De Novo assembly and comparative transcriptome analyses of purple and green morphs of Apostichopus japonicus during body wall pigmentation process

Lili Xing1,2,3, Lina Sun1,2, Shilin Liu1,2, Xiaoni Li1,2,3, Libin Zhang1,2, Hongsheng Yang1,2
1CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China
2Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
3University of Chinese Academy of Sciences, Beijing, 100049, China

Tài liệu tham khảo

Artavanis-Tsakonas, 1999, Notch signaling: Cell fate control and signal integration in development, Science, 284, 770, 10.1126/science.284.5415.770 Bai, 2015, The effect of salinity on the growth, energy budget and physiological performance of green, white and purple color morphs of sea cucumber, Apostichopus japonicus, Aquaculture, 437, 297, 10.1016/j.aquaculture.2014.12.020 Bai, 2016, Effects of dietary protein levels on the growth, energy budget, and physiological and immunological performance of green, white and purple color morphs of sea cucumber, Apostichopus japonicus, Aquaculture, 450, 375, 10.1016/j.aquaculture.2015.08.021 Barbato, 2007, Body patterns in cephalopods “Polyphenism” as a way of information exchange, Pattern Recogn. Lett., 28, 1854, 10.1016/j.patrec.2006.12.023 Braasch, 2007, Evolution of pigment synthesis pathways by gene and genome duplication in fish, BMC Evol. Biol., 7, 74, 10.1186/1471-2148-7-74 Bray, 2006, Notch signalling: a simple pathway becomes complex, Nat. Rev. Mol. Cell Biol., 7, 678, 10.1038/nrm2009 Chen, 2003, Overview of sea cucumber farming and sea ranching practices in China, SPC beche-de-mer Information Bulletin, 18, 18 Cheng, 2008, Skin color in fish and humans: impacts on science and society, Zebrafish, 5, 237, 10.1089/zeb.2008.0577 Cho, 2011, Pancreatic adenocarcinoma up-regulated factor (PAUF) enhances the expression of beta-catenin, leading to a rapid proliferation of pancreatic cells, Exp. Mol. Med., 43, 82, 10.3858/emm.2011.43.2.010 Cho, 2009, Cardamonin suppresses melanogenesis by inhibition of Wnt/beta-catenin signaling, Biochem. Biophys. Res. Commun., 390, 500, 10.1016/j.bbrc.2009.09.124 Choe, 1961, On the morphological and ecological differences between two commercial forms,“Green” and “Red”, of the Japanese common sea cucumber, Stichopus japonicus Selenka, Nippon Suisan Gakkaishi, 27, 105, 10.2331/suisan.27.97 Conesa, 2005, Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research, Bioinformatics, 21, 3674, 10.1093/bioinformatics/bti610 Croucher, 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, 10.1186/1471-2164-14-862 Dieci, 2013, Fibroblast growth factor receptor inhibitors as a cancer treatment: from a biologic rationale to medical perspectives, Cancer Discovery, 3, 264, 10.1158/2159-8290.CD-12-0362 Djurdjevic, 2015, Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids, J. Anat., 227, 583, 10.1111/joa.12373 Dorsky, 1998, Control of neural crest cell fate by the Wnt signalling pathway, Nature, 396, 370, 10.1038/24620 Dunn, 2000, Neural crest-directed gene transfer demonstrates Wnt1 role in melanocyte expansion and differentiation during mouse development, Proc. Natl. Acad. Sci. U. S. A., 97, 10050, 10.1073/pnas.97.18.10050 Ekblom, 2011, Applications of next generation sequencing in molecular ecology of non-model organisms, Heredity, 107, 1, 10.1038/hdy.2010.152 Elmer, 2009, Color assortative mating contributes to sympatric divergence of neotropical cichlid fish, Evolution, 63, 2750, 10.1111/j.1558-5646.2009.00736.x Fan, 2013, Skin transcriptome profiles associated with coat color in sheep, BMC Genomics, 