Skip to main content
Log in

Characterization of Embryo Transcriptome of Gynogenetic Olive Flounder Paralichthys olivaceus

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Olive flounder Paralichthys olivaceus is an important commercially cultured marine flatfish in China, Korea, and Japan. Gynogenesis, via meiogynogenesis and mitogynogenesis, shows advantages in breeding and sex control, but the low survival rate, especially for mitogynogenesis, limits its application. In this study, we sequenced the embryo transcriptomes of gynogenetic haploid, meiogynogenetic diploid, mitogynogenetic diploid, and common diploid flounder and investigated their respective genetic characteristics by analyzing differentiated expressed genes. Compared with common diploid, the gynogenetic haploid showed significant downregulation in notch signaling and wingless-related integration site (Wnt) signaling pathways, which may be the source of haploid syndrome. In both meiogynogenesis and mitogynogenesis, several upregulated genes including complement C3, formin-2, and intelectin may be related to increased survival compared to the haploid. The downregulation of immune system and energy metabolism-related genes caused retarded development of gynogenetic diploids compared with the common diploid. These data provided new and important information for application of artificially induced gynogenesis to aquaculture.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

  • Arai K (2001) Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 197:205–228

  • 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 

  • Belin BJ, Lee T, Mullins RD (2015) DNA damage induces nuclear actin filament assembly by formin-2 and spire-1/2 that promotes efficient DNA repair. Elife 4:e07735

    PubMed  PubMed Central  Google Scholar 

  • Borelli V, Vita F, Shankar S, Soranzo MR, Banfi E, Scialino G, Brocchetta C, Zabucchi G (2003) Human eosinophil peroxidase induces surface alteration, killing, and lysis of Mycobacterium tuberculosis. Infect Immun 71: 605--613

  • Cherfas NB (1975) Study of radiation induced diploid gynogenesis in the carp 1: experiments on the mass production of diploid gynogenetic progeny. Genetika 11:78–86

    CAS  PubMed  Google Scholar 

  • Clevers H (2006) Wnt/β-catenin signaling in development and disease. Cell 127:469–480

    Article  CAS  PubMed  Google Scholar 

  • Corley-Smith GE, Lim CJ, Brandhorst BP (1996) Production of androgenetic zebrafish (Danio rerio. Genetics 142:1265–1276

    CAS  PubMed  PubMed Central  Google Scholar 

  • Del Valle G, Taniguchi N, Tsujimura A (1994) Reduced variation of physiological traits in ayu clones, Plecoglossus altivelis. Fish Sci 60:523–526

    CAS  Google Scholar 

  • Del Valle G, Taniguchi N, Tsujimura A (1996) Genetic differences in some haematological traits of communally reared clonal ayu, Plecoglossus altivelis Temminck & Schlegel, under stressed and non-stressed conditions. Aquac Res 27:787–793

    Article  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, 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 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graw J (1997) The crystallins: genes, proteins and diseases. Biol Chem 378:1331–1348

    CAS  PubMed  Google Scholar 

  • Honda S, Kashiwagi M, Miyamoto K, Takei Y, Hirose S (2000) Multiplicity, structures, and endocrine and exocrine natures of eel fucose-binding lectins. J Biol Chem 275:33151–33157

    Article  CAS  PubMed  Google Scholar 

  • Khatib H (2007) Is it genomic imprinting or preferential expression? BioEssays 29:1022–1028

    Article  CAS  PubMed  Google Scholar 

  • Komen H, Thorgaard GH (2007) Androgenesis, gynogenesis and the production of clones in fishes: a review. Aquaculture 269:150–173

    Article  Google Scholar 

  • Kono T, Obata Y, Wu Q, Niwa K, Ono Y, Yamamoto Y, Park ES, Seo JS, Ogawa H (2004) Birth of parthenogenetic mice that can develop to adulthood. Nature 428:860–864

    Article  CAS  PubMed  Google Scholar 

  • Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, Pellman D, Maas R, Leder P (2002) Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4:921–928

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Li SZ, Li Z, Wang Y, Li XY, Zhong JX, Zhang XJ, Zhang J, Zhou L, Gui JF (2015) Complete depletion of primordial germ cells in an all-female fish leads to sex-biased gene expression alteration and sterile all-male occurrence. BMC Genomics 16:971

