The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis

The greenfin horse-faced filefish, Thamnaconus septentrionalis, which is widely distributed in the Indo-West Pacific Ocean, is an important commercial fish species with characteristic blue-green fins, rough skin, and a spine-like first dorsal fin. Recently, T. septentrionalis has captured the attent...

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Main Authors: Yan Liu, Wengang Xu, Xueli Zhang, Jiulong Wang, Xiaoling Chen, Xiaoyan Yu, Jun Zeng, Yanqing Wu, Liming Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Marine Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2025.1556002/full
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author Yan Liu
Yan Liu
Yan Liu
Wengang Xu
Wengang Xu
Wengang Xu
Xueli Zhang
Jiulong Wang
Jiulong Wang
Jiulong Wang
Xiaoling Chen
Xiaoyan Yu
Jun Zeng
Yanqing Wu
Liming Liu
Liming Liu
Liming Liu
author_facet Yan Liu
Yan Liu
Yan Liu
Wengang Xu
Wengang Xu
Wengang Xu
Xueli Zhang
Jiulong Wang
Jiulong Wang
Jiulong Wang
Xiaoling Chen
Xiaoyan Yu
Jun Zeng
Yanqing Wu
Liming Liu
Liming Liu
Liming Liu
author_sort Yan Liu
collection DOAJ
description The greenfin horse-faced filefish, Thamnaconus septentrionalis, which is widely distributed in the Indo-West Pacific Ocean, is an important commercial fish species with characteristic blue-green fins, rough skin, and a spine-like first dorsal fin. Recently, T. septentrionalis has captured the attention of conservation and development due to its sharply declining population, and its great economic value as an important marine aquaculture fish species. To protect the resources of T. septentrionalis and develop its fishery industry, artificial breeding is essential and has been carried out gradually in local farms in China. A previous study has shown that temperature can effectively influence the gonadal development in T. septentrionalis in its overwintering state. However, the molecular mechanisms underlying the effects of temperature on the gonadal development in T. septentrionalis are still unrevealed and worth further study. In the present study, we systematically investigated the effects of temperature on ovary development in T. septentrionalis through transcriptomics and metabolomics analysis. The results showed that temperature rises significantly regulated the metabolic status of T. septentrionalis and promoted ovary development and maturation process through the regulation of the pathways of ECM-receptor interaction, regulation of actin cytoskeleton, oocyte meiosis, steroid hormone biosynthesis, lipid metabolism, ABC transporters, protein digestion and absorption, biosynthesis of amino acids pathways, etc. The histological, scanning electron microscope, and transmission electron microscope analyses showed that the oocytes in the ovaries of T. septentrionalis experiencing the temperature rises developed from phase II to III with increased gonadal somatic index and 17β-estradiol level. The present study for the first time elucidated the potential molecular regulatory mechanism of ovary development in T. septentrionalis induced by temperature and will provide valuable information for the artificial breeding of T. septentrionalis and conservation of T. septentrionalis fishery resources in the future.
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spelling doaj-art-9ba013051579469aba45a71fc8edaeb12025-08-20T02:09:24ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452025-04-011210.3389/fmars.2025.15560021556002The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysisYan Liu0Yan Liu1Yan Liu2Wengang Xu3Wengang Xu4Wengang Xu5Xueli Zhang6Jiulong Wang7Jiulong Wang8Jiulong Wang9Xiaoling Chen10Xiaoyan Yu11Jun Zeng12Yanqing Wu13Liming Liu14Liming Liu15Liming Liu16School of Ocean, Yantai University, Yantai, ChinaShandong Engineering Research Center of Healthy Land-Sea Relay Farming of Economic Fish, Yantai, ChinaYantai Engineering Research Center of Deep-sea Aquaculture of Economic Fish, Yantai, ChinaSchool of Ocean, Yantai University, Yantai, ChinaShandong Engineering Research Center of Healthy Land-Sea Relay Farming of Economic Fish, Yantai, ChinaYantai Engineering Research Center of Deep-sea Aquaculture of Economic Fish, Yantai, ChinaSchool of Ocean, Yantai University, Yantai, ChinaSchool of Ocean, Yantai University, Yantai, ChinaShandong Engineering Research Center of Healthy Land-Sea Relay Farming of Economic Fish, Yantai, ChinaYantai Engineering Research Center of Deep-sea Aquaculture of Economic Fish, Yantai, ChinaRizhao Ocean and Fishery Research Institute, Rizhao, ChinaNational Fisheries Technology Extension Center, Beijing, ChinaGuangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning, ChinaEast China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai, ChinaSchool of Ocean, Yantai University, Yantai, ChinaShandong Engineering Research Center of Healthy Land-Sea Relay Farming of Economic Fish, Yantai, ChinaYantai Engineering Research Center of Deep-sea Aquaculture of Economic Fish, Yantai, ChinaThe greenfin horse-faced filefish, Thamnaconus septentrionalis, which is widely distributed in the Indo-West Pacific Ocean, is an important commercial fish species with characteristic blue-green fins, rough skin, and a spine-like first dorsal fin. Recently, T. septentrionalis has captured the attention of conservation and development due to its sharply declining population, and its great economic value as an important marine aquaculture fish species. To protect the resources of T. septentrionalis and develop its fishery industry, artificial breeding is essential and has been carried out gradually in local farms in China. A previous study has shown that temperature can effectively influence the gonadal development in T. septentrionalis in its overwintering state. However, the molecular mechanisms underlying the effects of temperature on the gonadal development in T. septentrionalis are still unrevealed and worth further study. In the present study, we systematically investigated the effects of temperature on ovary development in T. septentrionalis through transcriptomics and metabolomics analysis. The results showed that temperature rises significantly regulated the metabolic status of T. septentrionalis and promoted ovary development and maturation process through the regulation of the pathways of ECM-receptor interaction, regulation of actin cytoskeleton, oocyte meiosis, steroid hormone biosynthesis, lipid metabolism, ABC transporters, protein digestion and absorption, biosynthesis of amino acids pathways, etc. The histological, scanning electron microscope, and transmission electron microscope analyses showed that the oocytes in the ovaries of T. septentrionalis experiencing the temperature rises developed from phase II to III with increased gonadal somatic index and 17β-estradiol level. The present study for the first time elucidated the potential molecular regulatory mechanism of ovary development in T. septentrionalis induced by temperature and will provide valuable information for the artificial breeding of T. septentrionalis and conservation of T. septentrionalis fishery resources in the future.https://www.frontiersin.org/articles/10.3389/fmars.2025.1556002/fullThamnaconus septentrionalisovary developmentmolecular mechanismtranscriptomicsmetabolomics
spellingShingle Yan Liu
Yan Liu
Yan Liu
Wengang Xu
Wengang Xu
Wengang Xu
Xueli Zhang
Jiulong Wang
Jiulong Wang
Jiulong Wang
Xiaoling Chen
Xiaoyan Yu
Jun Zeng
Yanqing Wu
Liming Liu
Liming Liu
Liming Liu
The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
Frontiers in Marine Science
Thamnaconus septentrionalis
ovary development
molecular mechanism
transcriptomics
metabolomics
title The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
title_full The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
title_fullStr The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
title_full_unstemmed The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
title_short The molecular mechanism of ovary development in Thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
title_sort molecular mechanism of ovary development in thamnaconus septentrionalis induced by rising temperature via transcriptomics and metabolomics analysis
topic Thamnaconus septentrionalis
ovary development
molecular mechanism
transcriptomics
metabolomics
url https://www.frontiersin.org/articles/10.3389/fmars.2025.1556002/full
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