Skip to main content
SpringerLink
Log in

Transcriptic analysis of Huanghai No. 1 strain of Chinese shrimp Fenneropenaeus chinensis using 454 pyrosequencing

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

The Huanghai No. 1 strain of Chinese shrimp Fenneropenaeus chinensis is an ecologically and economically important variety that is cultivated mainly in northern China. This strain has been subjected to multiple selective events in recent years. Conventional methods are insufficient to reveal the genetic background of Huanghai No. 1, especially with regard to a genome-wide transcription profile, and publicly available genomic resources for Huanghai No. 1 are limited. We obtained 907,945 original reads with an average length of 467.5 bp from muscle and haemocyte samples from Huanghai No. 1 using 454 pyrosequencing. After preprocessing, 867,245 high-quality reads were screened. Of the 64,830 assembled sequences, 34,633 of the unigenes had significant matches in the databases (similarity >30 %), including 14,138 isotigs and 20,495 singletons. A gene ontology analysis assigned 8,257 unigenes to 44 subcategories, with the majority of unigenes assigned to cellular component (28.2 %), biological process (20.5 %) and molecular function (5.0 %) categories. Pathway mapping based on information in the Kyoto Encyclopedia of Genes and Genomes database showed that 15,461 transcripts were associated with 223 pathways. A total of 14,981 putative SSRs, 72,370 SNPs, and candidate genes involved in growth, reproduction, and the immune response were identified. Our findings represent the most comprehensive transcriptomic resources currently available for Huanghai No. 1, and provide an important foundation for further genomic studies of F. chinensis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Brock JA, Gose RB, Lightner DV, Hasson K (1997) Recent developments and an overview of Taura Syndrome of farmed shrimp in the Americas. In: Flegel TW, MacRae IH (eds) Diseases in Asian Aquaculture III. Fish Health Section, Asian Fisheries Society, Manila, pp 275–284

    Google Scholar 

  2. Lightner DV, Hasson KW, White BL, Redman RM (1998) Experimental infection of western hemisphere penaeid shrimp with Asian white spot syndrome virus and Asian yellow head virus. J Aquat Anim Health 10:271–281

    Article  Google Scholar 

  3. Gjedrem T, Fimland E (1995) Potential benefits from high health and genetically improved shrimp shocks. In: Browdy CL, Hopkins JS (eds) Swimming Through troubled water, proceedings of the special session on shrimp farming. World Society, Baton Rouge, LA, pp 60–65

    Google Scholar 

  4. Benzie JAH (1998) Penaeid genetics and biotechnology. Aquaculture 164:23–47

    Article  Google Scholar 

  5. Hetzel DJS, Crocos PJ, Davis GP, Moore SS, Preston NC (2000) Response to selection and heritability for growth in the Kuruma prawn, Penaeus japonicus. Aquaculture 181:215–223

    Article  Google Scholar 

  6. Argue BJ, Arce SM, Lotz JM, Moss SM (2002) Selective breeding of Pacific white shrimp (Litopenaeus vannamei) for growth and resistance to Taura Syndrome Virus. Aquaculture 204:447–460

    Article  Google Scholar 

  7. Goyard E, Patrois J, Reignon JM, Vanaa V, Dufour R, Bedier E (1999) IFREMER’s shrimp genetics program. Glob Aquac Advocate 2(6):26–28

    Google Scholar 

  8. Fjalestad KT, Gjedrem T, Carr WH, Sweeney JN (1997) Final report: the shrimp breeding program, selective breeding of Penaeus vannamei. The Oceanic Institute, Waimanalo

    Google Scholar 

  9. Moore SS, Whan V, Davis GP, Byrne K, Hetzel DJS, Preston N (1999) The development and application of genetic markers for the Kuruma prawn Penaeus japonicus. Aquaculture 173:19–32

    Article  CAS  Google Scholar 

  10. Li J, Liu P, He YY, Song QS, Mu NH, Wang QY (2005) Artificial selection in the new breed of Fenneropenaeus chinensis named Huanghai No.1 based on fast growth trait. J Fish China 29(1):1–5

    Google Scholar 

  11. He YY, Liu P, Li J, Kong J, Wang QY (2004) Analysis of genetic structure in the first cultured stock and the sixth cultured stock of Fenneropenaeus chinensis. J Fish Sci China 11(6):572–575

