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Comparative skin transcriptome of two Oujiang color common carp (Cyprinus carpio var. color) varieties

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Abstract

Body color variation has long been a hot research topic in evolutionary and functional biology. Oujiang color common carp (Cyprinus carpio var. color) is a well-known economical and ornamental fish. Three main types of pigments and four distinct color patterns are typical characters of Oujiang color common carp, which makes it an excellent fish model to study body coloration. In this study, skin transcriptome assembly and comparisons were conducted in two Oujiang color common carp varieties: whole red and whole white. Transcriptome comparison revealed that more differentially expressed energy metabolism genes were upregulated in whole white compared to whole red. The results indicated that energy metabolism genes might be strongly associated with environmental adaption and growth performance and likely affect the red and white color formation in Oujiang color common carp. Our study provided direct guidance for the aquaculture industrials of Oujiang color common carp and presented valuable genetic resources for body color research in fish.

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References

  • Andreas B, Simone A, Mareen N, Alexander R, Ronald MB, Tom G (2016) Transcriptome sequencing of maraena whitefish (Coregonus maraena). Mar Genomics 29:27–29

    Article  Google Scholar 

  • Bagnara JT, Matsumoto J (2007) Comparative anatomy and physiology of pigment cells in nonmammalian tissues. In: The Pigmentary System. Blackwell Publishing Ltd, pp 11–59

  • Baron M, Davies S, Alexander L, Snellgrove D, Sloman KA (2008) The effect of dietary pigments on the coloration and behaviour of flame-red dwarf gourami, Colisa lalia. Anim Behav 75:1041–1051

    Article  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequencedata. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braasch I, Schartl M, Volff JN (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 7:1–18

    Article  CAS  Google Scholar 

  • Braasch I, Brunet F, Volff JN, Schartl M (2009) Pigmentation pathway evolution after whole-genome duplication in fish. Genome Biol Evol 1:479–492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • David L, Rothbard S, Rubinstein I, Katzman H, Hulata G, Hillel J, Lavi U (2004) Aspects of red and black color inheritance in the Japanese ornamental (Koi) carp (Cyprinus carpio L.). Aquaculture 233:129–147

    Article  Google Scholar 

  • Enoch N, Marco G, Roberto R, Matthias P, Alessandro C (2014) Transcriptome profiling of natural dichromatismin the annual fishes Nothobranchius furzeri and Nothobranchius kadleci. BMC Genet 15:754

    Article  Google Scholar 

  • Fujii R (1993) Cytophysiology of fish chromatophores. In: Kwang W, Jeon MF, Jonathan J (eds) International review of cytology. Academic Press, Cambridge, pp 191–255

    Google Scholar 

  • Giulia M, Ralph B, Caroline R, Jorge MF, Alan SB, Samuel AM (2014) Exploring the transcriptome of Atlantic salmon (Salmo salar) skin, a major defense organ. Mar Biotechnol 14:559–569

    Google Scholar 

  • Goto M, Sato-Matsumura KC, Sawamura D, Yokota K, Nakamura H, Shimizu H (2004) Tyrosinase gene analysis in Japanese patients with oculocutaneous albinism. J Dermatol Sci 35:215–220

    Article  CAS  PubMed  Google Scholar 

  • Guo XL, Yin LZ, Zhong HL, Chun SG, Feng BY, Bian ZL, Jian XF (2015) De novo assembly and characterization of the spleen transcriptome of common carp (Cyprinus carpio) using Illumina paired-end sequencing. Fish Shellfish Immunol 44:420–429

    Article  CAS  Google Scholar 

  • Hoekstra HE (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity (Edinb) 97:222–234

    Article  CAS  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57

    Article  CAS  Google Scholar 

  • Imes DL, Geary LA, Grahn RA, Lyons LA (2006) Albinism in the domestic cat (Felis catus) is associated with a tyrosinase (TYR) mutation. Anim Genet 37:175–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji P, Liu G, Xu J, Li J, Zhao Z, Zhang X, Zhang Y, Xu P, Sun X (2012) Characterization of common carp transcriptome: sequencing, de novo assembly, annotation and comparative genomics. PLoS One 4:e35152

