Abstract

Pristella maxillaris is known as the X-ray fish based on its translucent body. However, the morphological characteristics and the molecular regulatory mechanisms of these translucent bodies are still unknown. In this study, the following three phenotypes, a black-and-gray body color or wild-type (WT), a silvery-white body color defined as mutant I (MU1), and a fully transparent body with a visible visceral mass named as mutant II (MU2), were investigated to analyze their chromatophores and molecular mechanisms. The variety and distribution of pigment cells in the three phenotypes of P. maxillaris significantly differed by histological assessment. Three types of chromatophores (melanophores, iridophores, and xanthophores) were observed in the WT, whereas MU1 fish were deficient in melanophores, and MU2 fish lacked melanophores and iridophores. Transcriptome sequencing of the skin and peritoneal tissues of P. maxillaris identified a total of 166,089 unigenes. After comparing intergroup gene expression levels, more than 3,000 unigenes with significantly differential expression levels were identified among three strains. Functional annotation and Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses of the differentially expressed genes (DEGs) identified a number of candidates melanophores and iridophores genes that influence body color. Some DEGs that were identified using transcriptome analysis were confirmed by quantitative real-time PCR. This study serves as a global survey of the morphological characteristics and molecular mechanism of different body colors observed in P. maxillaris and thus provides a valuable theoretical foundation for the molecular regulation of the transparent phenotype.

Highlights

  • As one of the most diverse phenotypic traits under strong selection pressure in many organisms, coloration plays numerous adaptive functions such as predator deterrence, species recognition, and even protecting the organism from solar ultraviolet radiation damage (Lowe and Goodman-Lowe, 1996; Parichy, 2006; Roberts et al, 2009; Zhang et al, 2015)

  • In the MU1 fish, melanophores were missing in the operculum lining, skin, and peritoneal tissues, which contained only two types of pigment cells, iridophores and xanthophores (Figures 1 B2, C2, D2)

  • Animal coloration plays an important role in ecological interactions, species recognition, and even protecting the organism from ultraviolet radiation damage (Muske and Fernald, 1987; Lowe and Goodman-Lowe, 1996; Fujimura et al, 2009; Sefc et al, 2014)

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Summary

Introduction

As one of the most diverse phenotypic traits under strong selection pressure in many organisms, coloration plays numerous adaptive functions such as predator deterrence, species recognition, and even protecting the organism from solar ultraviolet radiation damage (Lowe and Goodman-Lowe, 1996; Parichy, 2006; Roberts et al, 2009; Zhang et al, 2015). Most animals have different body colors that are mainly determined by diverse pigments synthesized by chromatophores or pigment cells. In adult red crucian carp (Carassius auratus, red var.), body color undergoes a gray-to-red change, which is due to alterations in the number of skin melanophores (Zhang et al, 2017). Several studies have reported that many fish species can change body transparency based on the differentiation and development of chromatophores (Nilsson Skold et al, 2010; Krauss et al, 2013; Franco-Belussi et al, 2016). The differentiation and development of pigment cells are strictly regulated by genes (Roberts et al, 2009; Dooley et al, 2013), whereas the genetics behind natural color morph variants in fish remains largely unknown

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