Abstract
Based on their cell ultrastructure, two types of erythrophores in the spotted skin regions of brown trout (Salmo trutta) were previously described. To test the hypothesis regarding the origin of a new cell type following genome duplication, we analysed the gene and paralogue gene expression patterns of erythrophores in brown trout skin. In addition, the ultrastructure of both erythrophore types was precisely examined using transmission electron microscopy (TEM) and correlative light microscopy and electron microscopy (CLEM). Ultrastructural differences between the sizes of erythrophore inclusions were confirmed; however, the overlapping inclusion sizes blur the distinction between erythrophore types, which we have instead defined as cell subtypes. Nevertheless, the red spots of brown trout skin with subtype 2 erythrophores, exhibited unique gene expression patterns. Many of the upregulated genes are involved in melanogenesis or xanthophore differentiation. In addition, sox10, related to progenitor cells, was also upregulated in the red spots. The expressions of paralogues derived from two genome duplication events were also analysed. Multiple paralogues were overexpressed in the red spots compared with other skin regions, suggesting that the duplicated gene copies adopted new functions and contributed to the origin of a new cell subtype that is characteristic for red spot. Possible mechanisms regarding erythrophore origin are proposed and discussed. To the best of our knowledge, this is the first study to evaluate pigment cell types in the black and red spots of brown trout skin using the advanced CLEM approach together with gene expression profiling.
Highlights
Based on their cell ultrastructure, two types of erythrophores in the spotted skin regions of brown trout (Salmo trutta) were previously described
Based on the analysis of two independent red and two independent black spots, from which we altogether took 49 images, we further demonstrated that melanophores in black spots are positioned immediately under the epithelium and are separated from type 1 erythrophores by a layer of fibroblasts or fibroblast-like cells (Fig. 1A–D)
The predominant cells were type 2 erythrophores (Fig. 1A,B) with erythrosomes of 882 ± 270 nm in diameter (Fig. 2C,D), some with a diameter of up to 3.5 μm (Fig. 2E). It seems that type 2 erythrophores are stabilized in the centres of red spots by fibroblasts or fibroblast-like cells, which they communicate with the extracellular space via prominent caveolae and are well connected with each other as well with type 2 erythrophores via desmosomes (Fig. 2F)
Summary
Based on their cell ultrastructure, two types of erythrophores in the spotted skin regions of brown trout (Salmo trutta) were previously described. The red spots of brown trout skin with subtype 2 erythrophores, exhibited unique gene expression patterns. To the best of our knowledge, this is the first study to evaluate pigment cell types in the black and red spots of brown trout skin using the advanced CLEM approach together with gene expression profiling. Xanthophores, and iridophores, erythrophores were found in the skin of some adult Salmonidae fish species: Salmo trutta and Salmo salar[4,8] They are distinguished from xanthophores based on the absence of xanthosomes, which are present only in xanthophores, while carotenoid-containing inclusions are present in both cell types, but may differ in size. Some studies even indicate evolutionary relationships between these cells (see[8] and the “Discussion” for more details)
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