    CAS  Google Scholar 

  12. He YY, Liu P, Li J, Kong J, Wang QY (2005) RAPD analysis of genetic diversities in the fast growth populations of Fenneropenaeus chinensis. Prog Fish Sci 26(4):8–13

    Google Scholar 

  13. Zhang TS, Wang QY, Liu P, Li J, Kong J (2005) Genetic diversity analysis on selected populations of shrimp Fenneropenaeus chinensis by microsatellites. Oceanol Limnol Sin 36(1):72–80

    CAS  Google Scholar 

  14. Li ZX, Li J, Wang QY, He YY, Liu P (2006) The effects of selective breeding on the genetic structure of shrimp Fenneropenaeus chinensis populations. Aquaculture 258:278–282

    Article  Google Scholar 

  15. Li ZX, Li J, Wang QY, He YY, Liu P (2006) AFLP-based genetic linkage map of marine shrimp Penaeus (Fenneropenaeus) chinensis. Aquaculture 261:463–472

    Article  CAS  Google Scholar 

  16. Liu B, Wang QY, Li J, Liu P, He YY (2010) A genetic linkage map of marine shrimp Penaeus (Fenneropenaeus) chinensis based on AFLP, SSR, and RAPD markers. Chin J Oceanol Limnol 28(4):815–825

    Article  Google Scholar 

  17. Lv JJ, Liu P, Wang Y, Gao BQ, Chen P, Li J (2013) Transcriptome analysis of Portunus trituberculatus in response to salinity stress provides insights into the molecular basis of osmoregulation. PLoS ONE 8(12):1–15

    Google Scholar 

  18. Hou R, Bao ZM, Wang S, Su HL, Li Y, Du HX, Hu JJ, Wang S, Hu XL (2011) Transcriptome sequencing and De Novo Analysis for Yesso scallop (Patinopecten yessoensis) using 454 GS FLX. PLoS ONE 6(6):1–7

    Article  Google Scholar 

  19. Huan P, Wang HX, Liu BZ (2012) Transcriptomic analysis of the clam Meretrix meretrix on different larval stages. Mar Biotechnol 14:69–78

    Article  CAS  PubMed  Google Scholar 

  20. Zeng DG, Chen XL, Xie DX, Zhao YZ, Yang CL, Li YM, Ma N, Peng M, Yang Q, Liao ZP, Wang H, Chen XH (2013) Transcriptome analysis of pacific white shrimp (Litopenaeus vannamei) hepatopancreas in response to Taura Syndrome Virus (TSV) experimental infection. PLoS ONE 8(2):e57515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Li SH, Zhang XJ, Sun Z, Li FH, Xiang JH (2013) Transcriptome analysis on Chinese shrimp Fenneropenaeus chinensis during WSSV acute infection. PLoS ONE 8(3):e58627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Emrich SJ, Barbazuk WB, Li L, Schnable PS (2007) Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Res 17(1):69–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Vega-Arreguín JC, Ibarra-Laclette E, Jiménez-Moraila B, Martínez O, Vielle-Calzada JP (2009) Deep sampling of the Palomero maize transcriptome by a high throughput strategy of pyrosequencing. BMC Genomics 10:299

    Article  PubMed  PubMed Central  Google Scholar 

  24. Hillier LW, Reinke V, Green P, Hirst M, Marra MA (2009) Massively parallel sequencing of the polyadenylated transcriptome of C. elegans. Genome Res 19:657–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Barakat A, Diloreto DS, Zhang Y, Smith C, Baier K (2009) Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chesnut (Castanea mollissima) in response to the chestnut blight infection. BMC Plant Biol 9:51

    Article  PubMed  PubMed Central  Google Scholar 

  26. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 17:1636–1647

    Article  CAS  PubMed  Google Scholar 

  27. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, Colbourne JK, Willis BL, Matz MV (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 12(10):219

    Article  Google Scholar 

  28. O’Neil ST, Dzurisim JD, Carmichael RD, Lobo NF, Emrich SJ (2010) Population-level transcriptome sequencing of nonmodel organisms Erynnis propertius and Papilio zelicaon. BMC Genomics 11:310

