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Transcriptome Analysis of Shell Color-Related Genes in the Clam Meretrix meretrix

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Abstract

Color polymorphism has received much attention due to its strong implications for speciation and adaptation. In contrast to body color, little is currently known about the molecular mechanism of shell color formation. This study represents the first analysis of the relationship between whole-scale gene expression and shell color variations in the marine bivalve mollusks via comparative transcriptome analyses. Three clam Meretrix meretrix strains with different and monotonous shell color patterns, which were developed by our 10-year artificial selection, combined with clams with nearly white shell color were used in the analyses. The results supported the idea that there was a relationship between gene expression and shell pigmentation in the clam M. meretrix, and complex signal transduction were involved. It was proposed that Notch signaling pathway played a crucial role in shell pigmentation in a gene-dosage dependent pattern and also potentially involved in the shell color patterning. Calcium signaling process may equally be implicated in shell color formation via activation of Notch pathway. Other differentially expressed genes (e.g., Myl, Mitf) potentially implicated in shell color pigmentation were also noticed. This study provides information on the expression profiles of clams with different shell color morphs and sheds light on color formation mechanism of shell.

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References

  • Adamkewicz L, Castagna M (1988) Genetics of shell color and pattern in the bay scallop Argopecten irradians. J Hered 79:14–17

    Google Scholar 

  • Addadi L, Weiner S (1985) Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci U S A 82:4110–4114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770–776

    Article  CAS  PubMed  Google Scholar 

  • Bagnara JT, Matsumoto J (2007) Comparative anatomy and physiology of pigment cells in nonmammalian tissues. The Pigmentary System: Physiology and Pathophysiology, Second Edition 11–59

  • Barbato M, Bernard M, Borrelli L, Fiorito G (2007) Body patterns in cephalopods: “polyphenism” as a way of information exchange. Pattern Recogn Lett 28:1854–1864

    Article  Google Scholar 

  • Beldade P, Brakefield PM (2002) The genetics and evo–devo of butterfly wing patterns. Nat Rev Genet 3:442–452

    CAS  PubMed  Google Scholar 

  • Boissy RE (2003) Melanosome transfer to and translocation in the keratinocyte. Exp Dermatol 12:5–12

    Article  PubMed  Google Scholar 

  • Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678–689

    Article  CAS  PubMed  Google Scholar 

  • Cain A (1988) The colours of marine bivalve shells with special reference to Macoma balthica. Malacologia 28:289–318

    Google Scholar 

  • Chang H, Choi H, Joo KM, Kim D, Lee TR (2012) Manassantin B inhibits melanosome transport in melanocytes by disrupting the melanophilin–myosin Va interaction. Pigm Cell Melanoma R 25:765–772

    Article  CAS  Google Scholar 

  • Croucher PJ, Brewer MS, Winchell CJ, Oxford GS, Gillespie RG (2013) De novo characterization of the gene-rich transcriptomes of two color-polymorphic spiders, Theridion grallator and T. californicum (Araneae: Theridiidae), with special reference to pigment genes. BMC Genomics 14:862

    Article  PubMed Central  PubMed  Google Scholar 

  • de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454

    Article  PubMed  Google Scholar 

  • Dent M, Raisman G, Lai FA (1996) Expression of type 1 inositol 1, 4, 5-trisphosphate receptor during axogenesis and synaptic contact in the central and peripheral nervous system of developing rat. Development 122:1029–1039

    CAS  PubMed  Google Scholar 

  • Fan R et al (2013) Skin transcriptome profiles associated with coat color in sheep. BMC Genomics 14:389

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fehon RG, Kooh PJ, Rebay I, Regan CL, Xu T, Muskavitch MA, Artavanis-Tsakonas S (1990) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61:523–534

    Article  CAS  PubMed  Google Scholar 

  • Freer A, Bridgett S, Jiang J, Cusack M (2014) Biomineral proteins from Mytilus edulis mantle tissue transcriptome. Mar Biotechnol 16:34–45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • French V, Brakefield PM (2004) Pattern formation: a focus on notch in butterfly eyespots. Curr Biol 14:R663–R665

    Article  CAS  PubMed  Google Scholar 

  • Garic-Stankovic A, Hernandez M, Flentke GR, Zile MH, Smith SM (2008) A ryanodine receptor-dependent Ca2+ asymmetry at Hensen's node mediates avian lateral identity. Development 135:3271–3280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heath D (1975) Colour, sunlight and internal temperatures in the land-snail Cepaea nemoralis (L.). Oecologia 19:29–38

    Article  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hillman RE (1961) Formation of the periostracum in Mercenaria mercenaria. Science 134:1754–1755

    Article  CAS  PubMed  Google Scholar 

  • Hlavacek WS, Faeder JR, Blinov ML, Perelson AS, Goldstein B (2003) The complexity of complexes in signal transduction. Biotechnol Bioeng 84:783–794

    Article  CAS  PubMed  Google Scholar 

  • Houde AE, Endler JA (1990) Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata. Science 248:1405–1408

    Article  CAS  PubMed  Google Scholar 

  • Innes DJHLE (1977) Inheritance of a shell-color polymorphism in the mussel. J Hered 68:203–204

    Google Scholar 

  • Joubert C et al (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11:613

    Article  PubMed Central  PubMed  Google Scholar 

  • Kobayashi T, Kawahara I, Hasekura O, Kijima A (2004) Genetic control of bluish shell color variation in the Pacific abalone, Haliotis discus hannai. J Shellfish Res 23:1153–1156

    Google Scholar 

  • Levy C, Khaled M, Fisher DE (2006) MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol Med 12:406–414

