Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

publishedVersio

A systemic study of lipid metabolism regulation in salmon fingerlings and early juveniles fed plant oil

In salmon farming, the scarcity of fish oil has driven a shift towards the use of plant-based oil from vegetable or seed, leading to fish feed low in long-chain PUFA (LC-PUFA) and cholesterol. Atlantic salmon has the capacity to synthesise both LC-PUFA and cholesterol, but little is known about the regulation of synthesis and how it varies throughout salmon life span. Here, we present a systemic view of lipid metabolism pathways based on lipid analyses and transcriptomic data from salmon fed contrasting diets of plant or fish oil from first feeding. We analysed four tissues (stomach, pyloric caeca, hindgut and liver) at three life stages (initial feeding 0·16 g, 2·5 g fingerlings and 10 g juveniles). The strongest response to diets higher in plant oil was seen in pyloric caeca of fingerlings, with up-regulation of thirty genes in pathways for cholesterol uptake, transport and biosynthesis. In juveniles, only eleven genes showed differential expression in pyloric caeca. This indicates a higher requirement of dietary cholesterol in fingerlings, which could result in a more sensitive response to plant oil. The LC-PUFA elongation and desaturation pathway was down-regulated in pyloric caeca, probably regulated by srebp1 genes. In liver, cholesterol metabolism and elongation and desaturation genes were both higher on plant oil. Stomach and hindgut were not notably affected by dietary treatment. Plant oil also had a higher impact on fatty acid composition of fingerlings compared with juveniles, suggesting that fingerlings have less metabolic regulatory control when primed with plant oil diet compared with juveniles.publishedVersion© The Authors 201

The Grayling Genome Reveals Selection on Gene Expression Regulation after Whole-Genome Duplication

Whole-genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ∼80 Ma (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one-third reflect nonneutral tissue expression evolution, with strong purifying selection, maintained over ∼50 Myr. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein–protein interactions. A small subset of the duplicates have evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points toward underlying differences in adaptive pressures on expression regulation in the nonanadromous grayling versus the anadromous Atlantic salmon. Our findings enhance our understanding of the role of WGD in genome evolution and highlight cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution