Genes & Genomics

, Volume 39, Issue 11, pp 1215–1225 | Cite as

Comparative transcriptome analysis of tube feet of different colors in the sea urchin Strongylocentrotus intermedius

  • Jun Ding
  • Dan Yang
  • Yaqing ChangEmail author
  • Yinan Wang
  • Weijie Zhang
  • Tingting Chen
Research Article


The Strongylocentrotus intermedius is an important commercially cultivated marine animal in China. In recent years, some individuals with diaphanous tube feet, rather than the normal red tube feet, have been observed among animals under cultivation; the basis of this phenotypic change is uncertain. In order to better understand the differences between two color tube feet of S. intermedius at the molecular level, we constructed four cDNA libraries from tube feet and coelomocytes of S. intermedius individuals with red or diaphanous tube feet. A total of 216,729,214 clean reads were assembled into 87,510 transcripts with an average size of 1677 bp. A BlastX search showed that 72,690 transcripts had significant matches in at least one target database. Expression profile analysis was performed on the four libraries and many differentially expressed genes were identified. Using gene enrichment analysis, several biological processes related to immune responses as well as immune-related candidate genes were identified. A total of 1694 genes were immune-related, and the genes expression of red tube feet were higher than that of diaphanous tube feet. In addition, 50,427 simple sequence repeats were obtained from the S. intermedius transcriptomes, while 32,650 and 42,264 single nucleotide polymorphisms were found in S. intermedius with diaphanous tube feet and red tube feet, respectively. These results provide valuable information for the future studies involving marker-assisted breeding and the studies of population genetics and genomics on S. intermedius.


Strongylocentrotus intermedius Transcriptome Coelomocytes Tube feet Gene expression 



This work was supported by Grants from State 863 High-Technology R & D Project of China (2012AA10A412), National Nature Science Foundation of China (31402275), and Ministry of Agriculture outstanding scientific research talent and innovation team.

Compliance with ethical standards

Conflict of interest

Jun Ding, Dan Yang, Yaqing Chang, Yinan Wang, Weijie Zhang and Tingting Chen declare that there is no conflict of interest.

Ethical approval

The sea urchins used in the current study were marine cultured animals, and all the experiments on sea urchins were conducted following institutional and national guidelines. No endangered or protected species was involved in the experiments of this study. No specific permission was required for the location of the culture experiment.