    Article  PubMed  PubMed Central  Google Scholar 

  29. Chou HH, Holmes MH (2001) DNA sequence quality trimming and vector removal. Bioinformatics 17:1093–1104

    Article  CAS  PubMed  Google Scholar 

  30. Ning Z, Caccamo M, Mullikin JC (2005) ssahaSNP a polymorphism detection tool on a whole genome scale. In: 2005 IEEE computational systems bioinformatics conference-workshops, pp 251–254

  31. 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(18):3674–3676

    Article  CAS  PubMed  Google Scholar 

  32. Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics. doi:10.1155/2008/619832

    PubMed  PubMed Central  Google Scholar 

  33. Kanehisa M, Goto S (2000) KEGG Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen HZ, Li J, Wang QY, He YY, Li JT, Dai FY, Wang XZ (2011) Sequence-related amplified polymorphism markers related to stress resistance traits in Huanghai No.1 Fenneropenaeus chinensis. J Fish Sci China 18(6):1243–1249

    CAS  Google Scholar 

  35. Morozova O, Hirst M, Marra MA (2009) Applications of new sequencing technologies for transcriptome analysis. Annu Rev Genomics Hum Genet 10:135–151

    Article  CAS  PubMed  Google Scholar 

  36. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GS FLX. BMC Genomics 10:219

    Article  PubMed  PubMed Central  Google Scholar 

  37. Parchman TL, Geist KS, Grahnen JA, Benkman CW, Buerkle CA (2010) Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics 16(11):180

    Article  Google Scholar 

  38. Kaur S, Cogan NO, Pembleton LW, Shinozuka M, Savin KW, Materne M, Forster JW (2011) Transcriptome sequencing of lentil based on second-generation technology permits large-scale unigene assembly and SSR marker discovery. BMC Genomics 12:265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Luo H, Sun C, Sun Y, Wu Q, Li Y, Song J, Niu Y, Cheng X, Xu H, Li C, Liu J, Steinmetz A, Chen S (2011) Analysis of the transcriptome of Panax notoginseng root uncovers putative triterpene saponin-biosynthetic genes and genetic markers. BMC Genomics 12(Suppl 1):S5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mcpherron AC, Lawler AM, Lee S (1997) Regulation of skeletal muscle mass in mice by a new TGF-βsuperfamily member. Nature 387:83–90

    Article  CAS  PubMed  Google Scholar 

  41. Zhao HB, Peng K, Wang YF, Hu W (2006) Progress of studies on myostatin of fish. Acta Hydrobiol Sin 30(2):227–231

    CAS  Google Scholar 

  42. Xu JY, Chen SL (2008) Cloning and expression analysis of the myostatin (MSTN) gene in Paralichthys olivaceus. J Fish China 32(4):497–506

    CAS  Google Scholar 

  43. Bachere E (2000) Shrimp immunity and disease control. Aquaculture 191(1–3):1–2

    Article  Google Scholar 

  44. Andriantahina F, Liu X, Feng T, Xiang J (2013) Current status of genetics and genomics of reared Penaeid shrimp: information relevant to access and benefit sharing. Mar Biotechnol 4:399–412

    Article  Google Scholar 

  45. Du ZQ, Ciobanu DC, Onteru SK, Gorbach D, Mileham AJ, Jaramillo G, Rothschild MF (2010) A gene-based SNP linkage map for pacific white shrimp, Litopenaeus vannamei. Anim Genet 41:286–294

    Article  CAS  PubMed  Google Scholar 

  46. You EM, Liu KF, Huang SW, Chen M, Groumellec ML, Fann SJ, Yu HT (2010) Construction of integrated genetic linkage maps of the tiger shrimp (Penaeus monodon) using microsatellite and AFLP markers. Anim Genet 41:365–376

    CAS  PubMed  Google Scholar 

  47. Lin FJ, Liu Y, Sha Z, Tsang LM, Chu KH, Chan TY, Liu R, Cui Z (2012) Evolution and phylogeny of the mud shrimps (Crustacea: Decapoda) revealed from complete mitochondrial genomes. BMC Genomics 13:631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Alejandra CS, Rogerio RS, Teresa GG, Jorge HL, Alma BP, Adriana MA, Gloria YP (2007) Transcriptome analysis of gills from the white shrimp Litopenaeus vannamei infected with White Spot Syndrome Virus. Fish Shellfish Immunol 23:459–472

