A gene expression study of dorso-ventrally restricted pigment pattern in adult fins ofNeolamprologus meeli, an African cichlid species

Abstract

Fish color patterns are among the most diverse phenotypic traits found in the animal kingdom. Understanding the molecular and cellular mechanisms that control in chromatophore distribution and pigmentation underlying this diversity is a major goal in developmental and evolutionary biology, which has predominantly been pursued in the zebrafish model system. Here, we apply results from zebrafish work to study a naturally occurring color pattern phenotype in the fins of an African cichlid species from Lake Tanganyika. The cichlid fish Neolamprologus meeli displays a distinct dorsal color pattern, with black and white stripes along the edges of the dorsal fin and of the dorsal half of the caudal fin, corresponding with differences in melanophore density. To elucidate the molecular mechanisms controlling the differences in dorsal and ventral color patterning in the fins, we quantitatively assessed the expression of 15 candidate target genes involved in adult zebrafish pigmentation and stripe formation. For reference gene validation, we screened the expression stability of seven widely expressed genes across the investigated tissue samples and identified tbp as appropriate reference. Relative expression levels of the candidate target genes were compared between the dorsal, striped fin regions and the corresponding uniform, grey-colored regions in the anal and ventral caudal fin. Dorso-ventral expression differences, with elevated levels in both white and black stripes, were observed in two genes, the melanosome protein coding gene pmel and in igsf11, which affects melanophore adhesion, migration and survival. Next, we predicted potential shared upstream regulators of pmel and igsf11. Testing the expression patterns of six predicted transcriptions factors revealed dorso-ventral expression difference of irf1 and significant, negative expression correlation of irf1 with both pmel and igsf11. Based on these results, we propose pmel, igsf11 and irf1 as likely components of the genetic mechanism controlling distinct dorso-ventral color patterns in N. meeli fins.

The developmental and genetic trajectory of coloration in the guppy (Poecilia reticulata)

“…The differentially expressed genes we describe here also represent a different subset of melanin-related genes associated with melanin expression. One exception is the gene igsf11, which has been shown to play a role in melanophore stripe formation of adult zebrafish bodies and pigment patterning of adult African cichlid caudal fins (Eom et al, 2012;Ahi & Sefc, 2017). This gene was more highly expressed in stage 3 compared to stage 1 male guppies and provides a link to melanin pattern formation across distantly related species (Hedges et al, 2015).…”

The cell adhesion molecule BT-IgSF is essential for a functional blood–testis barrier and male fertility in mice

“…In the mouse brain, BT-IgSF is highly expressed in the mature dentate gyrus of the hippocampus, and knockdown experiments revealed that BT-IgSF is implicated in ␣-amino-3hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR)mediated synaptic transmission and plasticity (6). For non-neuronal cells, a critical role for BT-IgSF in promoting the migration of melanophores and their precursors has been described in zebrafish and Neolamprologus meeli (4,7).…”

Anterior-posterior gene expression differences in three Lake Malawi cichlid fishes with variation in body stripe orientation

“…To identify stably expressed reference genes for further analysis, we screened 6 genes which are known to be expressed in different tissues and often used as reference genes for qPCR analysis in fishes ( Table S1 ) ( Yang et al, 2013 ; Ahi et al, 2013 ; Pashay Ahi et al, 2016 ; Ahi & Sefc, 2017 ). Expression levels of the melanosome marker gene slc24a5 , which encodes an intracellular membrane cation exchanger predominantly present in melanosomes ( Lamason et al, 2005 ), and the iridophore lineage specific marker ltk, which encodes a tyrosine kinase receptor required for iridophore differentiation and stripe formation in adult zebrafish ( Lopes et al, 2008 ), were quantified as proxies for the densities of the two chromatophore types.…”

“…Expression levels of the melanosome marker gene slc24a5 , which encodes an intracellular membrane cation exchanger predominantly present in melanosomes ( Lamason et al, 2005 ), and the iridophore lineage specific marker ltk, which encodes a tyrosine kinase receptor required for iridophore differentiation and stripe formation in adult zebrafish ( Lopes et al, 2008 ), were quantified as proxies for the densities of the two chromatophore types. The expression levels of both genes have been shown to be tightly associated with numbers of iridophores and melanophores ( Fadeev et al, 2016 ; Ahi & Sefc, 2017 ; Lamason et al, 2005 ). To examine potential differences in structural properites of melanophores along the dark stripes, we quantified the expression of pmel/silv , which encodes a melanophore-specific transmembrane glycoprotein with an essential role in the organization of premelanosomes, melanin localization and determination of melanophore shape ( Schonthaler et al, 2005 ).…”

“…Also, melanophores tend to migrate to iridophore-free sites ( Patterson & Parichy, 2013 ) and when encountering an expanding region of dense iridophores, their shape changes and they eventually disappear ( Nüsslein-Volhard & Singh, 2017 ). At the molecular level, a number of genes involved in adult stripe formation and/or maintenance have already been identified in the zebrafish ( Singh & Nüsslein-Volhard, 2015 ) and can readily be tested as candidates contributing to the natural variation of color patterns across different groups of fishes ( Ahi & Sefc, 2017 ).…”