Genomic, Transcriptomic, and Epigenomic Features Differentiate Genes That Are Relevant for Muscular Polyunsaturated Fatty Acids in the Common Carp

Abstract

Polyunsaturated fatty acids (PUFAs) are a set of important nutrients that mainly include arachidonic acid (ARA4), docosahexaenoic acid (DHA), eicosapentaenoic acid (EPA), and α-linolenic acid (ALA). Recently, fish-derived PUFAs have been associated with cardiovascular health, fetal development, and improvement of brain functions. Studies have shown that fish muscular tissues are rich in PUFAs, which are influenced by various factors, including genetic variations, regulatory profiles, and methylation status of desaturase genes during fatty acid desaturation and elongation processes. However, the genetic mechanism and the pathways involved in fatty acid metabolism in fishes remain unclear. The overall aim of this study was to assess differences in gene expression responses among fishes with different fatty acid levels. To achieve this goal, we conducted genome-wide association analysis (GWAS) using a 250K SNP array in a population of 203 samples of common carp (Cyprinus carpio) and identified nine SNPs and 15 genes associated with muscular PUFA content. Then, RNA-Seq and whole genome bisulfite sequencing (WGBS) of different groups with high and low EPA, DHA, ARA4, and ALA contents in muscle, liver and brain tissues were conducted, resulting in 6,750 differentially expressed genes and 5,631 genes with differentially methylated promoters. Gene ontology and KEGG pathway enrichment analyses of RNA-Seq and WGBS results identified enriched pathways for fatty acid metabolism, which included the adipocytokine signaling pathway, ARA4 and linoleic acid metabolism pathway, and insulin signaling pathway. Integrated analysis indicated significant correlations between gene expression and methylation status among groups with high and low PUFA contents in muscular tissues. Taken together, these multi-level results uncovered candidate genes and pathways that are associated with fatty acid metabolism and paved the way for further genomic selection and carp breeding for PUFA traits.

Multi-omics data reveal genes that are relevant for muscular amino acids in the common carp

“…Genotyping and phenotyping of C. carpio samples Based on previous work [1,19,20], 199 samples were randomly collected from a cultivated population of C. carpio. The raw genotyping data with 184,978 SNPs for the 199 samples were obtained from SNP genotyping.…”

“…The quality and concentration of DNA were examined by agarose gel electrophoresis and colorimetry. The genotyping and quality control were conducted following the previously reported procedures [19].…”

“…The genomic DNA was sonicated with sodium sul te, which rst converted unmethylated cytosine to uracil and then to thymine [40]. WGBS was conducted according to previously reported method [19]. Bismark [41] was applied to align the methylation data to the reference genome, and swDMR [42] was used to analyze the differentially methylated regions (DMR) through a sliding window method.…”

“…Bismark [41] was applied to align the methylation data to the reference genome, and swDMR [42] was used to analyze the differentially methylated regions (DMR) through a sliding window method. The process of DMR detection and annotation followed the protocols that were previously reported [15,19]. The correlation analysis of DEG and DMP was performed using the R package ggplot2.…”

“…Integrating the methods of GWAS, transcriptome and methylation analyses, Zhang et al identi ed candidate genes and pathways associated with fatty acid metabolism in the common carp [19]. Here, we conducted multi-omics analysis of muscular amino acid content in the Yellow River carp using genomic, transcriptomic and epigenomic data.…”