    Article  Google Scholar 

  49. Supungul P, Klinbunga S, Pichyangkura R, Jitrapakdee S, Hirono I, Aoki T (2002) Identification of immune-related genes in hemocytes of black tiger shrimp (Penaeus monodon). Mar Biotechnol 4:487–494

    Article  CAS  PubMed  Google Scholar 

  50. Siriporn P, Ratree W, Sureerat T, Arthit C, Anchalee T (2008) Abundantly expressed transcripts in the lymphoid organ of the black tiger shrimp, Penaeus monodon, and their implication in immune function. Fish Shellfish Immunol 25:485–493

    Article  Google Scholar 

  51. de Lorgeril J, Saulnier D, Janech MG, Gueguen Y, Bachere E (2005) Identification of genes that are differentially expressed in hemocytesof the Pacific blue shrimp (Litopenaeus stylirostris) surviving an infection with Vibrio penaeicida. Physiol Genomics 21:174–183

    Article  PubMed  Google Scholar 

  52. Dostert C, Jounaguy E, Irving P, Troxler L, Galiana-Arnoux D, Hetru C, Hoffmann JA, Imler JL (2005) The Jak-STAT signaling pathway is required but not sufficient four the antiviral response of drosophila. Nat Immunol 6:946–953

    Article  CAS  PubMed  Google Scholar 

  53. Chen WY, Ho KC, Leu JH, Liu KF, Wang HC, Kou GH, Lo CF (2008) WSSV infection activates STAT in shrimp. Dev Comp Immunol 32:1142–1150

    Article  CAS  PubMed  Google Scholar 

  54. Jonak C, Okrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signaling. Curr Opin Plant Biol 5(5):415–424

    Article  CAS  PubMed  Google Scholar 

  55. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415(6875):977–983

    Article  CAS  PubMed  Google Scholar 

  56. Sanges D, Cosma MP (2010) Reprogramming cell fate to pluripotency: the decision-making signaling pathways. Int J Dev Biol 54(11–12):1575–1587

    Article  CAS  PubMed  Google Scholar 

  57. Yan H, Zhang S, Li CZ, Chen YH, Chen YG, Weng SP, He JG (2013) Molecular characterization and function of a p38 MAPK gene from Litopenaeus vannamei. Fish Shellfish Immunol 34:1421–1431

    Article  CAS  PubMed  Google Scholar 

  58. He YY, Liu P, Li J, Wang QY (2007) Growth traits related SCAR markers in Fenneropenaeus chinensis. Oceanol Limnol Sin 38(1):42–48

    CAS  Google Scholar 

  59. Chen S, Luo H, Li Y, Sun Y, Wu Q, Niu Y, Song J, Lv A, Zhu Y, Sun C, Steinmetz A, Qian Z (2011) 454 EST analysis detects genes putatively involved in ginsenoside biosynthesis in Panax ginseng. Plant Cell Rep 30(9):1593–1601

    Article  CAS  PubMed  Google Scholar 

  60. Gorbach DM, Hu ZL, Du ZQ, Rothschild MF (2010) Mining ESTs to determine the usefulness of SNPs across shrimp species. Anim Biotechnol 21:100–103

    Article  CAS  PubMed  Google Scholar 

  61. Kim WJ, Jung HT, Gaffney PM (2011) Development of type I genetic markers from expressed sequence tags in highly polymorphic species. Mar Biotechnol 13:127–132

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Independent Innovation of Shandong Province (Grant No. 2013CXC80202), the National Natural Science Foundation of China (Grant No. 31172401), and the China Agriculture Research System (Grant No. CARS-47).

Author information

Authors and Affiliations

  1. Key Laboratory for Sustainable Utilization of Marine Fisheries, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Yuying He, Ping Liu, Qingyin Wang & Jian Li

  2. College of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, 266109, China

    Zhaoxia Li

Authors
  1. Yuying He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhaoxia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ping Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qingyin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, Y., Li, Z., Liu, P. et al. Transcriptic analysis of Huanghai No. 1 strain of Chinese shrimp Fenneropenaeus chinensis using 454 pyrosequencing. Fish Sci 82, 327–336 (2016). https://doi.org/10.1007/s12562-015-0961-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-015-0961-9

Keywords

Search

Navigation