    Article  PubMed  PubMed Central  Google Scholar 

  • MacDonald BT, Tamai K, He X (2009) Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makino S, Ozima Y (1943) Formation of the diploid egg nucleus due to suppression of the second maturation division, induced by refrigeration of fertilized eggs of common carp, Cyprinus carpio L. Cytologia 13:55–60

    Article  Google Scholar 

  • Mei J, Gui JF (2015) Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Sci China Life Sci 58:124–136

    Article  CAS  PubMed  Google Scholar 

  • Nagy A, Rajki K, Horvath L, Csanyi V (1978) Investigation on carp Cyprinus carpio gynogenesis. J Fish Biol 13:215–224

    Article  Google Scholar 

  • Neaves WB, Baumann P (2011) Unisexual reproduction among vertebrates. Trends Genet 27:81–88

    Article  CAS  PubMed  Google Scholar 

  • Purdom CE (1969) Radiation induced gynogenesis and androgenesis in fish. Heredity 24:431–444

    Article  CAS  PubMed  Google Scholar 

  • Schulze SK, Kanwar R, Gölzenleuchter M, Therneau TM, Beutler AS (2012) SERE: single-parameter quality control and sample comparison for RNA-Seq. BMC Genomics 13:524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sfyroera G, Ricklin D, Reis ES, Chen H, Wu EL, Kaznessis YN, Ekdahl KN, Nilsson B, Lambris JD (2015) Rare loss-of-function mutation in complement component C3 provides insight into molecular and pathophysiological determinants of complement activity. J Immunol 197:3305–3316

    Article  Google Scholar 

  • Streisinger G, Walker C, Dower N, Knauber D, Singer F (1981) Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291:293–296

    Article  CAS  PubMed  Google Scholar 

  • Suzuki R, Oshiro T, Nakanishi T (1985) Survival, growth, and fertility of gynogenetic diploids induced in the cyprinid loach, Misgurnus anguillicaudatus. Aquaculture 48:45–55

    Article  Google Scholar 

  • Suzuki YA, Shin K, Lönnerdal B (2001) Molecular cloning and functional expression of a human intestinal lactoferrin receptor. Biochemistry 40:15771–15779

    Article  CAS  PubMed  Google Scholar 

  • Thorgaard GH, Allendorf FW, Knudsen KL (1983) Gene–centromere mapping in rainbow trout: high interference over long map distances. Genetics 103:771–783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuji S, Uehori J, Matsumoto M, Suzuki Y, Matsuhisa A, Toyoshima K, Seya T (2001) Human intelectin is a novel soluble lectin that recognizes galactofuranose in carbohydrate chains of bacterial cell wall. J Biol Chem 276:23456–23463

    Article  CAS  PubMed  Google Scholar 

  • Ulrich M, Petre A, Youhnovski N, Prömm F, Schirle M, Schumm M, Pero RS, Doyle A, Checkel J, Kita H, Thiyagarajan N, Acharya KR, Schmid-Grendelmeier P, Simon HU, Schwarz H, Tsutsui M, Shimokawa H, Bellon G, Lee JJ, Przybylski M, Döring G (2008) Post-translational tyrosine nitration of eosinophil granule toxins mediated by eosinophil peroxidase. J Biol Chem 283:28629–28640

  • Wang W, You F, Xu J, Sun W, Zhu X, Gao T, Zhang P (2008) Genetic analysis of meio- and mito-gynogenetic stocks of Paralichthys olivaceus with microsatellite markers. ACTA Oceanol Sin 27:149–156

  • Wang ZW, Zhu HP, Wang D, Jiang FF, Guo W, Zhou L, Gui JF (2011) A novel nucleo-cytoplasmic hybrid clone formed via androgenesis in polyploid gibel carp. BMC Res Notes 4:82

  • Weadick CJ, Chang BS (2009) Molecular evolution of the βγ lens crystallin superfamily: evidence for a retained ancestral function in γN crystallins? Mol Biol Evol 26:1127–1142

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto E (1999) Studies on sex-manipulation and production of cloned populations in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173:235–246

    Article  Google Scholar 

  • You F, Liu J, Wang X, Xu Y, Huang R, Zhang P (2001) Study on embryonic development and early growth of triploid and gynogenetic diploid left-eyed flounder, Paralichthys olivaceus (T. et S.). Chin J Oceanol Limnol 19:147–151

