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Transcriptome analysis of skin color variation during and after overwintering of Malaysian red tilapia

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A Correction to this article was published on 27 June 2022

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Abstract

The commercial value of red tilapia is hampered by variations in skin color during overwintering. In this study, three types of skin of red tilapia, including the skin remained pink color during and after overwintering (P), the skin changed from pink color to black color during overwintering and remained black color after overwintering (P-B), and the skin changed from pink color to black color during overwintering but recovered to pink color when the temperature rose after overwintering (P-B-P), were used to analyze their molecular mechanisms of color variation. The transcriptome results revealed that the P, P-B, and P-B-P libraries had 43, 42, and 43 million clean reads, respectively. The top 10 abundance mRNAs and specific mRNAs (specificity measure SPM > 0.9) were screened. After comparing intergroup gene expression levels, there were 2528, 1924, and 1939 differentially expressed genes (DEGs) between P-B-P and P-B, P-B-P and P, and P-B and P, respectively. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses of color-related mRNAs showed that a number of DEGs, including tyrp1, tyr, pmel, mitf, mc1r, asip, tat, hpdb, and foxd3, might play a potential role in pigmentation. Additionally, the co-expression patterns of genes were detected within the pigment-related pathways by the PPI network from P-B vs. P group. Furthermore, DEGs from the apoptosis and autophagy pathways, such as baxα, beclin1, and atg7, might be involved in the fading of red tilapia melanocytes. The findings will aid in understanding the molecular mechanism underlying skin color variation in red tilapia during and after overwintering as well as lay a foundation for future research aimed at improving red tilapia skin color characteristics.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

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References

  • Andrews S (2014) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 20 June 2021

  • Bian FF, Yang XF, Ou ZJ et al (2019) Morphological characteristics and comparative transcriptome analysis of three different phenotypes of Pristella maxillaris. Front Genet 10:698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braasch I, Liedtke D, Volff JN et al (2010) Pigmentary function and evolution of tyrp1 gene duplicates in fish. Pigment Cell Melanoma Res 22(6):839–850

    Article  Google Scholar 

  • Ceinos RM, Guillot R, Kelsh RN et al (2015) Pigment patterns in adult fish result from superimposition of two largely independent pigmentation mechanisms. Pigment Cell Melanoma Res 28(2):196–209

    Article  CAS  PubMed  Google Scholar 

  • Cheli Y, Ohanna M, Ballotti R, Bertolotto C (2010) Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res 23(1):27–40

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Shi Y, Liu M et al (2018a) circHIPK3 regulates cell proliferation and migration by sponging miR-124 and regulating AQP3 expression in hepatocellular carcinoma. Cell Death Dis 9(2):175

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen YX, Chen YS, Shi CM et al (2018b) Soapnuke: a mapreduce acceleration supported software for integrated quality control and preprocessing of high-throughput sequencing data. Oxford Open 7(1):gix120

    Google Scholar 

  • Dong ZJ, Luo MK, Wang LM et al (2020) MicroRNA-206 regulation of skin pigmentation in koi carp (Cyprinus carpio L.). Front Genet 11:47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez PJ, Bagnara JT (1991) Effect of background color and low temperature on skin color and circulating α-MSH in two species of leopard frog. Gen Comp Endocrinol 83(1):132–141

    Article  CAS  PubMed  Google Scholar 

  • Franz M, Lopes CT, Huck G et al (2016) Cytoscape.Js a graph theory library for visualisation and analysis. Bioinformatics 32(2):309–311

    CAS  PubMed  Google Scholar 

  • Fujimura N, Taketo MM, Mori M et al (2009) Spatial and temporal regulation of Wnt/β-catenin signaling is essential for development of the retinal pigment epithelium. Dev Biol 334(1):31–45

    Article  CAS  PubMed  Google Scholar 

  • Gouveia L, Rema P (2005) Effect of microalgal biomass concentration and temperature on ornamental goldfish (Carassius auratus) skin pigmentation. Aquac Nutr 11(1):19–23

    Article  Google Scholar 

  • Gross JB, Borowsky R, Tabin CJ (2009) A novel role for mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax Mexicanus. PLoS Genet 5(1):1000326

    Article  Google Scholar 

  • Guillot R, Ceinos RM, Cal R et al (2012) Transient ectopic overexpression of agouti-signalling protein 1 (asip1) induces pigment anomalies in flatfish. PLoS One 7(12):e48526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta MV, Acosta BO (2004) A review of global tilapia farming practices. Aquacult Asia Pac 9(1):7–12

    Google Scholar 

  • Gutierrez GB, Wiener P, Williams JL (2007) Genetic effects on coat color in cattle: dilution of eumelanin and phaeomelanin pigments in an F2-backcross Charolais ×Holstein population. BMC Genet 8(1):56