Supplementary material

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  1. Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29CrossRefPubMedPubMedCentralGoogle Scholar
  3. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29(4):1165–1188CrossRefGoogle Scholar
  4. Benjamini Y, Yekutieli D (2005) Quantitative trait loci analysis using the false discovery rate. Genetics 171:783–790CrossRefPubMedPubMedCentralGoogle Scholar
  5. Billack B, Laskin JD, Heck PT, Troll W, Gallo MA, Heck DE (1998) Alterations in cholinergic signaling modulate contraction of isolated sea urchin tube feet: potential role of nitric oxide. Bio Bull 195:196–196CrossRefGoogle Scholar
  6. Chang YQ, Ding J, Song J, Yang W (2004) Biology research and breeding of sea cucumber and sea urchin. Ocean Press, BeijingGoogle Scholar
  7. Chang Y, Chen X, Ding J, Cao X, Li R, Sun X (2007) Genetic diversity in five scallop populations of the Japanese scallop (Patinopecten yessoensis). Acta Ecol Sin 27:1145–1152Google Scholar
  8. Chen Y, Chang Y, Wang X, Qiu X, Liu Y (2015) De novo assembly and analysis of tissue-specific transcriptomes revealed the tissue-specific genes and profile of immunity from Strongylocentrotus intermedius. Fish Shellfish Immun 46:723–736CrossRefGoogle Scholar
  9. Costa V, Angelini C, De FI, Ciccodicola A (2010) Uncovering the complexity of transcriptomes with RNA-SEq. J Biomed Biotechnol 2010:853916. doi: 10.1155/2010/853916
  10. Ding J, Zhao L, Chang Y, Zhao W, Du Z, Hao Z (2015a) Transcriptome sequencing and characterization of Japanese scallop Patinopecten yessoensis from different shell color lines. PLoS One 10(2):e0116406CrossRefPubMedPubMedCentralGoogle Scholar
  11. Ding W, Ding J, Zhang W, Ding Y, He P (2015b) A preliminary study of rising temperature on immune-related enzyme and MDA content in family of sea urchins (Strongylocentrotus intermedius) with different tube feet colors. J Agric 5(9):110–116Google Scholar
  12. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484CrossRefPubMedGoogle Scholar
  15. Karakostis K, Costa C, Zito F, Matranga V (2016) Erratum: heterologous expression of newly identified galectin-8 from sea urchin embryos produces recombinant protein with lactose binding specificity and anti-adhesive activity. Sci Rep. doi: 10.1038/srep19169 PubMedPubMedCentralGoogle Scholar
  16. Kondo M, Akasaka K (2012) Current status of echinoderm genome analysis-what do we know? Cur Genom 13:134–143CrossRefGoogle Scholar
  17. Leulier F, Lemaitre B (2008) Toll-like receptors-taking an evolutionary approach. Nat Rev Genet 9:165–178CrossRefPubMedGoogle Scholar
  18. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760CrossRefPubMedPubMedCentralGoogle Scholar
  19. Li C, Haug T, Styrvold OB, Jørgensen TØ, Stensvåg K (2008) Strongylocins, novel antimicrobial peptides from the green sea urchin, Strongylocentrotus droebachiensis. Dev Comp Immunol 32:1430–1440CrossRefPubMedGoogle Scholar
  20. Li C, Blencke HM, Haug T, Jørgensen Ø, Stensvåg K (2014) Expression of antimicrobial peptides in coelomocytes and embryos of the green sea urchin (Strongylocentrotus droebachiensis). Dev Comp Immunol 43:106–113CrossRefPubMedGoogle Scholar
  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  22. Ludwig A, Pruvost M, Reissmann M, Benecke N, Brockmann GA, Castaños P, Cieslak M, Lippold S, Llorente L, Malaspinas AS (2009) Coat color variation at the beginning of horse domestication. Science 324(5926):485–485CrossRefPubMedPubMedCentralGoogle Scholar
  23. Meng P, Yang S, Shen C, Jiang K, Rong M, Lai R (2013) The first salamander defensin antimicrobial peptide. PLoS One 8:e83044CrossRefPubMedPubMedCentralGoogle Scholar
  24. Moreira R, Balseiro P, Planas JV, Fuste B, Beltran S, Novoa B, Figueras A (2012) Transcriptomics of in vitro immune-stimulated hemocytes from the Manila clam Ruditapes philippinarum using high-throughput sequencing. PLoS One 7:e35009CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nair SV, Del VH, Gross PS, Terwilliger DP, Smith LC (2005) Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol Genom 22:33–47CrossRefGoogle Scholar
  26. Pearce CM, Daggett TL, Robinson SM (2004) Effect of urchin size and diet on gonad yield and quality in the green sea urchin (Strongylocentrotus droebachiensis). Aquaculture 233:337–367CrossRefGoogle Scholar
  27. Shao Y, Li C, Che Z, Zhang P, Zhang W, Duan X, Li Y (2015) Cloning and characterization of two lipopolysaccharide-binding protein/bactericidal permeability–increasing protein (LBP/BPI) genes from the sea cucumber Apostichopus japonicus with diversified function in modulating ROS production. Dev Comp Immunol 52(1):88–97CrossRefPubMedGoogle Scholar
  28. Smith LC (2012) Innate immune complexity in the purple sea urchin: diversity of the Sp185/333 system. Front Immuno 3:70Google Scholar
  29. Smith L, Rast J, Brockton V, Terwilliger D, Nair S, Buckley K, Majeske A (2006) The sea urchin immune system. Invertebr Surviv J 3:25–39Google Scholar
  30. Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952CrossRefPubMedGoogle Scholar
  31. Wang K, Li M, Hadley D, Liu R, Glessner J, Grant SF, Hakonarson H, Bucan M (2007) PennCNV: an integrated hidden Markov model designed for high-resolution copy number variation detection in whole-genome SNP genotyping data. Genome Res 17:1665–1674CrossRefPubMedPubMedCentralGoogle Scholar
  32. Zhang W, Zhao C, Liu P, Chang Y (2010) First report on tube feet differential pigmentation in the cultivated sea urchin Strongylocentrotus intermedius (Agassiz, 1863) and its relationship with growth performance. Aquac Res 41:e706–e708Google Scholar
  33. Zhang P, Dong S, Wang F, Wang H, Gao W, Yan Y (2012) Effect of salinity on growth and energy budget of red and green colour variant sea cucumber Apostichopus japonicus (Selenca). Aquac Res 43:1611–1619CrossRefGoogle Scholar
  34. Zhao X, Chang Y, Ding J, Zhang W (2011) Comparative analysis of immunological characteristics of two populations in sea urchin Strongylocentrotus intermedius. Adv Marine Sci 29:10–16Google Scholar
  35. Zheng G, Marino M, Zhao J, McCluskey RT (1998) Megalin (gp330): a putative endocytic receptor for thyroglobulin (Tg). Endocrinology 139:1462–1465CrossRefPubMedGoogle Scholar
  36. Zheng HP, Zhang GF, Liu X, Que HY (2003) Establishment of different shell color lines of bay scallop Argopecten irradians irradians Lamarck (1819) and their development. Oceanol Limnol Sin 34:634–639Google Scholar
  37. Zhou Z, Dong Y, Sun H, Yang A, Chen Z, Gao S, Jiang J, Guan X, Jiang B, Wang B (2014) Transcriptome sequencing of sea cucumber (Apostichopus japonicus) and the identification of gene-associated markers. Mol Ecol Resour 14:127–138CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer-Science and Media 2017

Authors and Affiliations

  • Jun Ding
    • 1
  • Dan Yang
    • 1
  • Yaqing Chang
    • 1
    Email author
  • Yinan Wang
    • 1
  • Weijie Zhang
    • 1
  • Tingting Chen
    • 2
  1. 1.Key Laboratory of Mariculture and Stock Enhancement in North China’s Sea, Ministry of AgricultureDalian Ocean UniversityDalianChina
  2. 2.BIG Data Center (BIGD), Beijing Institute of GenomicsChinese Academy of SciencesBeijingChina

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