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. 2020 Oct;15(10):1052-1067.
doi: 10.1080/15592294.2020.1748914. Epub 2020 Apr 7.

Major gene expression changes and epigenetic remodelling in Nile tilapia muscle after just one generation of domestication

Ioannis Konstantinidis  1 , Pål Sætrom  1   2   3   4   5 , Robin Mjelle  1   2 , Artem V Nedoluzhko  1 , Diego Robledo  6 , Jorge M O Fernandes  1
Affiliations

Major gene expression changes and epigenetic remodelling in Nile tilapia muscle after just one generation of domestication

Ioannis Konstantinidis et al. Epigenetics. 2020 Oct.

Abstract

The historically recent domestication of fishes has been essential to meet the protein demands of a growing human population. Selection for traits of interest during domestication is a complex process whose epigenetic basis is poorly understood. Cytosine hydroxymethylation is increasingly recognized as an important DNA modification involved in epigenetic regulation. In the present study, we investigated if hydroxymethylation plays a role in fish domestication and demonstrated for the first time at a genome-wide level and single nucleotide resolution that the muscle hydroxymethylome changes after a single generation of Nile tilapia (Oreochromis niloticus, Linnaeus) domestication. The overall decrease in hydroxymethylcytosine levels was accompanied by the downregulation of 2015 genes in fish reared in captivity compared to their wild progenitors. In contrast, several myogenic and metabolic genes that can affect growth potential were upregulated. There were 126 differentially hydroxymethylated cytosines between groups, which were not due to genetic variation; they were associated with genes involved in immune-, growth- and neuronal-related pathways. Taken together, our data unveil a new role for DNA hydroxymethylation in epigenetic regulation of fish domestication with impact in aquaculture and implications in artificial selection, environmental adaptation and genome evolution.

Keywords: Oreochromis niloticus; DNA hydroxymethylation; Domestication; epigenetics; muscle growth.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1.
Figure 1.
Hydroxymethylation differences between wild Nile tilapia and their offspring reared in captivity. (a), Circular representation of the Nile tilapia nuclear genome (linkage groups LG1-LG23, no scaffolds included for visualization purposes). Only sites with substantial levels of 5hmC were included (298289 CCGG sites). (b), Histogram with the average number of hydroxymethylated cytosines,5-hm(dC), per 1 million nucleotides, in fast muscle of wild fish compared to their offspring undergoing domestication. Significance was evaluated using the one-tailed Student’s t-test (n = 6, p = 0.04). Standard errors of the means are shown by black bars. (c), Circular representation of the Nile tilapia mitochondrial genome with its gene features in both L and H strands. (a,c), Blue and red peaks (oriented in and out, respectively) represent the hydroxymethylation levels in the groups of wild fish and their offspring undergoing domestication, respectively. The height of each peak is the average count for each group per location (n = 6). The 5hmC counts per genomic location and individual, as well as the standard deviation for the W and D groups in panels 1a and 1 c can be found in Supplementary Table S9.
Figure 2.
Figure 2.
Histogram of gene features (Promoters defined from −1kb to +100bp; TTS defined from −100bp to +1kb). Yellow and turquoise represent the enrichment of sites with substantial levels of 5hmC (RRHP – 295720 sites) and total CCGGs (whole genome – 1791,720 sites) across the Nile tilapia genome, respectively.
Figure 3.
Figure 3.
Circular representation of the Nile tilapia nuclear genome (linkage groups LG1-LG23 and scaffolds) showing 126 DhmCs. For visualization purposes the numbers in the scaffold symbols ‘Sc’ represent the last four digits in the accession number starting with ‘NW_02032’ in the NCBI database (e.g. ‘Sc7315’ represents scaffold ‘NW_020327315’). Gene symbols refer to the closest gene to the reported CCGG site. See Figure 1(a,c) for explanations of peaks. The 5hmC counts per genomic location and individual, as well as the standard deviation for the W and D groups in Figure 3 can be found in Supplementary Table S10.
Figure 4.
Figure 4.
Heatmap showing the differentially expressed genes assigned to their gene ontology (GO) terms between the two clustered groups. Red and blue brackets at the bottom of the heatmap correspond to the ‘Domestication’ and ‘Wild’ groups, respectively. The gradient from blue to red colour represents down- to upregulation, respectively. Each GO term is colour-coded as shown at the left side of this heatmap. All related statistics, including significance of each enriched GO term, are shown in tables S5 and S6.
Figure 5.
Figure 5.
Principal component analysis (PCA) showing the genetic diversity of the 6 wild and 6 first-generation offspring based on their SNPs. Blue triangles and red circles represent the wild fish (W) and their counterparts in the first generation of domestication (D), respectively.
See this image and copyright information in PMC

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