    Article  Google Scholar 

  • Henning F, Jones JC, Franchini P et al (2013) Transcriptomics of morphological color change in polychromatic Midas cichlids. BMC Genomics 14(1):171–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higdon CW, Mitra RD, Johnson SL et al (2013) Gene expression analysis of zebrafish melanocytes, iridophores, and retinal pigmented epithelium reveals indicators of biological function and developmental origin. PLoS One 8(7):e67801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbard JK, Uy JA, Hauber ME et al (2010) Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet 26:231–239

    Article  CAS  PubMed  Google Scholar 

  • Jiang BJ, Fu JJ, Dong ZJ et al (2019) Maternal ancestry analyses of red tilapia strains based on D-loop sequences of seven tilapia populations. PeerJ 7:e7007

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang YL, Zhang SH, Xu J et al (2014) Comparative transcriptome analysis reveals the genetic basis of skin color variation in common carp. PLoS One 9(9):e108200

    Article  PubMed  PubMed Central  Google Scholar 

  • José MCR, Tatjana H, Helgi BS et al (2005) Gene structure of the goldfish agouti-signaling protein: a putative role in the dorsal-ventral pigment pattern of fish. Endocrinology 146(3):1597–1610

    Article  Google Scholar 

  • Kats LB, Van DRG (1986) Background color-matching in the spring peeper. Hyla Crucifer 1:109–115

    Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) Hisat: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komatsu M, Waguri S, Ueno T et al (2005) Impairment of starvation-induced and constitutive autophagy in atg7 deficient mice. J Cell Biol 169(3):425–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krauss J, Geiger-Rudolph S, Koch I et al (2015) A dominant mutation in tyrp1a leads to melanophore death in zebrafish. Pigm Cell Melanoma Res 27(5):827–830

    Article  Google Scholar 

  • Li XJ, Li SF, Feng JH et al (2003) Preliminary study on salinity tolerance of Israel red tilapia. J Shanghai Fish Univ 12(3):205–208

    Google Scholar 

  • Li XM, Song YN, Xiao GB et al (2015) Gene expression variations of red-white skin coloration in common carp (Cyprinus carpio). Int J Mol Sci 16:21310–21329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao Y, Gordon K, Smyth et al (2014) Featurecounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7):923–930

    Article  CAS  PubMed  Google Scholar 

  • Lister JA, Close J, Raible DW (2001) Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev Biol 237(2):333–344

    Article  CAS  PubMed  Google Scholar 

  • Liu CS, Liu LY, Zhang Y et al (2020) Molecular mechanism of aqp3 in regulating differentiation and apoptosis of lung cancer stem cells through Wnt/GSK-3β/β-Catenin pathway. Jbuon 25(4):1714–1720

    PubMed  Google Scholar 

  • Luo MK, Lu GQ, Yin HR et al (2021) Fish pigmentation and coloration: molecular mechanisms and aquaculture perspectives. Rev Aquac 00:1–18

    Google Scholar 

  • Minvielle F, Bed’Hom B, Coville JL et al (2010) The “silver” Japanese quail and the mitf gene: causal mutation, associated traits and homology with the “blue” chicken plumage. BMC Genet 11(1):1–7

    Article  Google Scholar 

  • Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, bax, that accelerates programed cell death. Cell 74(4):609–619

    Article  CAS  PubMed  Google Scholar 

  • Pan JB, Hu SC, Wang H et al (2012) PaGeFinder: quantitative identification of spatiotemporal pattern genes. Bioinformatics 28(11):1544–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parmar MB, Venkatachalam AB, Wright JM (2012) The evolutionary relationship of the transcriptionally active fabp11a (intronless) and fabp11b genes of medaka with fabp11 genes of other teleost fishes. FEBS J 279(13):2310–2321

    Article  CAS  PubMed  Google Scholar 

  • Pavlidis M, Karkana M, Fanouraki E et al (2008) Environmental control of skin color in the red porgy, Pagrus Pagrus. Aquac Res 39(8):837–849

    Article  Google Scholar 

  • Pietrobono S, Anichini G, Sala C et al (2020) ST3GAL1 is a target of the SOX2-GLI1 transcriptional complex and promotes melanoma metastasis through AXL. Nat Commun 11(1):5865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pradeep PJ, Srijaya TC, Hassan A et al (2014) Optimal conditions for cold-shock induction of triploidy in red tilapia. Aquacult Int 22(3):1163–1174

    Article  CAS  Google Scholar 

  • Richardson J, Lundegaard PR, Reynolds NL, Dorin JR, Porteous DJ, Jackson IJ, Patton EE (2008) Mc1r pathway regulation of zebrafish melanosome dispersion. Zebrafish 5(4):289–295

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, Mccarthy DJ, Smyth GK (2010) Edger: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140

    Article  CAS  PubMed  Google Scholar 

  • Sherbrooke WC, Frost SK (1989) Integumental chromatophores of a color-change, thermoregulating lizard, Phrynosoma modestum (Iguanidae; reptilia). Am Mus Novit 2943(2):1–14

    Google Scholar 

  • Simon DJ, Peles D, Wakamatsu K et al (2009) Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology and function. Pigment Cell Melanoma Res 22(5):563–579