    Article  CAS  Google Scholar 

  • Jiang Y, Zhang S, Xu J, Feng J, Mahboob S, Al-Ghanim KA, Sun X, Xu P (2014) Comparative transcriptome analysis reveals the genetic basis of skin color variation in common carp. PLoS One 9:e108200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalinowski CT, Robaina LE, Fernández-Palacios H, Schuchardt D, Izquierdo MS (2005) Effect of different carotenoid sources and their dietary levels on red porgy (Pagrus pagrus) growth and skin color. Aquaculture 244:223–231

    Article  CAS  Google Scholar 

  • Katasonov VY(1978) A study of pigmentation in hybrids between the common and decorative Japanese carp. Genetika 14:2184–2192

  • Kelsh RN (2004) Genetics and evolution of pigment patterns in fish. Pigment Cell Res 17:326–336

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi S, Goto YN, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982–982

    Article  PubMed  Google Scholar 

  • Li SF, Wang CH (2001) Genetic diversity and selective breeding of red common carps in China. Naga: The ICLARM Quarterly 24:56–61

    Google Scholar 

  • Livak KJ, Schmittgen DT (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lynn LM, Kelsh RN, Wakamatsu Y, Ozato K (2005) Pigment pattern formation in the medaka embryo. Pigm Cell Res 18:64–73

    Article  Google Scholar 

  • Mariat D, Taourit S, Guerin G (2003) A mutation in the MATP gene causes the cream coat color in the horse. Genet Sel Evol 35:119–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montoliiu L, Oetting W, Bennett D (2016) Color genes. (July, 2016). European Society for Pigment Cell Research. URL: http://www.espcr.org/micemut

  • Naziroglu M, Gur S, Simsek H, Koprucu K (2000) Relationship between levels of beta-carotene, vitamin A and vitamin E in the seminal plasma, spermatozoa, blood serum and liver of rainbow trout. Vet Rec 147:484–486

    Article  CAS  PubMed  Google Scholar 

  • Parichy DM, Johnson SL (2001) Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol 211:319–328

    Article  CAS  PubMed  Google Scholar 

  • Protas ME, Patel NH (2008) Evolution of coloration patterns. Annu Rev Cell Dev Biol 24:425–446

    Article  CAS  PubMed  Google Scholar 

  • Rawls JF, Mellgren EM, Johnson SL (2001) How the zebrafish gets its stripes. Dev Biol 240:301–314

    Article  CAS  PubMed  Google Scholar 

  • Rodgers GM, Kelley JL, Morrell LJ (2010) Color change and assortment in the western rainbowfish. Anim Behav 79:1025–1030

    Article  Google Scholar 

  • Sarah JL, Trevor EP, Robert HD, Daniel DH (2016) Red and white Chinook salmon: genetic divergence and mate choice. Mol Ecol 25:1259–1274

    Article  Google Scholar 

  • Sturm RA (2002) Skin color and skin cancer-MC1R, the genetic link. Melanoma Res 12:405–416

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Chang Y, Ye Y, Ma Z, Liang Y, Li T, Jiang N, Xing W, Luo L (2012) The effect of dietary pigments on the coloration of Japanese ornamental carp (koi, Cyprinus carpio L.). Aquaculture 342-343:62–68

    Article  CAS  Google Scholar 

  • Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of Gene Ontology terms. PLoS One 6:e21800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzame VS, Sangeet L, Alvaro MB, Nima R, Leif A, Michel CM (2015) Amelanism in the corn snake is associated with the insertion of an LTR-retrotransposon in the OCA2 gene. Sci Rep 5:17118

    Article  CAS  Google Scholar 

  • Toomey MB, Lopes RJ, Araujo PM, Johnson JD, Gazda MA, Afonso S, Mota PG, Koch RE, Hill GE, Crobo JC, Carneiro M (2017) High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds. Proc Natl Acad Scl U S A 20:5219–5224

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villalta M, Estévez A, Bransden MP (2005) Arachidonic acid enriched live prey induces albinism in Senegal sole (Solea senegalensis) larvae. Aquaculture 245:193–209

