Red and White Chinook Salmon (Oncorhynchus tshawytscha): Differences in the Transcriptome Profile of Muscle, Liver, and Pylorus

Angelico Madaro,Jerome Schmeisser,Viviane Verlhac Trichet,Rolf Erik Olsen,Paul Whatmore,Santosh P. Lall,Ole Torrissen

doi:10.1007/s10126-020-09980-5

Abstract

Astaxanthin (Ax), the main carotenoid responsible for the distinct red flesh color in salmonids (Oncorhynchus, Salvelinus, Salmo, and Parahucho), is added to the diet of farmed fish at a substantial cost. Despite the great economical value for the salmon industry, the key molecular mechanisms involved in the regulation of muscle coloration are poorly understood. Chinook salmon (Oncorhynchus tshawytscha) represent an ideal model to study flesh coloration because they exhibit a distinct color polymorphism responsible for two color morphs, white and red flesh pigmented fish. This study was designed to identify the molecular basis for the development of red and white coloration of fish reared under the same experimental conditions and to better understand the absorption mechanism of Ax in salmonids. Pyloric caeca, liver, and muscle of both groups (n = 6 each) were selected as the most likely critical target organs to be involved respectively in the intestinal uptake, metabolism, and retention of Ax. Difference in the transcriptome profile of each tissue using next-generation sequencing technology was conducted. Ten KEGG pathways were significantly enriched for differentially expressed genes between red and white salmon pylorus tissue, while none for the transcriptome profile in the other two tissues. Differential expressed gene (DE) analyses showed that there were relatively few differences in muscle (31 DE genes, p < 0.05) and liver (43 DE genes, p < 0.05) of white and red Chinook salmon compared approximately 1125 DE genes characterized in the pylorus tissue, with several linked to Ax binding ability, absorption, and metabolism.

Highlights

Carotenoids are responsible for the bright yellow to red color in terrestrial and aquatic animals
Significant progress has been made to better understand the biochemical mechanisms involved in regulating the absorption, transport, tissue uptake, and metabolism of carotenoids in Atlantic salmon, many questions remain unanswered
As the organ or tissue governing the pigmentation difference is yet unknown, we focused on three likely target organs, pyloric caeca, liver, and muscle that regulate intestinal uptake, metabolism, and retention, respectively

Summary

Introduction

Carotenoids are responsible for the bright yellow to red color in terrestrial and aquatic animals. Ax is loosely bound to α-actinin, and the ability to bind to protein does not show any difference between Atlantic salmon and white-fleshed fish (halibut and haddock) (Saha et al 2005; Matthews et al 2006). Significant progress has been made to better understand the biochemical mechanisms involved in regulating the absorption, transport, tissue uptake, and metabolism of carotenoids in Atlantic salmon, many questions remain unanswered. Lipoproteins transport Ax to the liver and other tissues. Carotenoids are hydrophobic in nature and require class B scavenger proteins (Scarb) to transport them into the cell (Kiefer et al 2002). In Atlantic salmon, scarb is highly expressed in midgut as compared with other tissues (liver and skeletal muscle) (Sundvold et al 2011)

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Results

Conclusion