Research Article: Coordinated Regulation of Chromatophore Differentiation and Melanogenesis during the Ontogeny of Skin Pigmentation of Solea senegalensis (Kaup, 1858)

Date Published: May 9, 2013

Publisher: Public Library of Science

Author(s): Maria J. Darias, Karl B. Andree, Anaïs Boglino, Ignacio Fernández, Alicia Estévez, Enric Gisbert, Andre van Wijnen.


Abnormal pigmentation of Senegalese sole has been described as one problem facing the full exploitation of its commercial production. To improve our understanding of flatfish pigmentation of this commercially important species we have evaluated eleven genes related to two different processes of pigmentation: melanophore differentiation, and melanin production. The temporal distribution of gene expression peaks corresponds well with changes in pigmentation patterns and the intensity of skin melanization. Several gene ratios were also examined to put in perspective possible genetic markers for the different stages of normal pigmentation development. Further, the phenotypic changes that occur during morphogenesis correspond well with the main transitions in gene expression that occur. Given the dramatic phenotypic alterations which flatfish undergo, including the asymmetric coloration that occurs between the ocular and the blind side, and the synchrony of the two processes of morphogenesis and pigmentation ontogenesis, these species constitute an interesting model for the study of pigmentation. In this study we present a first approximation towards explaining the genetic mechanisms for regulating pigmentation ontogeny in Senegalese sole, Solea senegalensis.

Partial Text

Skin pigmentation of fishes is the result of the spatial combination and changes in number of several types of chromatophores that produce a huge variety of pigment patterns contributing to sex recognition, camouflage and predator avoidance, and speciation [1], [2], [3]. These neural crest-derived pigment cells are dermal and epidermal dark (brown-black) colored melanophores (equivalent to mammal melanocytes), yellow-orange xanthophores, red erythrophores, iridescent iridophores, white leucophores and blue cyanophores [4]. However, little is known about how these patterns are generated [5], [6]. Knowledge of the molecular ontogeny and pigment cell behavior underlying skin coloring is an essential step in understanding not only the origins of naturally occurring trait variation and evolution [7], but also the pigmentation disorders appearing in later stages of development [8], [9]. Insights into the mechanisms underlying these patterns can be gained by analyzing the expression profiles of pigmentation-related genes during the larval development of the fish.

The regulation of pigmentation in vertebrates is a quite complex process that encompasses the migration of crest-derived stem cells during the embryonic development, their proliferation in target tissues (i.e., skin) and differentiation into mature chromatophores, and a tightly controlled regulation of melanogenesis. Pigmentation biology has been extensively studied and many aspects are today well known, especially in melanocytes [62], [63]. However, less is known about the molecular basis of melanogenesis due to the intricate network of pathways regulating this process that includes many multifunctional mechanisms of action [64]. Due to the similarities shared with humans, fish have become extremely valuable experimental animal models for vertebrate developmental studies, especially those with underlying genetic components [60]. The genetics of pigmentation have been explored in several model teleost fish including zebrafish [5], [65], medaka [66], fugu [67], goldfish [35], [68] and, recently, in flatfish [27], [69]. To our knowledge, this is the first study that combines the characterization of the morphological ontogeny of skin pigmentation with the analysis of the expression profile of a set of key pigmentation-related genes during the larval development of a fish.