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Liu X, Wu F, Zhao H, Zhang G, Guo X (2009) A novel shell color variant of the Pacific abalone Haliotis discus hannai Ino subject to genetic control and dietary influence. J Shellfish Res 28:419–424

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (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 

  • Mitton JB (1977) Shell color and pattern variation in Mytilus edulis and its adaptive significance. Chesapeake Sci 18:387–390

    Article  Google Scholar 

  • Mori R, Wang Q, Danenberg KD, Pinski JK, Danenberg PV (2008) Both beta-actin and GAPDH are useful reference genes for normalization of quantitative RT-PCR in human FFPE tissue samples of prostate cancer. Prostate 68:1555–1560

    Article  CAS  PubMed  Google Scholar 

  • Moriyama M et al (2006) Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J Cell Biol 173:333–339

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Nickoloff BJ, Hendrix M, Pollock PM, Trent JM, Miele L, Qin J-Z (2005) Notch and NOXA-related pathways in melanoma cells. J Invest Dermatol Symp Proc 10:95–104

    Article  CAS  Google Scholar 

  • Nie H et al (2014) Transcriptome analysis of integument differentially expressed genes in the pigment mutant (quail) during molting of silkworm, Bombyx mori. PLoS One 9:e94185

    Article  PubMed Central  PubMed  Google Scholar 

  • Nijhout HF (1991) The development and evolution of butterfly wing patterns. Smithsonian series in comparative evolutionary biology (USA)

  • Pan Y, Lin M-H, Tian X, Cheng H-T, Gridley T, Shen J, Kopan R (2004) γ-Secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev Cell 7:731–743

    Article  CAS  PubMed  Google Scholar 

  • Parkash R, Kalra B, Sharma V (2009) Impact of body melanisation on contrasting levels of desiccation resistance in a circumtropical and a generalist Drosophila species. Evol Ecol 24:207–225

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rand MD, Lindblom A, Carlson J, Villoutreix BO, Stenflo J (1997) Calcium binding to tandem repeats of EGF‐like modules. Expression and characterization of the EGF‐like modules of human Notch‐1 implicated in receptor‐ligand interactions. Protein Sci 6:2059–2071

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raya Á et al (2004) Notch activity acts as a sensor for extracellular calcium during vertebrate left–right determination. Nature 427:121–128

    Article  CAS  PubMed  Google Scholar 

  • Reed RD (2004) Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales. Dev Genes Evol 214:43–46

    Article  CAS  PubMed  Google Scholar 

  • Reed RD, Serfas MS (2004) Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Curr Biol 14:1159–1166

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Scheil AE, Hilsmann S, Triebskorn R, Köhler H-R, Kapitel (2013) Shell colour polymorphism, injuries and immune defense in three helicid snail species, Cepaea hortensis, Theba pisana and Cornu aspersum maximum. Results in Immunol 3:73–78

    Article  Google Scholar 

  • Schouwey K, Beermann F (2008) The Notch pathway, hair graying and pigment cell homeostasis. Histol Histopathol 23:609–619

    CAS  PubMed  Google Scholar 

  • Schouwey K, Delmas V, Larue L, Zimber‐Strobl U, Strobl LJ, Radtke F, Beermann F (2007) Notch1 and Notch2 receptors influence progressive hair graying in a dose-dependent manner. Dev Dynam 236:282–289

    Article  CAS  Google Scholar 

  • Shi M, Lin Y, Xu G, Xie L, Hu X, Bao Z, Zhang R (2013) Characterization of the Zhikong scallop (Chlamys farreri) mantle transcriptome and identification of biomineralization-related genes. Mar Biotechnol 15:706–715

    Article  CAS  PubMed  Google Scholar 

  • Sivka U, Snoj A, Palandačić A, Sušnik Bajec S (2013) Identification of candidate genes involved in marble color pattern formation in genus Salmo. Comp Biochem Phys D 8:244–249

    CAS  Google Scholar 

  • Sokolova I, Berger VJ (2000) Physiological variation related to shell colour polymorphism in White Sea Littorina saxatilis. J Exp Mar Biol and Ecol 245:1–23

    Article  Google Scholar 

  • Somlyo AP, Somlyo AV (1994) Signal transduction and regulation in smooth muscle. Nature 372:231–236

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Liu B, Xiang J (2009) Cloning, characterization and expression of ferritin subunit from clam Meretrix meretrixin different larval stages. Comp Biochem Phys B 154:12–16

    Article  Google Scholar 

  • Wang C, Wachholtz M, Wang J, Liao X, Lu G (2014) Analysis of the skin transcriptome in two Oujiang color varieties of common carp. PLoS One 9:e90074

    Article  PubMed Central  PubMed  Google Scholar 

  • Winkler F, Estevez B, Jollan L, Garrido J (2001) Inheritance of the general shell color in the scallop Argopecten purpuratus (Bivalvia: Pectinidae). J Hered 92:521–525

    Article  CAS  PubMed  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Method Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11: R14

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (31202018) and the Chinese National High-Tech R & D Program (2012AA10A410).

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Authors and Affiliations

  1. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, China

    Xin Yue, Qing Nie & Baozhong Liu

  2. Zhejiang Mariculture Research Institute, Wenzhou, 325005, China

    Guoqiang Xiao

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  1. Xin Yue
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  2. Qing Nie
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Correspondence to Baozhong Liu.

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Yue, X., Nie, Q., Xiao, G. et al. Transcriptome Analysis of Shell Color-Related Genes in the Clam Meretrix meretrix . Mar Biotechnol 17, 364–374 (2015). https://doi.org/10.1007/s10126-015-9625-0

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