MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)

Zona Pellucida (Zp) proteins are intimately associated with the living environment and reproductive styles in fish. Environmental salinity has a pronounced effect on reproduction in the spotted scat (Scatophagus argus). However, the precise function of Zps in reproduction and their expression regula...

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Main Authors: Zhuoying Leng, Xinghua Lin, Yi Zhai, Hongjuan Shi, Dongneng Jiang, Mouyan Jiang, Huapu Chen, Tianli Wu, Siping Deng
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Aquaculture Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352513425000390
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author Zhuoying Leng
Xinghua Lin
Yi Zhai
Hongjuan Shi
Dongneng Jiang
Mouyan Jiang
Huapu Chen
Tianli Wu
Siping Deng
author_facet Zhuoying Leng
Xinghua Lin
Yi Zhai
Hongjuan Shi
Dongneng Jiang
Mouyan Jiang
Huapu Chen
Tianli Wu
Siping Deng
author_sort Zhuoying Leng
collection DOAJ
description Zona Pellucida (Zp) proteins are intimately associated with the living environment and reproductive styles in fish. Environmental salinity has a pronounced effect on reproduction in the spotted scat (Scatophagus argus). However, the precise function of Zps in reproduction and their expression regulation during salinity stress remain unclear. Therefore, the ovarian miRNA sequence (miRNA-seq) and RNA sequence (RNA-seq) of spotted scat were analyzed after 20 days of treatment period at salinities of 5 ppt (low salinity group, LS), 25 ppt (control group, Ctrl), and 35 ppt (high salinity group, HS). The RNA-seq analysis revealed that 41 DEGs associated with reproduction, including zp2, zp3, wt1b, erα, pgr, and others, exhibited significant differences in the Ctrl vs. HS or Ctrl vs. LS comparisons. The Ctrl vs. LS and Ctrl vs. HS comparisons yielded 193 and 258 DEMs, respectively, according to miRNA-seq analysis. The visualized target relationships showed that zp2 and zp3, formed 12 target pairs with 11 different DEMs. Five miRNA-target gene pairs, miR-9-x/zp2, miR-9-z/zp2, miR-3154-y/zp2, miR-3533-y/zp3, and miR-365-y/zp3, were predicted at the sequence level after salinity stress. The result of qRT-PCR demonstrated that both zp2 and zp3 exhibited the highest expression levels in the ovary. The expression levels of zp2, zp3, miR-9-z, miR-3154-y, and miR-3533-y were higher in phase Ⅴ than in other phases of ovarian development. The expression levels of zp2, zp3, and miR-3154-y increased significantly, while the expression levels of miR-9-z and miR-3533-y remained unchanged after 17β-estradiol (E2) injection. The dual-luciferase reporter assay, together with the changes observed in zp2, zp3, miR-9-z, miR-3154-y, and miR-3533-y after low and high salt treatment, demonstrated that zp2 expression was regulated by miR-9-z and miR-3154-y, while zp3 was regulated by miR-3533-y. These results suggest that miR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 are involved in ovarian development and adaptation to salinity stress in spotted scat.
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spelling doaj-art-6026bc4d53e54a81a412f4807a7d41f22025-02-06T05:12:26ZengElsevierAquaculture Reports2352-51342025-03-0140102653MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)Zhuoying Leng0Xinghua Lin1Yi Zhai2Hongjuan Shi3Dongneng Jiang4Mouyan Jiang5Huapu Chen6Tianli Wu7Siping Deng8Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, ChinaFisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, China; Corresponding authors at: Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China.Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Zhanjiang 524088, China; Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, 524088, China; Corresponding authors at: Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China.Zona Pellucida (Zp) proteins are intimately associated with the living environment and reproductive styles in fish. Environmental salinity has a pronounced effect on reproduction in the spotted scat (Scatophagus argus). However, the precise function of Zps in reproduction and their expression regulation during salinity stress remain unclear. Therefore, the ovarian miRNA sequence (miRNA-seq) and RNA sequence (RNA-seq) of spotted scat were analyzed after 20 days of treatment period at salinities of 5 ppt (low salinity group, LS), 25 ppt (control group, Ctrl), and 35 ppt (high salinity group, HS). The RNA-seq analysis revealed that 41 DEGs associated with reproduction, including zp2, zp3, wt1b, erα, pgr, and others, exhibited significant differences in the Ctrl vs. HS or Ctrl vs. LS comparisons. The Ctrl vs. LS and Ctrl vs. HS comparisons yielded 193 and 258 DEMs, respectively, according to miRNA-seq analysis. The visualized target relationships showed that zp2 and zp3, formed 12 target pairs with 11 different DEMs. Five miRNA-target gene pairs, miR-9-x/zp2, miR-9-z/zp2, miR-3154-y/zp2, miR-3533-y/zp3, and miR-365-y/zp3, were predicted at the sequence level after salinity stress. The result of qRT-PCR demonstrated that both zp2 and zp3 exhibited the highest expression levels in the ovary. The expression levels of zp2, zp3, miR-9-z, miR-3154-y, and miR-3533-y were higher in phase Ⅴ than in other phases of ovarian development. The expression levels of zp2, zp3, and miR-3154-y increased significantly, while the expression levels of miR-9-z and miR-3533-y remained unchanged after 17β-estradiol (E2) injection. The dual-luciferase reporter assay, together with the changes observed in zp2, zp3, miR-9-z, miR-3154-y, and miR-3533-y after low and high salt treatment, demonstrated that zp2 expression was regulated by miR-9-z and miR-3154-y, while zp3 was regulated by miR-3533-y. These results suggest that miR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 are involved in ovarian development and adaptation to salinity stress in spotted scat.http://www.sciencedirect.com/science/article/pii/S2352513425000390Scatophagus argusZona Pellucida ProteinMiRNA-SeqSalinity stress
spellingShingle Zhuoying Leng
Xinghua Lin
Yi Zhai
Hongjuan Shi
Dongneng Jiang
Mouyan Jiang
Huapu Chen
Tianli Wu
Siping Deng
MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)
Aquaculture Reports
Scatophagus argus
Zona Pellucida Protein
MiRNA-Seq
Salinity stress
title MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)
title_full MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)
title_fullStr MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)
title_full_unstemmed MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)
title_short MiR-9-z/zp2, miR-3154-y/zp2, and miR-3533-y/zp3 participated in ovarian development and adaptation to salinity stress in spotted scat (Scatophagus argus)
title_sort mir 9 z zp2 mir 3154 y zp2 and mir 3533 y zp3 participated in ovarian development and adaptation to salinity stress in spotted scat scatophagus argus
topic Scatophagus argus
Zona Pellucida Protein
MiRNA-Seq
Salinity stress
url http://www.sciencedirect.com/science/article/pii/S2352513425000390
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