Gene expression response to sea lice in Atlantic salmon skin: an RNA-Seq comparison between resistant and susceptible animals

Abstract

BackgroundSea lice are parasitic copepods that cause large economic losses to salmon aquaculture worldwide. Frequent chemotherapeutic treatments are typically required to control this parasite, and alternative measures such as breeding for improved host resistance are desirable. Insight into the host-parasite interaction and mechanisms of host resistance can lead to improvements in selective breeding, and potentially novel treatment targets. In this study, RNA sequencing was used to study the skin transcriptome of Atlantic salmon parasitized with sea lice (C. rogercresseyi). The overall aims were to compare the transcriptomic profile of skin at louse attachment sites and ‘healthy’ skin, and to assess differences between animals with varying levels of resistance to the parasite.ResultsAtlantic salmon were challenged with C. rogercresseyi, growth and lice count measurements were taken for each fish. 21 animals were selected and RNA-Seq was performed on skin from a louse attachment site, and skin distal to attachment sites for each animal. These animals were classified into family-balanced groups according to the traits of resistance (high vs low lice count), and growth during infestation (an indication of tolerance). Overall comparison of skin from louse attachment sites versus healthy skin showed that 4,355 genes were differentially expressed, indicating local up-regulation of several immune pathways and activation of tissue repair mechanisms. Comparison between resistant and susceptible animals highlighted expression differences in several immune response and pattern recognition genes, and also myogenic and iron availability factors. Genomic regions showing signs of differentiation between resistant and susceptible fish were identified using an Fst analysis.ConclusionsComparison of the skin transcriptome between louse attachment sites and healthy skin has yielded a detailed profile of genes and pathways with putative roles in the local host immune response to C. rogercresseyi. The difference in skin gene expression profile between resistant and susceptible animals led to the identification of several immune and myogenic pathways potentially involved in host resistance. Components of these pathways may be targets for studies aimed at improved or novel treatment strategies, or to prioritise candidate functional polymorphisms to enhance genomic selection for host resistance in commercial salmon farming.

Atlantic salmon (Salmo salar L.) genetics in the 21st century: taking leaps forward in aquaculture and biological understanding

“…The cost‐effective discovery and concurrent genotyping of multiple, multiplexed samples in a single Illumina sequencing lane has been widely applied in many salmonid species (reviewed by Robledo et al . ). RAD‐seq and similar genotyping‐by‐sequencing techniques were applied in salmon even before the availability of a reference genome and have been used for QTL mapping, linkage mapping, genome‐wide association (GWA) studies, population genetics and SNP discovery for creating genotyping tools, including SNP arrays (Robledo et al .…”

“…RAD‐seq and similar genotyping‐by‐sequencing techniques were applied in salmon even before the availability of a reference genome and have been used for QTL mapping, linkage mapping, genome‐wide association (GWA) studies, population genetics and SNP discovery for creating genotyping tools, including SNP arrays (Robledo et al . ). Subsequently, high‐density SNP arrays were published for salmon (Houston et al .…”

Genomic selection in salmonids: new discoveries and future perspectives

“…However, genomic selection is an expensive method (fish genotyping costs range between 40 and 80 €/sample), so similar to the MAS method, it will be mostly relevant for traits of high economic value. Genomic selection has so far been applied for bacterial cold-water disease resistance in rainbow trout (Abdelrahman et al 2017, Vallejo et al 2017, Liu et al 2018Yoshida et al 2018) and sea lice resistance in Atlantic salmon (Tsai et al 2016b(Tsai et al , 2017Robledo et al 2018b). In different studies, the accuracy of the GEBVs varied from 0.16 to 0.83 for different traits (+ 24% for growth traits and 22% for disease resistance) compared to traditional methods based on genealogy (Ødegård et al 2014;Tsai et al 2015;Robledo et al 2018aRobledo et al , 2018b.…”

“…GWAS was used to study and dissect complex importatant traits (Correa et al 2015(Correa et al , 2016Gonzalez-Pena et al 2016;Tsai et al 2016b;Gutierrez et al 2018). QTLs identified for rainbow trout include stress response (Vallejo et al 2009), spawning time (Colihueque et al 2010), growth rate (Wringe et al 2010), osmoregulation capacity (Le Bras et al 2011), salinity tolerance (Norman et al 2012) and for Atlantic salmon growth rate (Houston et al 2009;Baranski et al 2010;Gutierrez et al 2012;Tsai et al 2015;Yoshida et al 2018), salinity tolerance (Norman et al 2012), resistence to sea lice (Tsai et al 2016a), pancreatic disease (Gonen et al 2015a) and amoebic gill disease (Robledo et al 2018b). In Table 2 are reported some QTLs identified for the Atlantic salmon and rainbow trout.…”

“…Recent innovations in the field of molecular biology have allowed greater efficiency and accuracy in animal selection . Meuwissen (2007) defined genomic Resistence to amoebic gill disease (AGD) Robledo et al 2018aRobledo et al , 2018b selection the simultaneous selection of several tens or hundreds of thousands of markers, with which it is possible to cover the entire genome so densely that all genes are expected to be in LD with at least some of the markers used. In particular, genomic selection is based on the prediction of the genomic breeding values of individuals (Genomic Estimated Breeding Values, GEBV), consisting of a large number of DNA markers that are in LD with QTLs encoding traits with important economic value and that span the genome (Solberg et al 2008;Clark et al 2011;Börner and Reinsch 2012).…”