Advertisement

A comparative transcriptomic analysis in late embryogenesis of the red claw crayfish Cherax quadricarinatus

  • Yan Wang
  • Baojie Wang
  • Xuqing Shao
  • Mei Liu
  • Keyong Jiang
  • Mengqiang WangEmail author
  • Lei WangEmail author
Original Article

Abstract

The red claw crayfish (Cherax quadricarinatus) is an emerging and important commercial species in several countries, and is also a potential biological model in crustacean biology. However, its molecular embryonic development mechanism remains largely unknown because of a lack of genomic resources and systematic research. A comprehensive and integrated transcriptomic analysis is necessary to reveal the cell biological function, gene expression profiles, and embryo patterning that occur during embryogenesis. In the present study, transcriptomic profiles of C. quadricarinatus embryos during three developmental stages were investigated by high-throughput Illumina sequencing technology, and the genes related to development were further analyzed. In total, 49,436 unigenes were assembled and clustered, in which 13,727 were annotated in the Nonredundant database, 5087 were classified based on Gene Ontology annotations, and 2735 were associated with 189 Kyoto Encyclopedia of Genes and Genomes pathways. Furthermore, gene expression differences among the embryos stages were analyzed, and 6658 differentially expressed genes (DEGs) were identified. In total, 3300, 5211, and 1262 DEGs were identified between the eye pigments forming stage (EP) and prepare-hatching stage (PH), EP and larvae (L), as well as PH and L; meanwhile, 1595, 2540 and 680 DEGs were annotated, respectively. The fundamental developmental genes related to apoptosis, neurogenesis, and segmentation, as well as signaling pathways related to Hedgehog, MAPK, Wnt, TGF-β and Notch, showed higher expression during the EP stage than in other two stages, indicating that the EP stage has more active biological processes than the latter stages. This transcriptome studies gene expression at different stages of embryonic development and the datasets provide a basis for understanding crustacean developmental biology and guiding seedling production.

Keywords

Cherax quadricarinatus Embryonic development Transcriptome 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (U1706209) and the Marine S&T Fund of Shandong Province for National Laboratory for Marine Science and Technology (2018SDKJ0502-2).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

438_2019_1621_MOESM1_ESM.jpg (176 kb)
Supplementary Fig. S1. The length distribution of unigenes. The X axis represents the different length intervals of unigenes. The Y axis represents the number of unigenes in each length interval. (JPEG 175 kb)
438_2019_1621_MOESM2_ESM.jpg (389 kb)
Supplementary Fig. S2. KEGG annotation of the total unigenes. (JPEG 388 kb)
438_2019_1621_MOESM3_ESM.jpg (163 kb)
Supplementary Fig. S3. Up- and downregulated genes of the EP, PH, and L stage embryos. (A) Comparison of upregulated genes. (B) Comparison of downregulated genes. (JPEG 162 kb)
438_2019_1621_MOESM4_ESM.jpg (8.7 mb)
Supplementary Fig. S4. GO classification of DEGs. (A) EP vs PH. (B) EP vs L. (C) PH vs L. (JPEG 8872 kb)
438_2019_1621_MOESM5_ESM.docx (20 kb)
Supplementary material 5 (DOCX 20 kb)

