Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami

Sinocyclocheilus grahami is an economically valuable and famous fish in Yunnan Province, China. However, given its slow growth (40 g/2 years) and large growth differences among individuals, its growth performance needs to be improved for sustainable future use, in which molecular breeding technology...

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Main Authors: Yanhui Yin, Yuanwei Zhang, Zexiang Hua, Anli Wu, Xiaofu Pan, Junxing Yang, Xiaoai Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2023.1217952/full
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author Yanhui Yin
Yanhui Yin
Yanhui Yin
Yanhui Yin
Yuanwei Zhang
Yuanwei Zhang
Yuanwei Zhang
Zexiang Hua
Anli Wu
Anli Wu
Anli Wu
Xiaofu Pan
Xiaofu Pan
Xiaofu Pan
Junxing Yang
Junxing Yang
Junxing Yang
Xiaoai Wang
Xiaoai Wang
Xiaoai Wang
author_facet Yanhui Yin
Yanhui Yin
Yanhui Yin
Yanhui Yin
Yuanwei Zhang
Yuanwei Zhang
Yuanwei Zhang
Zexiang Hua
Anli Wu
Anli Wu
Anli Wu
Xiaofu Pan
Xiaofu Pan
Xiaofu Pan
Junxing Yang
Junxing Yang
Junxing Yang
Xiaoai Wang
Xiaoai Wang
Xiaoai Wang
author_sort Yanhui Yin
collection DOAJ
description Sinocyclocheilus grahami is an economically valuable and famous fish in Yunnan Province, China. However, given its slow growth (40 g/2 years) and large growth differences among individuals, its growth performance needs to be improved for sustainable future use, in which molecular breeding technology can play an important role. In the current study, we conducted muscle transcriptomic analysis to investigate the growth gaps among individuals and the mechanism underlying growth within 14 fast- and 14 slow-growth S. grahami. In total, 1,647 differentially expressed genes (DEGs) were obtained, including 947 up-regulated and 700 down-regulated DEGs in fast-growth group. Most DEGs were significantly enriched in ECM-receptor interaction, starch and sucrose metabolism, glycolysis/gluconeogenesis, pyruvate metabolism, amino acids biosynthesis and metabolism, peroxisome, and PPAR signaling pathway. Some genes related to glycogen degradation, glucose transport, and glycolysis (e.g., adipoq, prkag1, slc2a1, agl, pygm, pgm1, pfkm, gapdh, aldoa, pgk1, pgam2, bpgm, and eno3) were up-regulated, while some genes related to fatty acid degradation and transport (e.g., acox1, acaa1, fabp1b.1, slc27a1, and slc27a2) and amino acid metabolism (e.g., agxt, shmt1, glula, and cth) were down-regulated in the fast-growth group. Weighted gene co-expression network analysis identified col1a1, col1a2, col5a1, col6a2, col10a1, col26a1, bglap, and krt15 as crucial genes for S. grahami growth. Several genes related to bone and muscle growth (e.g., bmp2, bmp3, tgfb1, tgfb2, gdf10, and myog) were also up-regulated in the fast-growth group. These results suggest that fast-growth fish may uptake adequate energy (e.g., glucose, fatty acid, and amino acids) from fodder, with excess energy substances used to synthesize collagen to accelerate bone and muscle growth after normal life activities are maintained. Moreover, energy uptake may be the root cause, while collagen synthesis may be the direct reason for the growth gap between fast- and slow-growth fish. Hence, improving food intake and collagen synthesis may be crucial for accelerating S. grahami growth, and further research is required to fully understand and confirm these associations.
