li0Weike Zeng1Xiayang Jin2Huiming Xu3Xingyan Fang4Zhijie Ma5Gangjian Cao6Ruizhe Li7Liuyin Ma8Academy of Animal Science and Veterinary Medicine, Qinghai University, Xining 810016, ChinaCollege of Forestry, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaAcademy of Animal Science and Veterinary Medicine, Qinghai University, Xining 810016, ChinaCollege of Forestry, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Forestry, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaAcademy of Animal Science and Veterinary Medicine, Qinghai University, Xining 810016, ChinaCollege of Forestry, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaAcademy of Animal Science and Veterinary Medicine, Qinghai University, Xining 810016, ChinaCollege of Forestry, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaHigh-altitude stress threatens the survival rate of Tibetan sheep and reduces their fertility. However, the molecular basis of this phenomenon remains elusive. Here, we used RNA-seq to elucidate the transcriptome dynamics of high-altitude stress in Tibetan sheep ovaries. In total, 104 genes were characterized as high-altitude stress-related differentially expressed genes (DEGs). In addition, 36 DEGs contributed to ovarian follicle development, and 28 of them were downregulated under high-altitude stress. In particular, high-altitude stress significantly suppressed the expression of two ovarian lymphatic system marker genes: <i>LYVE1</i> and <i>ADAMTS-1</i>. Network analysis revealed that luteinizing hormone (LH)/follicle-stimulating hormone (FSH) signaling-related genes, such as <i>EGR1</i>, <i>FKBP5</i>, <i>DUSP1</i>, and <i>FOS</i>, were central regulators in the DEG network, and these genes were also suppressed under high-altitude stress. As a post-transcriptional regulation mechanism, alternative splicing (AS) is ubiquitous in Tibetan sheep. High-altitude stress induced 917 differentially alternative splicing (DAS) events. High-altitude stress modulated DAS in an AS-type-specific manner: suppressing skipped exon events but increasing retained intron events. C<sub>2</sub>H<sub>2</sub>-type zinc finger transcription factors and RNA processing factors were mainly enriched in DAS. These findings revealed high-altitude stress repressed ovarian development by suppressing the gene expression of LH/FSH hormone signaling genes and inducing intron retention of C<sub>2</sub>H<sub>2</sub>-type zinc finger transcription factors.https://www.mdpi.com/2076-2615/12/20/2812ovary tissuegene expressiontranscription factoralternative splicingfollicular developmenthigh-altitude stress
spellingShingle Wenhao Li
Weike Zeng
Xiayang Jin
Huiming Xu
Xingyan Fang
Zhijie Ma
Gangjian Cao
Ruizhe Li
Liuyin Ma
High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep
Animals
ovary tissue
gene expression
transcription factor
alternative splicing
follicular development
high-altitude stress
title High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep
title_full High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep
title_fullStr High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep
title_full_unstemmed High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep
title_short High-Altitude Stress Orchestrates mRNA Expression and Alternative Splicing of Ovarian Follicle Development Genes in Tibetan Sheep
title_sort high altitude stress orchestrates mrna expression and alternative splicing of ovarian follicle development genes in tibetan sheep
topic ovary tissue
gene expression
transcription factor
alternative splicing
follicular development
high-altitude stress
url https://www.mdpi.com/2076-2615/12/20/2812
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