    Article  Google Scholar 

  • You F, Xu J, Ni J, Sun W, Zhu X, Xu D, Xu Y, Zhang P (2008) Study on artificial induction of mitogynogenetic diploid in Paralichthys olivaceus. Chin High Technol Lett 18:874–880 (in Chinese)

  • Yuan X, Wu H, Han N, Xu H, Chu Q, Yu S, Chen Y, Wu K (2014) Notch signaling and EMT in non-small cell lung cancer: biological significance and therapeutic application. J Hematol Oncol 7:87

  • Zhang X, Hou J, Wang G, Jiang H, Wang Y, Sun Z, Jiang X, Yu Q, Liu H (2015a) Gonadal transcriptome analysis in sterile double haploid Japanese flounder. PLoS One 10:e0143204

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Sun M, Zhou L, Li Z, Liu Z, Li XY, Liu XL, Liu W, Gui JF (2015b) Meiosis completion and various sperm responses lead to unisexual and sexual reproduction modes in one clone of polyploid Carassius gibelio. Sci Rep 5:10898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong HL, Liu HJ, Zhang SK, Jiang XF, Wang YF (2009) Comparison of embryonic development in gynogenetic and diploid barfin flounder (Verasper moseri). Fish Sci 28:752–756

    Google Scholar 

  • Zhu XP, You F, Zhang PJ, Xu YL, Xu JH (2006) Effects of cold shock on microtubule organization and cell cycle in gynogenetically activated eggs of olive flounder (Paralichthys olivaceus). Mar Biotechnol l8:312–318

Download references

Acknowledgments

This work was supported by the grants from the National Natural Science Foundation of China (Nos. 41276171 and 31502156), the Scientific and Technological Innovation Project Financially Supported by Qingdao National Laboratory for Marine Science and Technology (No. 2015ASKJ02), the National Flatfish Industry System Construction Programme, China (No. nycytx-50), and the National Key Basic Program of Science and Technology-Platforms of Aquaculture Stock Resources.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Feng You.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary Materials

Fig. S1

Hierarchical clustering of DEGs between haploid and common diploid. Common diploid (T04, T05, T06) were clustered together and were distinct from the haploid (T01, T02, T03). Scale bar represents the log2 (FPKM). (PNG 34 kb)

Fig. S2

GO assignment of DEGs between haploid and common diploid. The horizontal axis represents the GO secondary term. The right vertical axis is the number of genes assigned to the GO term, and the left vertical axis is the percent of genes assigned to the GO term. The yellow column is the unigenes subjected to the GO term. Blue represents the DEGs between haploid and common diploid subjected to the GO term. (GIF 421 kb)

High resolution image (TIFF 3405 kb)

Fig. S3

COG assignment of DEGs between haploid and common diploid. The horizontal axis represents the COG term. The vertical axis is the number of genes subjected to the COG term. (PNG 486 kb)

Fig. S4

KEGG class diagram of DEGs between haploid and common diploid. Horizontal coordinate stands for DEGs number and the percent of DEGs among annotated genes. Vertical coordinate stands for pathway class. (PNG 83 kb)

Fig. S5

Scatter diagram of KEGG enrichment of DEGs between haploid and common diploid. Every graphic spot stands for a single kind of pathway, and enrichment factor means the ratio of unigene number to DEG number. Q value is the q value corrections in multiple hypothesis testing. (PNG 398 kb)

Fig. S6

Scatter diagram of KEGG enrichment of DEGs between mitogynogenesis and haploid. (PNG 159 kb)

Fig. S7

Scatter diagram of KEGG enrichment of DEGs between meiogynogenesis and haploid. (PNG 177 kb)

Fig. S8

Scatter diagram of KEGG enrichment of DEGs between mitogynogenesis and common diploid. (PNG 206 kb)

Table S1

The annotated DEGs between haploid and common diploid. (XLSX 163 kb)

Table S2

The annotated DEGs between gynogenetic diploids and haploid. (XLSX 15 kb)

Table S3

The annotated DEGs between gynogenetic diploids and common diploid. (XLSX 11 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, Z., Wu, Z., Wang, L. et al. Characterization of Embryo Transcriptome of Gynogenetic Olive Flounder Paralichthys olivaceus . Mar Biotechnol 18, 545–553 (2016). https://doi.org/10.1007/s10126-016-9716-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-016-9716-6

Keywords

Navigation