14, 389, 10.1186/1471-2164-14-389 Gadd, 1988, Biosorption of copper by fungal melanin, Appl. Microbiol. Biotechnol., 29, 610, 10.1007/BF00260993 Geng, 2008, Protective action of bacterial melanin against spectrums by a sensitive plasmid-based DNA damage in full UV noncellular system, J. Biochem. Biophys. Methods, 70, 1151, 10.1016/j.jprot.2007.12.013 Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat. Biotechnol., 29, 10.1038/nbt.1883 Hallinan, 2016, Targeting the fibroblast growth factor receptor family in cancer, Cancer Treat. Rev., 46, 51, 10.1016/j.ctrv.2016.03.015 Han, 2008, A genome-wide association study identifies novel alleles associated with hair color and skin pigmentation, PLoS Genet., 10.1371/journal.pgen.1000074 Hayes, 2010, Genetic architecture of complex traits and accuracy of genomic prediction: coat colour, milk-fat percentage, and type in holstein cattle as contrasting model traits, PLoS Genet., 10.1371/journal.pgen.1001139 Heath, 1975, Color, sunlight and internal temperatures in land-snail cepaea-nemoralis (l), Oecologia, 19, 29, 10.1007/BF00377587 Hennebert, 2015, An integrated transcriptomic and proteomic analysis of sea star epidermal secretions identifies proteins involved in defense and adhesion, J. Proteome, 128, 83, 10.1016/j.jprot.2015.07.002 Henning, 2013, Transcriptomics of morphological color change in polychromatic Midas cichlids, BMC Genomics, 14, 1, 10.1186/1471-2164-14-171 Hoekstra, 2006, A single amino acid mutation contributes to adaptive beach mouse color pattern, Science, 313, 101, 10.1126/science.1126121 Holland, 1984 Hollocher, 2000, Evolution of abdominal pigmentation differences across species in the Drosophila dunni subgroup, Evolution, 54, 2046, 10.1111/j.0014-3820.2000.tb01248.x Houde, 1990, Correlated evolution of female mating preferences and male color patterns in the guppy poecilia-reticulata, Science, 248, 1405, 10.1126/science.248.4961.1405 Hubbard, 2010, Vertebrate pigmentation: from underlying genes to adaptive function, Trends Genet., 26, 231, 10.1016/j.tig.2010.02.002 Jiang, 2013, Comparative study on nutrient composition and growth of green and red sea cucumber, Apostichopus japonicus (Selenka, 1867), under the same culture conditions, Aquac. Res., 44, 317, 10.1111/j.1365-2109.2011.03033.x Jimbow, 1984, Characterization of melanogenesis and morphogenesis of melanosomes by physicochemical properties of melanin and melanosomes in malignant-melanoma, Cancer Res., 44, 1128 Kaelin, 2012, Specifying and sustaining pigmentation patterns in domestic and wild cats, Science, 337, 1536, 10.1126/science.1220893 Kanehisa, 2000, KEGG: Kyoto encyclopedia of genes and genomes, Nucleic Acids Res., 28, 27, 10.1093/nar/28.1.27 Kang, 2011, Allele-specific PCR genotyping of the HSP70 gene polymorphism discriminating the green and red color variants sea cucumber (Apostichopus japonicus), Journal of Genetics and Genomics, 38, 351 Kanno, 2002, Quantitative and qualitative evaluation on the color variation of the Japanese sea cucumber Stichopus japonicus, Suisanzoshoku (Japan)., 50, 63 Kanno, 2003, Genetic differentiation among three color variants of Japanese sea cucumber Stichopus japonicus, Fish. Sci., 69, 806, 10.1046/j.1444-2906.2003.00690.x Kern, 2011, Ras and Raf pathways in epidermis development and carcinogenesis, Br. J. Cancer, 104, 229, 10.1038/sj.bjc.6606009 Kijas, 2012, Genome-wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection, PLoS Biol., 10.1371/journal.pbio.1001258 Kim, 2015, HISAT: a fast spliced aligner with low memory requirements, Nat. Methods, 