References

  1. Abdu URI, Yehezkel G, Sagi A (2000) Oocyte development and polypeptide dynamics during ovarian maturation in the red-claw crayfish Cherax quadricarinatus. Int J Invertebr Reprod 37(1):75–83CrossRefGoogle Scholar
  2. Anson KJ, Rouse DB (2010) Effects of salinity on hatching and post-hatch survival of the Australian red claw crayfish Cherax quadricarinatus. J World Aquaculture Soc 25(2):277–280CrossRefGoogle Scholar
  3. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284(5415):770–776PubMedCrossRefPubMedCentralGoogle Scholar
  4. Blander JM, Medzhitov R (2006) On regulation of phagosome maturation and antigen presentation. Nat Immunol 7(10):1029–1035PubMedCrossRefPubMedCentralGoogle Scholar
  5. Challa M, Malladi S, Pellock BJ, Dresnek D, Varadarajan S, Yin YW, White K, Bratton SB (2007) Drosophila Omi, a mitochondrial-localized IAP antagonist and proapoptotic serine protease. EMBO J 26(13):3144–3156PubMedPubMedCentralCrossRefGoogle Scholar
  6. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127(3):469–480PubMedCrossRefGoogle Scholar
  7. Dearden PK, Wilson MJ, Sablan L, Osborne PW, Havler M, McNaughton E, Kimura K, Milshina NV, Hasselmann M, Gempe T, Schioett M, Brown SJ, Elsik CG, Holland PWH, Kadowaki T, Beye M (2006) Patterns of conservation and change in honey bee developmental genes. Genome Res 16(11):1376–1384PubMedPubMedCentralCrossRefGoogle Scholar
  8. Dixit E, Boulant S, Zhang YJ, Lee ASY, Odendall C, Shum B, Hacohen N, Chen ZJ, Whelan SP, Fransen M, Nibert ML, Superti-Furga G, Kagan JC (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141(4):668–681PubMedPubMedCentralCrossRefGoogle Scholar
  9. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516PubMedPubMedCentralCrossRefGoogle Scholar
  10. Fang DA, Wang Q, Wang J, He L, Liu LH, Wang Y (2011) A novel DDX5 gene in the freshwater crayfish Cherax quadricarinatus is highly expressed during ontogenesis and spermatogenesis. Genet Mol Res 10(4):3963–3975PubMedCrossRefGoogle Scholar
  11. Flynn JL, Chan J (2001) Immunology of tuberculosis. Annu Rev Immunol 19:93–129PubMedCrossRefGoogle Scholar
  12. Garcia-Guerrero M, Hendrickx ME, Villarreal H (2003a) Description of the embryonic development of Cherax quadricarinatus (Von Martens, 1868) (Decapoda, Parastacidae), based on the staging method. Crustaceana 76:269–280CrossRefGoogle Scholar
  13. Garcia-Guerrero M, Villarreal H, Racotta IS (2003b) Effect of temperature on lipids, proteins, and carbohydrates levels during development from egg extrusion to juvenile stage of Cherax quadricarinatus (Decapoda: Parastacidae). Comp Biochem Physiol Part A Mol Integr Physiol 135(1):147–154CrossRefGoogle Scholar
  14. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M (2001) The phagosome proteome: insight into phagosome functions. J Cell Biol 152(1):165–180PubMedPubMedCentralCrossRefGoogle Scholar
  15. Ghanawi J, Saoud IP (2012) Molting, reproductive biology, and hatchery management of redclaw crayfish Cherax quadricarinatus (von Martens 1868). Aquaculture 358:183–195CrossRefGoogle Scholar
  16. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644U130CrossRefGoogle Scholar
  17. Hartenstein AY, Rugendorff A, Tepass U, Hartenstein V (1992) The function of the neurogenic genes during epithelial development in the Drosophila Embryo. Development 116(4):1203–1220PubMedGoogle Scholar
  18. Harzsch S, Miller J, Benton J, Dawirs RR, Beltz B (1998) Neurogenesis in the thoracic neuromeres of two crustaceans with different types of metamorphic development. J Exp Biol 201(17):2465–2479PubMedGoogle Scholar
  19. Hettema EH, Motley AM (2009) How peroxisomes multiply. J Cell Sci 122(14):2331–2336PubMedPubMedCentralCrossRefGoogle Scholar
