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

Abstract

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.

Morphological and Molecular Characterization of Dietary-Induced Pseudo-Albinism during Post-Embryonic Development of Solea senegalensis (Kaup, 1858)

“…Interactions between these pigment cells have already been reported and it is believed that xanthophores regulate melanophore pattern [22]. In fact, this relationship is required to form the Turing pattern of zebrafish [23] and has also been suggested for the pigmentation patterning of Senegalese sole [15]. Moreover, it has been shown that when melanophores and xanthophores are adjacent, these cells exclude each other [23].…”

“…This indicates that the new population of chromatophores that should appear after metamorphosis was not formed (or cells were not pigmented) in pseudo-albinos. While molecular signaling towards the differentiation of new populations of melanophores, xanthophores and iridophores occurs during pro-metamorphosis (11–19 dph), morphological changes occur later at post-metamorphosis [15]. Considering that the amount and proportions of these chromatophores were similar in pigmented and pseudo-albino specimens until 27 dph, and that their number remained invariable from that day onwards, it seemed that pigment cell precursors were likely influenced by the asymmetric signaling during pro-metamorphosis rather than in mature larval chromatophores [13].…”

“…Indeed, fish have been used as models for melanoma research because it has been shown tissues within fish share molecular signatures and histopathological features with human cancers [6]. The genetics of pigmentation have been explored in several model teleost fish including zebrafish [7], [8], medaka [9], fugu [10], goldfish [11], [12] and, recently, in flatfish [13], [14], [15]. Flatfish are particularly useful to analyze the origin of pigmentation disorders during the ontogeny because altered pigmentation can be induced under intensive rearing conditions [16], [17], [18], [19].…”

“…The process of pigmentation development can be seen as a cooperative relationship among three different processes: tissue remodeling (involving apoptosis), cellular differentiation of chromatophores, and pigment production. As a previous step, we have recently studied in the ocular side of this species the morphological and molecular ontogeny of skin pigmentation [15], which are essential to elucidate the mechanisms of formation of the adult pigmentation pattern and to understand when and how the albino phenotype appears. Gene markers for the above mentioned processes were seen to alter in a progression that was in synchrony with metamorphosis.…”

“…The above cited study revealed different stages of skin pigmentation and development in Senegalese sole that coincided with the progress of metamorphosis and patterns of gene expression: i) pre-metamorphosis period (2–11 dph), low expression of a marker of apoptosis ( casp3 ) and genes related to melanogenesis and high expression of melanophore differentiating genes; ii) pro-metamorphosis period (11–19 dph), high expression of casp3 (apoptosis and tissue remodeling) and melanophore differentiating and melanogenic genes; iii) post-metamorphosis (19–47 dph), low expression of all analyzed genes, especially those associated to melanophore differentiation. Major molecular changes in the pigment pattern occurred during pro-metamorphosis and morphological changes in the population of melanophores, xanthophores and iridophores were evidenced at post-metamorphosis to enable the juveniles to conform to the adult pattern of pigmentation [15].…”