Transcriptome Analysis Reveals Differences in Gene Expression in the Muscle of the Brown-Marbled Grouper (Epinephelus fuscoguttatus) with Different Growth Rates

Brown-marbled grouper is one of the most important mariculture species in China and is widely used as a crossbreeding parent in the grouper industry. Enhancing growth rates is a key target in fish breeding, and gaining insight into the underlying mechanisms responsible for growth differences between individuals can aid in the improvement of grouper growth rates. However, the mechanism behind growth differences in this fish remains unclear. We analyzed the transcriptome profiles of muscle tissues between fast- and slow-growing brown-marbled grouper using RNA-seq and identified 77 significantly up-regulated genes and 92 significantly down-regulated genes in the extreme growth groups. Our findings suggest that up-regulated genes such as ghr and tnni2, as well as down-regulated genes such as stc2 and pdp1, are associated with growth advantages in brown-marbled grouper. We used differentially expressed genes (DEGs) for GO and KEGG enrichment analyses. The results of the GO enrichments showed that the significantly up-regulated genes in the fast-growing group were involved in protein folding, the actin cytoskeleton, the myosin complex, and other processes. The results of the KEGG enrichments showed that the significantly up-regulated genes in the fast-growing group were involved in various pathways such as glycolysis/gluconeogenesis, adipocytokine signaling, MAPK signaling, carbon metabolism, and PI3K-Akt signaling. Additionally, gene set enrichment analysis (GSEA) showed that the PI3K/AKT/mTOR pathway was up-regulated in the fast-growing group, which may be responsible for the higher nutrient absorption efficiency and muscle growth in these fish. Our results contribute to a better understanding of the molecular mechanisms and regulatory pathways underlying fast growth in brown-marbled grouper. However, further studies are necessary to fully elucidate the mechanisms behind growth differences between individuals.

[1]  L. Braden,et al.  RNA-Seq Analysis of the Growth Hormone Transgenic Female Triploid Atlantic Salmon (Salmo salar) Hepatic Transcriptome Reveals Broad Temperature-Mediated Effects on Metabolism and Other Biological Processes , 2022, Frontiers in Genetics.

[2]  Dong Han,et al.  Heterozygous depletion of pik3r1 improves growth and feed conversion efficiency in Gibel carp (Carassius gibelio) , 2021 .

[3]  Li-na Wu,et al.  Whole‐genome sequencing of brown‐marbled grouper (Epinephelus fuscoguttatus) provides insights into adaptive evolution and growth differences , 2021, Molecular ecology resources.

[4]  Praveen Kumar Guttula,et al.  Molecular modeling, docking and dynamic simulations of growth hormone receptor (GHR) of Labeo rohita , 2020, Journal of biomolecular structure & dynamics.

[5]  Xuange Liu,et al.  Identifying the Related Genes of Muscle Growth and Exploring the Functions by Compensatory Growth in Mandarin Fish (Siniperca chuatsi) , 2020, Frontiers in Physiology.

[6]  Xiaoyan Xu,et al.  Transcriptome Analysis of the Liver and Muscle Tissues of Black Carp (Mylopharyngodon piceus) of Different Growth Rates , 2020, Marine Biotechnology.

[7]  D. Sabatini,et al.  mTOR at the nexus of nutrition, growth, ageing and disease , 2020, Nature Reviews Molecular Cell Biology.

[8]  Lina Wu,et al.  Identification of Candidate Growth-Related SNPs and Genes Using GWAS in Brown-Marbled Grouper (Epinephelus fuscoguttatus) , 2020, Marine Biotechnology.

[9]  Steven L Salzberg,et al.  Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype , 2019, Nature Biotechnology.

[10]  Gang Liu,et al.  The complete mitochondrial genome of the breed Ningbo brown-marbled grouper (Epinephelus fuscoguttatus) , 2019, Mitochondrial DNA. Part B, Resources.

[11]  W. Guo,et al.  Characterization and expression profiles of muscle transcriptome in Schizothoracine fish, Schizothorax prenanti. , 2019, Gene.

[12]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[13]  Gerard Arrey,et al.  Exercise-Induced Hypertrophic and Oxidative Signaling Pathways and Myokine Expression in Fast Muscle of Adult Zebrafish , 2017, Front. Physiol..

[14]  David M. Sabatini,et al.  mTOR Signaling in Growth, Metabolism, and Disease , 2017, Cell.

[15]  H. Liu,et al.  Transcriptome assembly and identification of genes and SNPs associated with growth traits in largemouth bass (Micropterus salmoides) , 2017, Genetica.

[16]  Y. Mukai,et al.  Morphogenesis of free neuromasts in the larvae of brown-marbled grouper Epinephelus fuscoguttatus , 2016 .

[17]  Yong Zhang,et al.  Transcriptome analysis reveals the molecular mechanisms underlying growth superiority in a novel grouper hybrid (Epinephelus fuscogutatus♀ × E. lanceolatus♂) , 2016, BMC Genetics.

[18]  Wenjia Yang,et al.  Two Chitin Biosynthesis Pathway Genes in Bactrocera dorsalis (Diptera: Tephritidae): Molecular Characteristics, Expression Patterns, and Roles in Larval—Pupal Transition , 2015, Journal of economic entomology.

