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

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:

• Domestication
• epigenetics
• DNA hydroxymethylation
• muscle growth
• Oreochromis niloticus

Acknowledgments

The LC-MS/MS analysis was performed by the Proteomics and Modomics Experimental Core facility (PROMEC), Norwegian University of Science and Technology (NTNU). PROMEC is funded by the Faculty of Medicine and Health Sciences at NTNU and the Central Norway Regional Health Authority.

We are thankful to Hilde Ribe, Øivind Torslett, Steinar Johnsen and Kaspar Klaudiussen for their assistance and unparalleled commitment to the husbandry and welfare of the fish.

Authors’ contributions

IK carried out the sampling, wet lab and bioinformatic analysis, interpreted the results and wrote the article. PS contributed significantly to the bioinformatic analysis of the RRHP data set, the interpretation of the results and revised the article. RM contributed significantly to the bioinformatic analysis of the RNA-Seq data set and revised the article. AVN contributed significantly in the wet lab and revised the article. DR contributed significantly to the bioinformatic analysis of the SNP data set. JMOF conceived the study, carried out the sampling, provided reagents and consumables, and contributed significantly to the interpretation of the results and the article revision.

Code availability

The scripts used for transcriptomic and hydroxymethylation analyses are available from the corresponding author upon request.

Disclosure statement

The authors declare that they have no competing interests.

Data availability statement

The RRHP dataset generated and analysed during the current study is available in the SRA (NCBI) repository, under the accession number PRJNA559277. The RNA-seq dataset generated and analysed during the current study is available in the GEO (NCBI) repository, under the accession number GSE135811.

Supplemental material

Supplemental data for this article can be accessed here.

Additional information

Funding

This work was funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreements nos 683210 and 812986) and by the Research Council of Norway under the Toppforsk programme (grant agreement no 250548/F20).