    Article  CAS  PubMed  Google Scholar 

  • Skarnes WC, Rosen B, West AP et al (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474(7351):337–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solano F, Martinez-Esparza M, Jimenez-Cervantes C, Hill SP, Lozano JA, Garcia-Borron JC (2000) New insights on the structure of the mouse silver locus and on the function of the silver protein. Pigment Cell Res 13(8):118–124

    Article  PubMed  Google Scholar 

  • Swiercz JM, Worzfeld T, Offermanns S (2008) ErbB-2 and met reciprocally regulate cellular signaling via plexin-B1. J Biol Chem 283(4):1893–1901

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S et al (2015) STRING v10: protein-protein networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452

    Article  CAS  PubMed  Google Scholar 

  • Takacs-Vellai K, Vellai T, Puoti A et al (2005) Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Curr Biol 15(16):1513–1517

    Article  CAS  PubMed  Google Scholar 

  • Tezuka A, Yamamoto H, Yokoyama J et al (2011) The mc1r gene in the guppy (Poecilia reticulata): genotypic and phenotypic polymorphisms. BMC Res Notes 4(1):31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas AJ, Erickson CA (2009) Foxd3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing mitf through a non-canonical mechanism. Development 136(11):1849–1858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voisey J, Box NF, Daal AV (2001) A polymorphism study of the human agouti gene and its association with mc1r. Pigment Cell Res 14(4):264–267

    Article  CAS  PubMed  Google Scholar 

  • Wang LG, Wang SQ, Li W (2012) RSeQC: quality control of RNA-seq experiments. Bioinformatics 28(16):2184–2185

    Article  CAS  PubMed  Google Scholar 

  • Wang LM, Song FB, Zhu WB et al (2018) Effects of temperature on body color of Malaysian red tilapia during overwintering period. J Fish China 42(1):72–79

    Google Scholar 

  • Wang XY, Yang J, Yao Y et al (2020) Aqp3 facilitates proliferation and adipogenic differentiation of porcine intramuscular adipocytes. Genes 11(4):453

    Article  CAS  PubMed Central  Google Scholar 

  • Wardani WW, Alimuddin A, Junior MZ et al (2020) Growth performance, robustness against stress, serum insulin, igf-1 and glut4 gene expression of red tilapia (Oreochromis sp.) fed diet containing graded levels of creatine. Aquac Nutr 27(1):274–286

    Article  Google Scholar 

  • Wu X, Zhao JD, Ruan YY et al (2018) Sialyltransferase st3gal1 promotes cell migration, invasion, and TGF-β1-induced EMT and confers paclitaxel resistance in ovarian cancer. Cell Death Dis 9(11):1102

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie C, Mao XZ, Huang JJ et al (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39(suppl_2):W316-22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu GC, Wang LG, Han YY et al (2012) Clusterprofiler: an r package for comparing biological themes among gene clusters. OMICS 16(5):284–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Wang L, Zhang S et al (2008) HmgA, transcriptionally activated by hpda, influences the biosynthesis of actinorhodin in Streptomyces Coelicolor. FEMS Microbiol Lett 280(2):219–225

    Article  CAS  PubMed  Google Scholar 

  • Zhang YP, Wang ZD, Guo YS et al (2015) Morphological characters and transcriptome profiles associated with black skin and red skin in crimson snapper (Lutjanus erythropterus). Int J Mol Sci 16(11):26991–27004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YQ, Liu JH, Peng LY et al (2017) Comparative transcriptome analysis of molecular mechanism underlying gray-to-red body color formation in red crucian carp (Carassius auratus, red var.). Fish Physiol Biochem 43(6):1387–1398

    Article  CAS  PubMed  Google Scholar 

  • Zhu WB, Wang LM, Dong ZJ et al (2016) Comparative transcriptome analysis identifies candidate genes related to skin color differentiation in red tilapia. Sci Rep 6(1):31347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by the National Natural Science Foundation-Youth Fund Project (31802290).

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Zaijie Dong conceived the study; Bingjie Jiang performed the experiments and wrote the paper; Wenbin Zhu provided the experimental materials; Lanmei Wang provided the funding for the experiment; Jianjun Fu and Wei Liu provided technical assistance in the experiments; Mingkun Luo revised the manuscript; Zaijie Dong reviewed the manuscript; all authors read and approved the manuscript.

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Correspondence to Zaijie Dong.

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The sampling scheme and experimental protocols were subject to approval by the Bioethical Committee of Freshwater Fisheries Research Center (FFRC) of the Chinese Academy of Fishery Sciences (CAFS) (BC 2013863, 9/2013). The methods of samples handled and experimental procedures carried out in accordance with the guidelines for the care and use of animals for scientific purposes issued by the Ministry of Science and Technology, Beijing, China (No.398, 2006).

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Jiang, B., Wang, L., Luo, M. et al. Transcriptome analysis of skin color variation during and after overwintering of Malaysian red tilapia. Fish Physiol Biochem 48, 669–682 (2022). https://doi.org/10.1007/s10695-022-01073-5

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