Comparative Transcriptome Analysis Identifies Candidate Genes Related to Black-Spotted Pattern Formation in Spotted Scat (Scatophagus argus)

Simple Summary Spotted scat (Scatophagus argus) is a commercially important marine aquaculture and ornamental fish species in China and East Asian countries. There are dozens of black spots on each side of the body, and the caudal fin, which is yellow and black, is appreciated in ornamental fish markets. To explore the genetic mechanisms of its pattern formation, we found 2357 differentially expressed genes (DEGs) by comparing the transcriptome in the black-spotted skin, non-spotted skin and caudal fin in S. argus. The results will expand our knowledge about the molecular mechanism of important genes and pathways associated with pigment pattern formation and provide a certain theoretical basis for the molecular breeding in S. argus. Abstract Spotted scat (Scatophagus argus) is an economically important marine aquaculture and ornamental fish species in Asia, especially in southeast China. In this study, skin transcriptomes of S. argus were obtained for three types of skin, including black-spotted skin (A), non-spotted skin (B) and caudal fin (C). A total of nine complementary DNA (cDNA) libraries were obtained by Illumina sequencing. Bioinformatics analysis revealed that 1358, 2086 and 487 genes were differentially expressed between A and B, A and C, and B and C, respectively. The results revealed that there were 134 common significantly differentially expressed genes (DEGs) and several key genes related to pigment synthesis and pigmentation, including tyrp1, mitf, pmel, slc7a2, tjp1, hsp70 and mart-1. Of these, some DEGs were associated with pigmentation-related Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways, such as tyrosine metabolism, melanogenesis, the Wnt signaling pathway and the mitogen-activated protein kinase (MAPK) signaling pathway. The results will facilitate understanding the molecular mechanisms of skin pigmentation differentiation in S. argus and provide valuable information for skin coloration, especially the formation of spotted patterns on other marine fish species.

[1]  M. Kreft,et al.  Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids , 2015, Journal of anatomy.

[2]  C. Nüsslein-Volhard,et al.  Tight Junction Protein 1a regulates pigment cell organisation during zebrafish colour patterning , 2015, eLife.

[3]  S. Mahboob,et al.  Comparative Transcriptome Analysis Reveals the Genetic Basis of Skin Color Variation in Common Carp , 2014, PloS one.

[4]  Shuhong Zhao,et al.  Identification of Genes Related to White and Black Plumage Formation by RNA-Seq from White and Black Feather Bulbs in Ducks , 2012, PloS one.

[5]  K. Kullander,et al.  Inactivation of Pmel Alters Melanosome Shape But Has Only a Subtle Effect on Visible Pigmentation , 2011, PLoS genetics.

[6]  L. Morrell,et al.  Colour change and assortment in the western rainbowfish , 2010, Animal Behaviour.

[7]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[8]  H. Hoekstra,et al.  Vertebrate pigmentation: from underlying genes to adaptive function. , 2010, Trends in genetics : TIG.

[9]  W. Huber,et al.  which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets , 2011 .

[10]  J. Volff,et al.  Pigmentary function and evolution of tyrp1 gene duplicates in fish , 2009, Pigment cell & melanoma research.

[11]  J. Volff,et al.  Pigmentation Pathway Evolution after Whole-Genome Duplication in Fish , 2009, Genome biology and evolution.

[12]  S. Kerje,et al.  The Dominant white mutation in the PMEL17 gene does not cause visual impairment in chickens. , 2009, Veterinary ophthalmology.

[13]  Meredith E. Protas,et al.  Evolution of coloration patterns. , 2008, Annual review of cell and developmental biology.

[14]  J. Miyoshi,et al.  Structural and functional associations of apical junctions with cytoskeleton. , 2008, Biochimica et biophysica acta.

[15]  V. Hearing,et al.  Direct interaction of tyrosinase with Tyrp1 to form heterodimeric complexes in vivo , 2007, Journal of Cell Science.

[16]  J. Matsumoto,et al.  Comparative Anatomy and Physiology of Pigment Cells in Nonmammalian Tissues , 2007 .

[17]  R. Sturm,et al.  Post-transcriptional regulation of melanin biosynthetic enzymes by cAMP and resveratrol in human melanocytes. , 2007, The Journal of investigative dermatology.

[18]  J. Bartek,et al.  The Sunny Side of p53 , 2007, Cell.

[19]  J. T. Bagnara,et al.  On the blue coloration of vertebrates. , 2007, Pigment cell research.

[20]  Manfred Schartl,et al.  Evolution of pigment synthesis pathways by gene and genome duplication in fish , 2007, BMC Evolutionary Biology.

[21]  P. Visscher,et al.  Compelling evidence that a single nucleotide substitution in TYRP1 is responsible for coat-colour polymorphism in a free-living population of Soay sheep , 2007, Proceedings of the Royal Society B: Biological Sciences.

[22]  L. Andersson,et al.  A missense mutation in PMEL17 is associated with the Silver coat color in the horse , 2006, BMC Genetics.

[23]  D. Parichy Evolution of danio pigment pattern development , 2006, Heredity.

[24]  W. Pavan,et al.  Interspecies difference in the regulation of melanocyte development by SOX10 and MITF. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[25]  I. Jackson,et al.  Regulation of pigmentation in zebrafish melanophores. , 2006, Pigment cell research.

[26]  S. O’Brien,et al.  Tyrosinase and tyrosinase related protein 1 alleles specify domestic cat coat color phenotypes of the albino and brown loci. , 2005, The Journal of heredity.

[27]  K. Wakamatsu,et al.  Tyrosinase-related proteins suppress tyrosinase-mediated cell death of melanocytes and melanoma cells. , 2004, Experimental cell research.

[28]  R. Kelsh,et al.  The Tomita collection of medaka pigmentation mutants as a resource for understanding neural crest cell development , 2004, Mechanisms of Development.

[29]  S. Schmutz,et al.  TYRP1 is associated with dun coat colour in Dexter cattle or how now brown cow? , 2003, Animal genetics.

[30]  W. Pavan,et al.  The importance of having your SOX on: role of SOX10† in the development of neural crest-derived melanocytes and glia , 2003, Oncogene.

[31]  Shu Chien,et al.  Role of integrins in endothelial mechanosensing of shear stress. , 2002, Circulation research.

[32]  S. Schmutz,et al.  TYRP1 and MC1R genotypes and their effects on coat color in dogs , 2002, Mammalian Genome.

[33]  J. Volff,et al.  Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. , 2002, Genetics.

[34]  Stephen L. Johnson,et al.  The evolution of morphological complexity in zebrafish stripes. , 2002, Trends in genetics : TIG.

[35]  R. Boissy,et al.  Tyrp1 and oculocutaneous albinism type 3. , 2001, Pigment cell research.

[36]  C. Nüsslein-Volhard,et al.  Zebrafish pigmentation mutations and the processes of neural crest development. , 1996, Development.

[37]  S. Shibahara,et al.  Identification of mutations in the pigment cell-specific gene located at the brown locus in mouse. , 2008, Pigment cell research.