Integration of host-pathogen functional genomics data into the chromosome-level genome assembly of turbot (Scophthalmus maximus)

Disease resilience is of utmost relevance for turbot aquaculture. Several infective diseases, covering a broad spectrum from viruses, bacteria to different parasites, have been identified by industry. Since they increase mortality rates, reduce feed conversion ratios and slow down growth rate, genetic breeding programs for increasing disease resilience are recognized as a useful alternative for controlling pathologies. For this, knowledge of the genetic basis underlying resilience using genomic tools is essential to develop the best effective breeding strategies. In the present study, we compiled the existing genomic information generated in the last decade to construct an integrated atlas of candidate genes and genomic regions involved in pathogen resistance against the main turbot industrial pathogens (Aeromonas salmonicida, Philasterides dicentrarchi, Enteromyxum scophthalmi and the VHS virus) within the chromosome-level turbot genome assembly recently released. Information comprehends reannotated differentially expressed genes (DEG) in different tissues along temporal series, QTL markers associated with important productive traits (disease resistance and growth) and signatures of domestic or wild selection, represented by runs of homozygosity (ROHi) islands and outlier markers for divergent selection. Most genetic features were successfully relocated in the turbot assembly including 81.1% of the total DEGs, plus all QTL markers, ROHi and outlier markers. The updated annotation of DEGs for resistance to each pathology demonstrated significant changes. While the new annotation of 53–83% of the DEGs was coherent with the original, roughly 10–24% showed imprecise annotations in both assembly versions, ∼5% lost their original annotation and 2–24% were now annotated. Functional enrichment revealed mostly functions related to immune response, such as chemotaxis, apoptosis regulation, leukocyte differentiation, cell adhesion, iron homeostasis and vascular permeability. Some DEGs, such as celsr1a (cadherin EGF LAG seen-pass G-type receptor 1), fgg (fibrinogen gamma chain) and c1qtnf9 (C1q and TNF related 9) were found near pathogen-associated QTL markers. Also, some shared DEGs for resistance to all pathogens were positioned near QTL markers or ROHi, such as hamp (hepcidin-1), plg (plasminogen) and a fibrinogen alpha chain-like gene. Overall, our results provide an integrative insight into the genetic architecture of turbot response to a range of pathogens that could prove useful for future genomic studies to benefit aquaculture breeding programsS