Quantitative trait loci for resistance to Flavobacterium psychrophilum in rainbow trout: effect of the mode of infection and evidence of epistatic interactions

Clémence Fraslin,Jean-François Bernardet,René Guyomard,Claire Kuchly,Diane Esquerré,Francine Krieg,Eric Duchaud,Edwige Quillet,Pierre Boudinot,Tatiana Rochat,Maria Bernard,Nicolas Dechamp,Caroline Hervet,Johanna Barbieri

doi:10.1186/s12711-018-0431-9

Abstract

BackgroundBacterial cold-water disease, which is caused by Flavobacterium psychrophilum, is one of the major diseases that affect rainbow trout (Oncorhynchus mykiss) and a primary concern for trout farming. Better knowledge of the genetic basis of resistance to F. psychrophilum would help to implement this trait in selection schemes and to investigate the immune mechanisms associated with resistance. Various studies have revealed that skin and mucus may contribute to response to infection. However, previous quantitative trait loci (QTL) studies were conducted by using injection as the route of infection. Immersion challenge, which is assumed to mimic natural infection by F. psychrophilum more closely, may reveal different defence mechanisms.ResultsTwo isogenic lines of rainbow trout with contrasting susceptibilities to F. psychrophilum were crossed to produce doubled haploid F2 progeny. Fish were infected with F. psychrophilum either by intramuscular injection (115 individuals) or by immersion (195 individuals), and genotyped for 9654 markers using RAD-sequencing. Fifteen QTL associated with resistance traits were detected and only three QTL were common between the injection and immersion. Using a model that accounted for epistatic interactions between QTL, two main types of interactions were revealed. A “compensation-like” effect was detected between several pairs of QTL for the two modes of infection. An “enhancing-like” interaction effect was detected between four pairs of QTL. Integration of the QTL results with results of a previous transcriptomic analysis of response to F. psychrophilum infection resulted in a list of potential candidate immune genes that belong to four relevant functional categories (bacterial sensors, effectors of antibacterial immunity, inflammatory factors and interferon-stimulated genes).ConclusionsThese results provide new insights into the genetic determinism of rainbow trout resistance to F. psychrophilum and confirm that some QTL with large effects are involved in this trait. For the first time, the role of epistatic interactions between resistance-associated QTL was evidenced. We found that the infection protocol used had an effect on the modulation of defence mechanisms and also identified relevant immune functional candidate genes.

Highlights

Bacterial cold-water disease, which is caused by Flavobacterium psychrophilum, is one of the major diseases that affect rainbow trout (Oncorhynchus mykiss) and a primary concern for trout farming
Average performance after immersion and injection infectious challenges Fish from the quantitative trait loci (QTL) family were challenged with F. psychrophilum via two modes of infection: after the immersion challenge, the overall survival rate was 77% at day 48 whereas after the injection challenge, it was 55% at day 34
After removing fish with a genotype call rate lower than 20% (n = 444) and markers with more than 70% missing genotypes (n = 11,570), 24 additional individuals that exhibited a rate of heterozygous loci higher than 1% were removed before the last filtering step based on minor allele frequency (MAF) (> 0.30) and marker call rate (> 90%)

Summary

Introduction

Bacterial cold-water disease, which is caused by Flavobacterium psychrophilum, is one of the major diseases that affect rainbow trout (Oncorhynchus mykiss) and a primary concern for trout farming. BCWD occurs worldwide and, according to [3], it is the second most important trout disease that affects French farms It causes high mortalities (up to 70%) and deformities may occur in surviving fish [1, 2, 4], with important economic impacts. Quantitative trait loci (QTL) associated with resistance measured as time to death or survival have been detected using linkage or association studies [15,16,17,18,19,20] in which resistance to F. psychrophilum was assessed using injection protocols for experimental infection

Methods

Results

Discussion

Conclusion