DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation

Leopard coral grouper (<i>Plectropomus leopardus</i>), possessing a distinct red body color, is an important species in commercial markets; however, the high ratio of black individuals under intensive cultivation has limited the commercial value of the species. To dissect the regulatory...

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Main Authors: Yang Liu, Linna Wang, Zhentong Li, Linlin Li, Tangtang Ding, Shuai Chen, Pengfei Duan, Xinyi Wang, Yishu Qiu, Xiaoyu Ding, Yongsheng Tian
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Antioxidants
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Online Access:https://www.mdpi.com/2076-3921/14/1/93
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author Yang Liu
Linna Wang
Zhentong Li
Linlin Li
Tangtang Ding
Shuai Chen
Pengfei Duan
Xinyi Wang
Yishu Qiu
Xiaoyu Ding
Yongsheng Tian
author_facet Yang Liu
Linna Wang
Zhentong Li
Linlin Li
Tangtang Ding
Shuai Chen
Pengfei Duan
Xinyi Wang
Yishu Qiu
Xiaoyu Ding
Yongsheng Tian
author_sort Yang Liu
collection DOAJ
description Leopard coral grouper (<i>Plectropomus leopardus</i>), possessing a distinct red body color, is an important species in commercial markets; however, the high ratio of black individuals under intensive cultivation has limited the commercial value of the species. To dissect the regulatory mechanisms underlying the red skin trait in <i>P. leopardus</i>, gene expression and DNA methylation modifications were compared between red and black skin tissues after astaxanthin treatment. Astaxanthin effectively increased the redness value a* and body weight. Multi-omics analyses revealed the crucial roles of pathways related to antioxidants and lipid metabolism, particularly “Tyrosine metabolism”, “Melanogenesis”, “Fatty acid metabolism”, “Fatty acid elongation”, and “Biosynthesis of unsaturated acids”, in red skin coloration. A molecular network for the regulation of red skin coloration in <i>P. leopardus</i> was constructed, and <i>pmel</i>, <i>tyr</i>, <i>tyrp1a</i>, <i>tyrp1b</i>, <i>dct</i>, <i>slc24a5</i>, <i>wnt1</i>, <i>acsl4</i>, <i>elovl1</i>, <i>elovl6l.1</i>, <i>elovl6l.2</i>, and <i>elovl7</i> were identified as key genes. Notably, <i>pmel</i>, <i>acsl4</i>, and <i>elovl7</i> were negatively regulated by differential DNA methylation. Our results provide new insight into the molecular and epigenetic mechanisms of body color variation, representing a significant step towards breeding for the red skin trait in <i>P. leopardus</i>.
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spelling doaj-art-1ca2da4c29ec4d339072f2cf7553b5442025-01-24T13:19:28ZengMDPI AGAntioxidants2076-39212025-01-011419310.3390/antiox14010093DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color FormationYang Liu0Linna Wang1Zhentong Li2Linlin Li3Tangtang Ding4Shuai Chen5Pengfei Duan6Xinyi Wang7Yishu Qiu8Xiaoyu Ding9Yongsheng Tian10State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaLeopard coral grouper (<i>Plectropomus leopardus</i>), possessing a distinct red body color, is an important species in commercial markets; however, the high ratio of black individuals under intensive cultivation has limited the commercial value of the species. To dissect the regulatory mechanisms underlying the red skin trait in <i>P. leopardus</i>, gene expression and DNA methylation modifications were compared between red and black skin tissues after astaxanthin treatment. Astaxanthin effectively increased the redness value a* and body weight. Multi-omics analyses revealed the crucial roles of pathways related to antioxidants and lipid metabolism, particularly “Tyrosine metabolism”, “Melanogenesis”, “Fatty acid metabolism”, “Fatty acid elongation”, and “Biosynthesis of unsaturated acids”, in red skin coloration. A molecular network for the regulation of red skin coloration in <i>P. leopardus</i> was constructed, and <i>pmel</i>, <i>tyr</i>, <i>tyrp1a</i>, <i>tyrp1b</i>, <i>dct</i>, <i>slc24a5</i>, <i>wnt1</i>, <i>acsl4</i>, <i>elovl1</i>, <i>elovl6l.1</i>, <i>elovl6l.2</i>, and <i>elovl7</i> were identified as key genes. Notably, <i>pmel</i>, <i>acsl4</i>, and <i>elovl7</i> were negatively regulated by differential DNA methylation. Our results provide new insight into the molecular and epigenetic mechanisms of body color variation, representing a significant step towards breeding for the red skin trait in <i>P. leopardus</i>.https://www.mdpi.com/2076-3921/14/1/93<i>Plectropomus leopardus</i>body colormethylometranscriptomeantioxidant pathwaylipid metabolism
spellingShingle Yang Liu
Linna Wang
Zhentong Li
Linlin Li
Tangtang Ding
Shuai Chen
Pengfei Duan
Xinyi Wang
Yishu Qiu
Xiaoyu Ding
Yongsheng Tian
DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation
Antioxidants
<i>Plectropomus leopardus</i>
body color
methylome
transcriptome
antioxidant pathway
lipid metabolism
title DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation
title_full DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation
title_fullStr DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation
title_full_unstemmed DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation
title_short DNA Methylation and Transcriptome Profiling Reveal the Role of the Antioxidant Pathway and Lipid Metabolism in <i>Plectropomus leopardus</i> Skin Color Formation
title_sort dna methylation and transcriptome profiling reveal the role of the antioxidant pathway and lipid metabolism in i plectropomus leopardus i skin color formation
topic <i>Plectropomus leopardus</i>
body color
methylome
transcriptome
antioxidant pathway
lipid metabolism
url https://www.mdpi.com/2076-3921/14/1/93
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