Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation
Abstract Background The ovary is a central organ in the reproductive system that produces oocytes and synthesizes and secretes steroid hormones. Healthy development and regular cyclical change in the ovary is crucial for regulating reproductive processes. However, the key genes and metabolites that...
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2024-12-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-024-11122-3 |
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| author | Binyun Pan Jin Chai Kaixin Fei Ting Zheng Yanzhi Jiang |
| author_facet | Binyun Pan Jin Chai Kaixin Fei Ting Zheng Yanzhi Jiang |
| author_sort | Binyun Pan |
| collection | DOAJ |
| description | Abstract Background The ovary is a central organ in the reproductive system that produces oocytes and synthesizes and secretes steroid hormones. Healthy development and regular cyclical change in the ovary is crucial for regulating reproductive processes. However, the key genes and metabolites that regulate ovarian development and pregnancy have not been fully elucidated. This study conducted high-throughput RNA sequencing and untargeted metabolite profiling of the ovarian tissues from Chenghua pigs at four stages, including postnatal day 3 (D3), puberty at the age of about 125 days (Pub), sexual maturity at the age of about 365 days (Y1), and 105 days after pregnancy at the age of about 360 days (Pre). Results A total of 9,264 and 1,593 differentially expressed genes (DEGs) were identified during ovarian development and pregnancy. Several key genes involved in ovarian development, including SQLE, HMGCS1, MSMO1, SCARB1, CYP11A1, HSD3B1, HSD17B1, and SERPINE1 were identified. Similarly, LUM, FN1, PLAUR, SELP, SDC1, and VCAN were considered to be associated with pregnancy maintenance. Overexpression of HSD17B1 in granulosa cells significantly upregulated estrogen synthesis-related genes (HSD3B1, CYP11A1, and STAR); meanwhile, overexpression of PLAUR promotes granulosa cell proliferation. Furthermore, 66, 24, 77, and 7 differentially expressed miRNAs (DEMis) were found, leading to the selection of key miRNAs such as ssc-miR-206, ssc-miR-107, ssc-miR-429, ssc-miR-210, and ssc-miR-133a-3p by differential miRNA-targeted mRNA interaction network; meanwhile, ssc-miR-133a-3p was validated to have a targeting relationship with KCNA1 by dual-luciferase reporter systems assay. At the metabolic levels, androstenedione, 17a-hydroxyprogesterone, dehydroepiandrosterone, and progesterone were identified, with their synthesis regulated by these DEGs in the ovarian steroidogenesis pathway. Furthermore, treatment of cells with androstenedione upregulated the expression of HSD3B1, CYP11A1, and STAR. Conclusions This study revealed the dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation, indicating that it may provide new theoretical insights for improving sow fertility. |
| format | Article |
| id | doaj-art-4bed33ef89de4ff382aa3e990524b272 |
| institution | OA Journals |
| issn | 1471-2164 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj-art-4bed33ef89de4ff382aa3e990524b2722025-08-20T01:57:15ZengBMCBMC Genomics1471-21642024-12-0125112210.1186/s12864-024-11122-3Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestationBinyun Pan0Jin Chai1Kaixin Fei2Ting Zheng3Yanzhi Jiang4Department of Zoology, College of Life Science, Sichuan Agricultural UniversityDepartment of Zoology, College of Life Science, Sichuan Agricultural UniversityDepartment of Zoology, College of Life Science, Sichuan Agricultural UniversityDepartment of Zoology, College of Life Science, Sichuan Agricultural UniversityDepartment of Zoology, College of Life Science, Sichuan Agricultural UniversityAbstract Background The ovary is a central organ in the reproductive system that produces oocytes and synthesizes and secretes steroid hormones. Healthy development and regular cyclical change in the ovary is crucial for regulating reproductive processes. However, the key genes and metabolites that regulate ovarian development and pregnancy have not been fully elucidated. This study conducted high-throughput RNA sequencing and untargeted metabolite profiling of the ovarian tissues from Chenghua pigs at four stages, including postnatal day 3 (D3), puberty at the age of about 125 days (Pub), sexual maturity at the age of about 365 days (Y1), and 105 days after pregnancy at the age of about 360 days (Pre). Results A total of 9,264 and 1,593 differentially expressed genes (DEGs) were identified during ovarian development and pregnancy. Several key genes involved in ovarian development, including SQLE, HMGCS1, MSMO1, SCARB1, CYP11A1, HSD3B1, HSD17B1, and SERPINE1 were identified. Similarly, LUM, FN1, PLAUR, SELP, SDC1, and VCAN were considered to be associated with pregnancy maintenance. Overexpression of HSD17B1 in granulosa cells significantly upregulated estrogen synthesis-related genes (HSD3B1, CYP11A1, and STAR); meanwhile, overexpression of PLAUR promotes granulosa cell proliferation. Furthermore, 66, 24, 77, and 7 differentially expressed miRNAs (DEMis) were found, leading to the selection of key miRNAs such as ssc-miR-206, ssc-miR-107, ssc-miR-429, ssc-miR-210, and ssc-miR-133a-3p by differential miRNA-targeted mRNA interaction network; meanwhile, ssc-miR-133a-3p was validated to have a targeting relationship with KCNA1 by dual-luciferase reporter systems assay. At the metabolic levels, androstenedione, 17a-hydroxyprogesterone, dehydroepiandrosterone, and progesterone were identified, with their synthesis regulated by these DEGs in the ovarian steroidogenesis pathway. Furthermore, treatment of cells with androstenedione upregulated the expression of HSD3B1, CYP11A1, and STAR. Conclusions This study revealed the dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation, indicating that it may provide new theoretical insights for improving sow fertility.https://doi.org/10.1186/s12864-024-11122-3PigOvaryDevelopmentGestationMRNAMiRNA |
| spellingShingle | Binyun Pan Jin Chai Kaixin Fei Ting Zheng Yanzhi Jiang Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation BMC Genomics Pig Ovary Development Gestation MRNA MiRNA |
| title | Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation |
| title_full | Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation |
| title_fullStr | Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation |
| title_full_unstemmed | Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation |
| title_short | Dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation |
| title_sort | dynamic changes in the transcriptome and metabolome of pig ovaries across developmental stages and gestation |
| topic | Pig Ovary Development Gestation MRNA MiRNA |
| url | https://doi.org/10.1186/s12864-024-11122-3 |
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