[19]  I. Johnston,et al.  RNAseq analysis of fast skeletal muscle in restriction-fed transgenic coho salmon (Oncorhynchus kisutch): an experimental model uncoupling the growth hormone and nutritional signals regulating growth , 2015, BMC Genomics.

[20]  D. Calvisi,et al.  PI3K/AKT/mTOR pathway plays a major pathogenetic role in glycogen accumulation and tumor development in renal distal tubules of rats and men , 2015, Oncotarget.

[21]  E. Füchtbauer,et al.  Stanniocalcin-2 Inhibits Mammalian Growth by Proteolytic Inhibition of the Insulin-like Growth Factor Axis* , 2014, The Journal of Biological Chemistry.

[22]  Dongling Zhang,et al.  The complete mitochondrial genome of the hybrid grouper Epinephelus fuscoguttatus (♀)×Epinephelus lanceolatus (♂) , 2014, Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis.

[23]  Cheng Zhou,et al.  A Gain-of-Function Mutation in Tnni2 Impeded Bone Development through Increasing Hif3a Expression in DA2B Mice , 2014, PLoS genetics.

[24]  L. Cantley,et al.  Spatial Control of the TSC Complex Integrates Insulin and Nutrient Regulation of mTORC1 at the Lysosome , 2014, Cell.

[25]  B. Björnsson,et al.  Regulation of skeletal muscle growth in fish by the growth hormone--insulin-like growth factor system. , 2013, General and comparative endocrinology.

[26]  M. Sandri,et al.  Mechanisms regulating skeletal muscle growth and atrophy , 2013, The FEBS journal.

[27]  Zhanjiang Liu,et al.  RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. , 2013, Physiological genomics.

[28]  I. Johnston,et al.  What determines growth potential and juvenile quality of farmed fish species , 2013 .

[29]  Wei Shi,et al.  featureCounts: an efficient general purpose program for assigning sequence reads to genomic features , 2013, Bioinform..

[30]  Zhanjiang Liu,et al.  Transcriptomic signatures of attachment, NF-κB suppression and IFN stimulation in the catfish gill following columnaris bacterial infection. , 2012, Developmental and comparative immunology.

[31]  Jian Ye,et al.  Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction , 2012, BMC Bioinformatics.

[32]  D. Sabatini,et al.  mTOR Signaling in Growth Control and Disease , 2012, Cell.

[33]  I. Johnston,et al.  Growth and the regulation of myotomal muscle mass in teleost fish , 2011, Journal of Experimental Biology.

[34]  B. Picard,et al.  Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. II--Genetic factors related to animal performance and advances in methodology. , 2011, Animal : an international journal of animal bioscience.

[35]  B. Björnsson,et al.  IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. , 2011, American journal of physiology. Regulatory, integrative and comparative physiology.

[36]  S. Cohen,et al.  Regulation of tissue growth through nutrient sensing. , 2009, Annual review of genetics.

[37]  Davis J. McCarthy,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[38]  S. Panserat,et al.  Hepatic protein kinase B (Akt)–target of rapamycin (TOR)-signalling pathways and intermediary metabolism in rainbow trout (Oncorhynchus mykiss) are not significantly affected by feeding plant-based diets , 2009, British Journal of Nutrition.

[39]  T. Anthony,et al.  The leucine content of a complete meal directs peak activation but not duration of skeletal muscle protein synthesis and mammalian target of rapamycin signaling in rats. , 2009, The Journal of nutrition.

[40]  S. Panserat,et al.  An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[41]  Yoshihiro Yamanishi,et al.  KEGG for linking genomes to life and the environment , 2007, Nucleic Acids Res..

[42]  F. Giorgino,et al.  The IGF-I signaling pathway. , 2007, Current pharmaceutical design.

[43]  I. Johnston.  Environment and plasticity of myogenesis in teleost fish , 2006, Journal of Experimental Biology.

[44]  Pablo Tamayo,et al.  Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  T. Zhu,et al.  Signal transduction via the growth hormone receptor. , 2001, Cellular signalling.

[46]  P. Barton,et al.  Structural characterization of the human fast skeletal muscle troponin I gene (TNNI2). , 2000, Gene.

[47]  M. Waters,et al.  Molecular recognition events involved in the activation of the growth hormone receptor by growth hormone , 1999, Journal of molecular recognition : JMR.

[48]  K. Reddy,et al.  PDP1, a novel Drosophila PAR domain bZIP transcription factor expressed in developing mesoderm, endoderm and ectoderm, is a transcriptional regulator of somatic muscle genes. , 1997, Development.

[49]  A. H. Weatherley,et al.  Recruitment and maximal diameter of axial muscle fibres in teleosts and their relationship to somatic growth and ultimate size , 1988 .

[50]  Zhongliang Wang,et al.  Identification, characterization, and expressions profile analysis of growth hormone receptors (GHR1 and GHR2) in Hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus polyphekadion ♂). , 2019, Genomics.

[51]  M. Gerstein,et al.  RNA-Seq: a revolutionary tool for transcriptomics , 2009, Nature Reviews Genetics.

[52]  H. Bern,et al.  Insulin-like growth factor signaling in fish. , 2005, International review of cytology.

[53]  H. Dutta.  Growth in fishes. , 1994, Gerontology.