  20. Holdich DM (2002) Biology of freshwater crayfish. Blackwell Science, OxfordGoogle Scholar
  21. Igaki T, Suzuki Y, Tokushige N, Aonuma H, Takahashi R, Miura M (2007) Evolution of mitochondrial cell death pathway: proapoptotic role of HtrA2/Omi in Drosophila. Biochem Biophys Res Commun 356(4):993–997PubMedCrossRefPubMedCentralGoogle Scholar
  22. Ingham PW, McMahon AP (2001) Hedgehog signaling in animal development: paradigms and principles. Gene Dev 15(23):3059–3087PubMedCrossRefPubMedCentralGoogle Scholar
  23. Isaksson A, Peverali FA, Kockel L, Mlodzik M, Bohmann D (1997) The deubiquitination enzyme fat facets negatively regulates RTK/Ras/MAPK signalling during Drosophila eye development. Mech Dev 68(1–2):59–67PubMedCrossRefPubMedCentralGoogle Scholar
  24. Jarman AP, Grau Y, Jan LY, Jan YN (1993) Atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous-system. Cell 73(7):1307–1321PubMedCrossRefGoogle Scholar
  25. Jones CM (1995) Production of juvenile redclaw crayfish, Cherax quadricarinatus (von Martens) (Decapoda, Parastacidae). 1. Development of hatchery and nursery procedures. Aquaculture 138(1–4):221–238CrossRefGoogle Scholar
  26. Kaitetzidou E, Katsiadaki I, Lagnel J, Antonopoulou E, Sarropoulou E (2019) Unravelling paralogous gene expression dynamics during three-spined stickleback embryogenesis. Sci Rep 9:3752PubMedPubMedCentralCrossRefGoogle Scholar
  27. Kang PF, Mao B, Fan C, Wang YF (2019) Transcriptomic information from the ovaries of red swamp crayfish (Procambarus clarkii) provides new insights into development of ovaries and embryos. Aquaculture 505:333–343CrossRefGoogle Scholar
  28. Kurata S, Ariki S, Kawabata S (2006) Recognition of pathogens and activation of immune responses in Drosophila and horseshoe crab innate immunity. Immunobiology 211(4):237–249PubMedCrossRefGoogle Scholar
  29. Levi T, Barki A, Hulata G, Karplus I (1999) Mother-offspring relationships in the red-claw crayfish Cherax quadricarinatus. J Crustacean Biol 19(3):477–484CrossRefGoogle Scholar
  30. Li YD, Hui M, Cui ZX, Liu Y, Song CW, Shi GH (2015) Comparative transcriptomic analysis provides insights into the molecular basis of the metamorphosis and nutrition metabolism change from zoeae to megalopae in Eriocheir sinensis. Comp Biochem Phys D 13:1–9Google Scholar
  31. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810PubMedCrossRefPubMedCentralGoogle Scholar
  32. Luo W, Zhao YL, Zhou ZL, An CG, Ma Q (2008) Digestive enzyme activity and mRNA level of trypsin in embryonic redclaw crayfish, Cherax quadricarnatus. Chin J Oceanol Limnol 26(1):62–68CrossRefGoogle Scholar
  33. Macaranas JM, Mather PB, Hoeben P, Capra MF (1995) Assessment of genetic variation in wild populations of the redclaw crayfish (Cherax quadricarinatus, von Martens 1868) by means of allozyme and RAPD-PCR markers. Mar Freshw Res 46(8):1217–1228CrossRefGoogle Scholar
  34. Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793PubMedCrossRefPubMedCentralGoogle Scholar
  35. Martin-Blanco E (2000) p38 MAPK signalling cascades: ancient roles and new functions. BioEssays 22(7):637–645PubMedCrossRefPubMedCentralGoogle Scholar
  36. Massague J, Blain SW, Lo RS (2000) TGF beta signaling in growth control, cancer, and heritable disorders. Cell 103(2):295–309PubMedCrossRefPubMedCentralGoogle Scholar
  37. McGinnis N, Ragnhildstveit E, Veraksa A, McGinnis W (1998) A cap ‘n’ collar protein isoform contains a selective Hox repressor function. Development 125(22):4553–4564PubMedPubMedCentralGoogle Scholar
  38. Meng F, Zhao Y, Chen L, Gu Z, Xu G, Liu Q (2000) The study on the embryonic development of Cherax quadricarinatus I. Morphogenesis of external structures of embryo. Zool Res 21(6):468–472Google Scholar