12, 357, 10.1038/nmeth.3317 Kollias, 1991, Photoprotection by melanin, J. Photochem. Photobiol. B, 9, 135, 10.1016/1011-1344(91)80147-A Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 10.1038/nmeth.1923 Li, 2011, RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome, BMC Bioinformatics, 12, 16, 10.1186/1471-2105-12-323 Liu, 2011, Characterization and in vitro antioxidation of papain hydrolysate from black-bone silky fowl (Gallus gallus domesticus Brisson) muscle and its fractions, Food Res. Int., 44, 133, 10.1016/j.foodres.2010.10.050 Manceau, 2011, The developmental role of agouti in color pattern evolution, Science, 331, 1062, 10.1126/science.1200684 Manning, 2003, Melanin and HIV in sub-Saharan Africa, J. Theor. Biol., 223, 131, 10.1016/S0022-5193(03)00070-5 Mckenna, 2010, The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res., 20, 1297, 10.1101/gr.107524.110 Milovanovic, 2004, Expression of Wnt genes and frizzled 1 and 2 receptors in normal breast epithelium and infiltrating breast carcinoma, Int. J. Oncol., 25, 1337 Moriyama, 2006, Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells, J. Cell Biol., 173, 333, 10.1083/jcb.200509084 Ng'oma, 2014, Transcriptome profiling of natural dichromatism in the annual fishes Nothobranchius furzeri and Nothobranchius kadleci, BMC Genomics, 15, 754, 10.1186/1471-2164-15-754 Nickoloff, 2005, Notch and NOXA-related pathways in melanoma cells, J. Investig. Dermatol. Symp. Proc., 10, 95, 10.1111/j.1087-0024.2005.200404.x Okorie, 2008, Preliminary study of the optimum dietary ascorbic acid level in sea cucumber, Apostichopus japonicus (Selenka), J. World Aquacult. Soc., 39, 758, 10.1111/j.1749-7345.2008.00211.x Park, 2009, Cellular mechanisms regulating human melanogenesis, Cell. Mol. Life Sci., 66, 1493, 10.1007/s00018-009-8703-8 Parkash, 2010, Impact of body melanisation on contrasting levels of desiccation resistance in a circumtropical and a generalist Drosophila species, Evol. Ecol., 24, 207, 10.1007/s10682-009-9301-9 Presgraves, 2003, Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila, Nature, 423, 715, 10.1038/nature01679 Protas, 2008, Evolution of coloration patterns, Annu. Rev. Cell Dev. Biol., 24, 425, 10.1146/annurev.cellbio.24.110707.175302 Quevillon, 2005, InterProScan: protein domains identifier, Nucleic Acids Res., 33, W116, 10.1093/nar/gki442 Racioppi, 2014, Fibroblast growth factor signalling controls nervous system patterning and pigment cell formation in Ciona intestinalis, Nat. Commun., 5, 17, 10.1038/ncomms5830 Reed, 2011, optix drives the repeated convergent evolution of butterfly wing pattern mimicry, Science, 333, 1137, 10.1126/science.1208227 Roberts, 2009, Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi Cichlid Fishes, Science, 326, 998, 10.1126/science.1174705 Rodgers, 2010, Colour change and assortment in the western rainbowfish, Anim. Behav., 79, 1025, 10.1016/j.anbehav.2010.01.017 Sang, 1990 Sava, 2001, A novel melanin-like pigment derived from black tea leaves with immune-stimulating activity, Food Res. Int., 34, 337, 10.1016/S0963-9969(00)00173-3 Sava, 2002, Protective activity of melanin-like pigment derived from tea on Drosophila melasnogaster against the toxic effects of benzidine, Food Res. Int., 35, 619, 10.1016/S0963-9969(01)00163-6 Scheil, 2013, Shell colour polymorphism, injuries and immune defense in three helicid snail species, Cepaea hortensis, Theba pisana and Cornu aspersummaximum, Res. Immunol., 3, 73, 10.1016/j.rinim.2013.06.002 Schepsky, 2006, The microphthalmia-associated transcription