    Article  CAS  Google Scholar 

  • Wang CH, Xiang SP, Lv Y, Wang J, Pan Z (2008) Preliminary study on inheritance of red and white color phenotypes in Oujiang color carp, C. carpio var. color (in Chinese). J Shanghai Fish Univ 4:004

    Google Scholar 

  • Wang CM, Jiao CS, Bai SQ, Yan B (2011) Nutritional factors influence the body color in fish (in Chinese). Vet Ornt S1:220–222

    Google Scholar 

  • Wei W (2009) Pathomorphology of vitamin E deficiency in channel catfish (Ictalurus punctatus) (in Chinese). Master Thesis, Sichuan Agricultural Universiy, China

  • Wishkerman A, Boglino A, Darias MJ, Andree KB, Estévez A, Gisbert E (2016) Image analysis-based classification of pigmentation patterns in fish: a case study of pseudo-albinism in Senegalese sole. Aquaculture 464:303–308

    Article  Google Scholar 

  • Xu X, Dong GX, Hu XS, Miao L, Zhang XL, Zhang DL, Yang HD, Zhang TY, Zou ZT, Zhang TT, Zhuang Y, Bhak J, Cho YS, Dai WT, Jiang TJ, Xie C, Li RQ, Luo SL (2013) The genetic basis of white tigers. Curr Biol 23:1031–1035

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y, Xu J, Zheng X, Ren L, Wang G, Zhang Y, Huo L, Zhao Z, Cao D, Lu C, Li C, Zhou Y, Liu Z, Fan Z, Shan G, Li X, Wu S, Song L, Hou G, Jiang Y, Jeney Z, Yu D, Wang L, Shao C, Song L, Sun J, Ji P, Wang J, Li Q, Xu L, Sun F, Feng J, Wang C, Wang S, Wang B, Li Y, Zhu Y, Xue W, Zhao L, Wang J, Gu Y, Lv W, Wu K, Xiao J, Wu J, Zhang Z, Yu J, Sun X (2014) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212–1219

    Article  CAS  PubMed  Google Scholar 

  • Zhu LY, Ma YQ, Xiang SP, Bi X, Wang J, Li W, Wang CH (2013) Observation and analysis of growth dynamics in Oujiang color common carp with different pigmentation types (in Chinese). J Shanghai Fish Univ 22:341–348

    Google Scholar 

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Acknowledgments

We would like to thank the Holland Computing Center (HCC) at the University of Nebraska for computational support and technical assistance.

Funding

This work was supported by the National Natural Science Foundation of China (31372521, 31772840), Guangxi Innovative Development Project (AA17204095-7), Leading Agricultural Talents in Shanghai Project (D-8004-16-0217), the Shanghai Science and Technology Project (15391900800), and Innovation Project of Shanghai Ocean University Graduate Education (A1-0209-15-0903-2).

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Correspondence to Chenghui Wang.

Ethics declarations

All experiments in this study were performed under the guidance of ethical regulation from the Institutional Animal Care and Use Committee (IACUS) of Shanghai Ocean University (Shanghai, China).

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Data archiving

Sequencing reads are available at NCBI SRA database (SRR6853720, SRR6853721).

Electronic supplementary material

Supplementary Figure S1–S4

(DOCX 1066 kb)

Supplementary Table S1

Primer sequences, amplicon sizes, qPCR efficiency, and coefficient of determination of standard curves for each gene. (DOCX 18 kb)

Supplementary Table S2

GO enrichment analysis for specifically expressed genes in WR (XLSX 14 kb)

Supplementary Table S3

GO enrichment analysis for specifically expressed genes in WW (XLSX 17 kb)

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Du, J., Chen, X., Wang, J. et al. Comparative skin transcriptome of two Oujiang color common carp (Cyprinus carpio var. color) varieties. Fish Physiol Biochem 45, 177–185 (2019). https://doi.org/10.1007/s10695-018-0551-8

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  • DOI: https://doi.org/10.1007/s10695-018-0551-8

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