Evolution of the Parvalbumin Genes in Teleost Fishes after the Whole-Genome Duplication

Petr Hanák,Zuzana Musilova,Kamila Zdeňková,Petra Horká,Subham Mukherjee,Oldřich Bartoš

doi:10.3390/fishes6040070

Abstract

Parvalbumin is considered a major fish allergen. Here, we report the molecular evolution of the parvalbumin genes in bony fishes based on 19 whole genomes and 70 transcriptomes. We found unexpectedly high parvalbumin diversity in teleosts; three main gene types (pvalb-α, pvalb-β1, and pvalb-β2, including oncomodulins) originated at the onset of vertebrates. Teleosts have further multiplied the parvalbumin gene repertoire up to nine ancestral copies—two copies of pvalb-α, two copies of pvalb-β1, and five copies of pvalb-β2. This gene diversity is a result of teleost-specific whole-genome duplication. Two conserved parvalbumin genomic clusters carry pvalb-β1 and β2 copies, whereas pvalb-α genes are located separately in different linkage groups. Further, we investigated parvalbumin gene expression in 17 tissues of the common carp (Cyprinus carpio), a species with 21 parvalbumin genes in its genome. Two pvalb-α and eight pvalb-β2 copies are highly expressed in the muscle, while two alternative pvalb-α copies show expression in the brain and the testes, and pvalb-β1 is dominant in the retina and the kidney. The recent pairs of muscular pvalb-β2 genes show differential expression in this species. We provide robust genomic evidence of the complex evolution of the parvalbumin genes in fishes.

Highlights

Parvalbumins are proteins from the calmodulin family, found mostly in the muscular tissues in vertebrates, and they are considered to be major fish allergens, which cause an IgE-mediated food hypersensitivity reaction in sensitive consumers [1]
We reconstructed the evolutionary history of parvalbumin genes based on the data of 19 genomes of the teleost fish, ray-finned fish, and vertebrate representatives
We report on the higher diversity of parvalbumin genes in teleost fishes compared to other vertebrate groups

Summary

Introduction

Parvalbumins are proteins from the calmodulin family, found mostly in the muscular tissues in vertebrates, and they are considered to be major fish allergens, which cause an IgE-mediated food hypersensitivity reaction in sensitive consumers [1]. As an example of the diversified gene family, parvalbumin genes (referred to as pvalb) carry traces of the ancient genomic duplications in eukaryotes, vertebrates, and teleost fishes [2,3,4]. The parvalbumin gene (including its intron) is an interesting marker that is used to identify fish species, or for phylogenetic studies [5,6,7,8]. A different amount of parvalbumin has been detected in the dark and light muscles of fishes [25,26]

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