factor Mitf interacts with beta-catenin to determine target gene expression, Mol. Cell. Biol., 26, 8914, 10.1128/MCB.02299-05 Seo, 2011, Optimum dietary protein and lipid levels for growth of juvenile sea cucumber Apostichopus japonicus, Aquac. Nutr., 17, E56, 10.1111/j.1365-2095.2009.00728.x Slominski, 2004, Melanin pigmentation in mammalian skin and its hormonal regulation, Physiol. Rev., 84, 1155, 10.1152/physrev.00044.2003 Slominski, 2005, Hair follicle pigmentation, J. Investig. Dermatol., 124, 13, 10.1111/j.0022-202X.2004.23528.x Slominski, 2015, The role of melanin pigment in melanoma, Exp. Dermatol., 24, 258, 10.1111/exd.12618 Sokolova, 2000, Physiological variation related to shell colour polymorphism in White Sea Littorina saxatilis, J. Exp. Mar. Biol. Ecol., 245, 1, 10.1016/S0022-0981(99)00132-X Sturm, 2006, A golden age of human pigmentation genetics, Trends Genet., 22, 464, 10.1016/j.tig.2006.06.010 Sun, 2010, Comparative mitochondrial genomics within sea cucumber (Apostichopus japonicus): provide new insights into relationships among color variants, Aquaculture, 309, 280, 10.1016/j.aquaculture.2010.08.001 Takeda, 2000, Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a, J. Biol. Chem., 275, 14013, 10.1074/jbc.C000113200 Tarazona, 2011, Differential expression in RNA-seq: a matter of depth, Genome Res., 21, 2213, 10.1101/gr.124321.111 Thiel, 2003, Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.), Theor. Appl. Genet., 106, 411, 10.1007/s00122-002-1031-0 Turkington, 2014, Fibroblast growth factor receptor 4 (FGFR4): a targetable regulator of drug resistance in colorectal cancer, Cell Death Dis., 5, 10.1038/cddis.2014.10 Vasudev, 2014, Anti-angiogenic therapy for cancer: current progress, unresolved questions and future directions, Angiogenesis, 17, 471, 10.1007/s10456-014-9420-y Wang, 2016, Forkhead containing transcription factor Albino controls tetrapyrrole-based body pigmentation in planarian, Cell Discovery, 2, 16029, 10.1038/celldisc.2016.29 Wu, 2008, Identification and antioxidant activity of melanin isolated from Hypoxylon archeri, a companion fungus of Tremella fuciformis, J. Basic Microbiol., 48, 217, 10.1002/jobm.200700366 Xing, 2017, Comparison of pigment composition and melanin content among white, light-green, dark-green, and purple morphs of sea cucumber, Apostichopus japonicus, Acta Oceanol. Sin., 10.1007/s13131-017-1056-5 Xing, 2017, Growth, histology, ultrastructure and expression of MITF and astacin in the pigmentation stages of green, white and purple morphs of the sea cucumber, Apostichopus japonicus, Aquac. Res. Yamaguchi, 2007, The regulation of skin pigmentation, J. Biol. Chem., 282, 27,557, 10.1074/jbc.R700026200 Yue, 2015, Transcriptome analysis of shell color-related genes in the Clam Meretrix meretrix, Mar. Biotechnol., 17, 364, 10.1007/s10126-015-9625-0 Zhang, 2015, Taxonomic status of the three color variants in sea cucumber (Apostichopus japonicus): evidence from mitochondrial phylogenomic analyses, Mitochondrial DNA, 1 Zhao, 2012, Differences in MITF gene expression and histology between albino and normal sea cucumbers (Apostichopus japonicus Selenka), Chin. J. Oceanol. Limnol., 30, 80, 10.1007/s00343-012-1043-9 Zhao, 2011, Optimizing de novo transcriptome assembly from short-read RNA-Seq data: a comparative study, BMC Bioinformatics, 12, S2, 10.1186/1471-2105-12-S14-S2 Zhao, 2014, Differential gene expression in the respiratory tree of the sea cucumber Apostichopus japonicus during aestivation, Mar. Genomics, 18, 173, 10.1016/j.margen.2014.07.001