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spelling doaj.art-207a015a94b2400998084fc1778b7fbb2023-07-19T08:19:03ZengFrontiers Media S.A.Frontiers in Genetics1664-80212023-07-011410.3389/fgene.2023.12179521217952Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahamiYanhui Yin0Yanhui Yin1Yanhui Yin2Yanhui Yin3Yuanwei Zhang4Yuanwei Zhang5Yuanwei Zhang6Zexiang Hua7Anli Wu8Anli Wu9Anli Wu10Xiaofu Pan11Xiaofu Pan12Xiaofu Pan13Junxing Yang14Junxing Yang15Junxing Yang16Xiaoai Wang17Xiaoai Wang18Xiaoai Wang19State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Key Laboratory of Plateau Fish Breeding, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaKunming College of Life Science, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Key Laboratory of Plateau Fish Breeding, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaFishery Technology Extension Station of Yunnan, Kunming, Yunnan, ChinaState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Key Laboratory of Plateau Fish Breeding, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Key Laboratory of Plateau Fish Breeding, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Key Laboratory of Plateau Fish Breeding, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Key Laboratory of Plateau Fish Breeding, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaYunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, ChinaSinocyclocheilus grahami is an economically valuable and famous fish in Yunnan Province, China. However, given its slow growth (40 g/2 years) and large growth differences among individuals, its growth performance needs to be improved for sustainable future use, in which molecular breeding technology can play an important role. In the current study, we conducted muscle transcriptomic analysis to investigate the growth gaps among individuals and the mechanism underlying growth within 14 fast- and 14 slow-growth S. grahami. In total, 1,647 differentially expressed genes (DEGs) were obtained, including 947 up-regulated and 700 down-regulated DEGs in fast-growth group. Most DEGs were significantly enriched in ECM-receptor interaction, starch and sucrose metabolism, glycolysis/gluconeogenesis, pyruvate metabolism, amino acids biosynthesis and metabolism, peroxisome, and PPAR signaling pathway. Some genes related to glycogen degradation, glucose transport, and glycolysis (e.g., adipoq, prkag1, slc2a1, agl, pygm, pgm1, pfkm, gapdh, aldoa, pgk1, pgam2, bpgm, and eno3) were up-regulated, while some genes related to fatty acid degradation and transport (e.g., acox1, acaa1, fabp1b.1, slc27a1, and slc27a2) and amino acid metabolism (e.g., agxt, shmt1, glula, and cth) were down-regulated in the fast-growth group. Weighted gene co-expression network analysis identified col1a1, col1a2, col5a1, col6a2, col10a1, col26a1, bglap, and krt15 as crucial genes for S. grahami growth. Several genes related to bone and muscle growth (e.g., bmp2, bmp3, tgfb1, tgfb2, gdf10, and myog) were also up-regulated in the fast-growth group. These results suggest that fast-growth fish may uptake adequate energy (e.g., glucose, fatty acid, and amino acids) from fodder, with excess energy substances used to synthesize collagen to accelerate bone and muscle growth after normal life activities are maintained. Moreover, energy uptake may be the root cause, while collagen synthesis may be the direct reason for the growth gap between fast- and slow-growth fish. Hence, improving food intake and collagen synthesis may be crucial for accelerating S. grahami growth, and further research is required to fully understand and confirm these associations.https://www.frontiersin.org/articles/10.3389/fgene.2023.1217952/fullgrowthmetabolismcollagen synthesisWGCNAcrucial genes
spellingShingle Yanhui Yin
Yanhui Yin
Yanhui Yin
Yanhui Yin
Yuanwei Zhang
Yuanwei Zhang
Yuanwei Zhang
Zexiang Hua
Anli Wu
Anli Wu
Anli Wu
Xiaofu Pan
Xiaofu Pan
Xiaofu Pan
Junxing Yang
Junxing Yang
Junxing Yang
Xiaoai Wang
Xiaoai Wang
Xiaoai Wang
Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami
Frontiers in Genetics
growth
metabolism
collagen synthesis
WGCNA
crucial genes
title Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami
title_full Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami
title_fullStr Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami
title_full_unstemmed Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami
title_short Muscle transcriptome analysis provides new insights into the growth gap between fast- and slow-growing Sinocyclocheilus grahami
title_sort muscle transcriptome analysis provides new insights into the growth gap between fast and slow growing sinocyclocheilus grahami
topic growth
metabolism
collagen synthesis
WGCNA
crucial genes
url https://www.frontiersin.org/articles/10.3389/fgene.2023.1217952/full
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