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...
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2022-10-01
|
Series: | Animals |
Subjects: | |
Online Access: | https://www.mdpi.com/2076-2615/12/20/2812 |
_version_ | 1797475987886178304 |
---|---|
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. |
first_indexed | 2024-03-09T20:51:30Z |
format | Article |
id | doaj.art-587d127ad39e41d89e54ab4642983847 |
institution | Directory Open Access Journal |
issn | 2076-2615 |
language | English |
last_indexed | 2024-03-09T20:51:30Z |
publishDate | 2022-10-01 |
publisher | MDPI AG |
record_format | Article |
series | Animals |
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 |
work_keys_str_mv | AT wenhaoli highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT weikezeng highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT xiayangjin highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT huimingxu highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT xingyanfang highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT zhijiema highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT gangjiancao highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT ruizheli highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep AT liuyinma highaltitudestressorchestratesmrnaexpressionandalternativesplicingofovarianfollicledevelopmentgenesintibetansheep |