  39. Meng F, Zhao Y, Chen L, Gu Z, Xu G, Liu Q (2001) Embryonic development of redclaw crayfish Cherax quadricarinatus: II. Development of Digestive System. Zool Res 22(5):383–387Google Scholar
  40. Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628PubMedPubMedCentralCrossRefGoogle Scholar
  41. Patterson GI, Padgett RW (2000) TGFβ-related pathways: roles in Caenorhabditis elegans development. Trends Genet 16(1):27–33PubMedCrossRefGoogle Scholar
  42. Sellars MJ, Trewin C, McWilliam SM, Glaves RSE, Hertzler PL (2015) Transcriptome profiles of Penaeus (Marsupenaeus) japonicus animal and vegetal half-embryos: identification of sex determination, germ line, mesoderm, and other developmental genes. Mar Biotechnol 17(3):252–265PubMedCrossRefGoogle Scholar
  43. Shi YG, Massague J (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113(6):685–700CrossRefGoogle Scholar
  44. Simon S, Sagasser S, Saccenti E, Brugler MR, Schranz ME, Hadrys H, Amato G, DeSalle R (2017) Comparative transcriptomics reveal developmental turning points during embryogenesis of a hemimetabolous insect, the damselfly Ischnura elegans. Sci Rep UK 7:13547CrossRefGoogle Scholar
  45. Stevens BG (2006) Embryo development and morphometry in the blue king crab Paralithodes platypus studied by using image and cluster analysis. J Shellfish Res 25(2):569–576CrossRefGoogle Scholar
  46. Ten Dijke PT, Goumans MJ, Itoh F, Itoh S (2002) Regulation of cell proliferation by Smad proteins. J Cell Physiol 191(1):1–16PubMedCrossRefGoogle Scholar
  47. Vilpoux K, Sandeman R, Harzsch S (2006) Early embryonic development of the central nervous system in the Australian crayfish and the Marbled crayfish (Marmorkrebs). Dev Genes Evol 216(4):209–223PubMedCrossRefGoogle Scholar
  48. Wang LM, Zuo D, Lv WW, Wang DL, Liu AJ, Zhao YL (2013) Characterization of Cdc2 kinase in the red claw crayfish (Cherax quadricarinatus): evidence for its role in regulating oogenesis. Gene 515(2):258–265PubMedCrossRefGoogle Scholar
  49. Wang LM, Lv WW, Zuo D, Dong ZJ, Zhao YL (2015) Characteristics of Cyclin B and its potential role in regulating oogenesis in the red claw crayfish (Cherax quadricarinatus). Genet Mol Res 14(3):10786–10798PubMedCrossRefGoogle Scholar
  50. Wei JK, Zhang XJ, Yu Y, Huang H, Li FH, Xiang JH (2014) Comparative transcriptomic characterization of the early development in pacific white shrimp Litopenaeus vannamei. PloS One 9(9):e106201PubMedPubMedCentralCrossRefGoogle Scholar
  51. Xiong YM, Hu L, Yan ZH, Zhang JE, Li HY (2018) Transcriptomic analysis of embryo development in the invasive snail Pomacea canaliculata. J Molluscan Stud 84:233–239CrossRefGoogle Scholar
  52. Yeh HS, Rouse DB (2010) Indoor spawning and egg development of the red claw crayfish Cherax quadricarinatus. J World Aquacult Soc 25(2):297–302CrossRefGoogle Scholar
  53. Yin A, Pan LL, Zhang XW, Wang L, Yin YX, Jia SG, Liu WF, Xin CQ, Liu K, Yu XG, Sun GY, Al-hudaib K, Hu SN, Al-Mssallem IS, Yu J (2015) Transcriptomic study of the red palm weevil Rhynchophorus ferrugineus embryogenesis. Insect Sci 22(1):65–82PubMedCrossRefGoogle Scholar
  54. Zhao Y, Meng F, Chen L, Zhimin GU, Guxin XU, Liu Q (2000) Effects of different gradient temperatures on embryonic development of the Cherax Quadricarinatus (Crustacea, Decapoda). J Lake Sci 12(1):59–62CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.CAS Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Laboratory for Marine Biology and BiotechnologyNational Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.Research Platform for Marine Molecular Biotechnology, National Laboratory for Marine Science and TechnologyQingdaoChina
  5. 5.CAS Center for Ocean Mega-Science, Chinese Academy of SciencesQingdaoChina
  6. 6.Shandong Cigna Detection Technology Co., LtdQingdaoChina

Personalised recommendations