Skip to main content
SpringerLink
Log in

Identification and Expression Analysis of Genes Involved in Early Ovary Development in Diploid Gynogenetic Hybrids of Red Crucian Carp × Common Carp

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

Abstract

Diploid eggs of allotetraploid hybrids (red crucian carp ♀ × common carp ♂), when activated by UV-irradiated sperm of scatter scale carp, can develop into diploid progenies without chromosome duplication treatment. Diploid progenies produce diploid eggs, which develop into diploid population by the same way. To understand the molecular mechanism underlying the production of diploid eggs by the diploid fish, we constructed a forward suppression subtractive hybridization complementary DNA (cDNA) library. The cDNAs from the ovary in proliferation phase were employed as the “tester,” and those in growth phase were used as the “driver.” Seventy-three cDNA clones that are specifically expressed in proliferation phase were detected by dot-blot hybridization. Sequencing analyses revealed that several of these cDNAs have high homologies to the known sequences in the NCBI database. Their encoded proteins include the protein preventing mitosis catastrophe (PMC), the signal recognition particle 9, the ATP-binding cassette transporter, the glucanase–xylanase fusion protein, and others. These genes were confirmed by reverse transcriptase–polymerase chain reaction. The expression profile of the PMC gene at different time points was analyzed by quantitative real-time polymerase chain reaction. The results indicated that the expression of this suppression subtractive hybridization-identified gene changed during the time course, corresponding with the cellular phenomenon in the ovary development. Our studies provide insights into the molecular mechanism underlying the ovary development of diploid gynogenetic fish.

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
Fig. 4

Similar content being viewed by others

References

  • Auslander M, Yudkovski Y, Chalifa-Caspi V, Herut B, Ophir R, Reinhardt R, Neumann PM, Tom M (2008) Pollution-affected fish hepatic transcriptome and its expression patterns on exposure to cadmium. Mar Biotechnol 10:250–261

    Article  CAS  PubMed  Google Scholar 

  • Cho HK, Nam BH, Kong HJ, Han HS, Hur YB, Choi TJ, Choi YH, Kim WJ, Cheong J (2008) Identification of softness syndrome-associated candidate genes and DNA sequence variation in the sea squirt, Halocynthia roretzi. Mar Biotechnol 10:447–456

    Article  CAS  PubMed  Google Scholar 

  • Christine OI, Holland B, Schmitt L (2006) The motor domains of ABC-transporters, what can structures tell us? Naunyn-Schmiedeberg's Arch Pharmacol 372:385–399

    Article  Google Scholar 

  • Darias MJ, Zambonino-Infante JL, Hugot K, Cahu CL, Mazurais D (2008) Gene expression patterns during the larval development of European sea bass (dicentrarchus labrax) by microarray analysis. Mar Biotechnol 10:416–428

    Article  CAS  PubMed  Google Scholar 

  • Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and blibraries. Proc Natl Acad Sci U S A 93:6025–6030

    Article  CAS  PubMed  Google Scholar 

  • Enoch T, Nurse P (1991) Coupling M phase and S phase: controls maintaining the dependence of mitosis on chromosome replication. Cell 65:921–923

    Article  CAS  PubMed  Google Scholar 

  • Fagutao FF, Yasuike M, Caipang CM, Kondo H, Hirono I, Takahashi Y, Aoki T (2008) Gene expression profile of hemocytes of kuruma shrimp, Marsupenaeus japonicas following peptidoglycan stimulation. Mar Biotechnol 10:731–740

    Article  CAS  PubMed  Google Scholar 

  • Gottesman MM, Ambudkar SV (2001) Overview: ABC transporters and human disease. J Bioenerg Biomembr 33:453–458

    Article  CAS  PubMed  Google Scholar 

  • Kato S, Kosaka T, Watanabe K (2008) Comparative transcriptome analysis of responses of Methanothermobacter thermautotrophicus to different environmental stimuli. Environ Microbiol 10:893–905

    Article  CAS  PubMed  Google Scholar 

  • Kovalskaya ON, Sergiev PV, Bogdanov AA, Dontsova OA (2006) Does a deficiency of the signal recognition particle (SRP) pathway affect the biosynthesis of its components in Saccharomyces cerevisiae and Escherichia coli? Biochemistry (Moscow) 71:723–729

    Article  CAS  Google Scholar 

  • Li P, Nijhawan D, Bidojardkp I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome C and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489

    Article  CAS  PubMed  Google Scholar 

  • Liu Y (1993) Propagation physiology of main cultivated fish in China. Agricultural Publishing House, Beijing, pp 22–29

    Google Scholar 

  • Liu Y, Zhou GJ (1986) Cytological study on the gonadal development of F1 hybrids produced by crossing Carassius auratus (♀) with Cyprinus carpio (♂). Acta Hydrobiol Sin 10:101–108

    Google Scholar 

  • Liu SJ, Liu Y, Zhou GJ, Zhang XJ, Luo S, Feng H, He XX, Zhu GH, Yang H (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192:171–186

    Article  Google Scholar 

  • Liu SJ, Sun YD, Zhang C, Luo KK, Liu Y (2004) Production of gynogenetic progeny from allotetraploid hybrids red crucian carp × common carp. Aquaculture 236:193–200

    Article  Google Scholar 

  • Liu LG, Tao M, Duan W, Liu SJ, Liu D, Liu Y (2007a) Cloning and genetic analysis of cyclin B gene in allotetraploids and their original parents. J Biochem Mol Bio 23:849–858

    CAS  Google Scholar 

  • Liu SJ, Duan W, Tao M, Zhang C, Sun YD, Shen JM, Wang J, Luo KK, Liu Y (2007b) Establishment of the diploid gynogenetic hybrid clonal line of red crucian carp × common carp. Sci China C Life Sci 50:186–193

    Article  PubMed  Google Scholar 

  • Livark KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25(4):402–408

    Article  Google Scholar 

  • Lundgren K, Walworth N, Booher R, Dembski M, Kirschner M, Beach D (1991) Mikl and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 64:1111–1122

    Article  CAS  PubMed  Google Scholar 

  • Marchand J, Tanguy A, Charrier G, Quiniou L, Plee-Gauthier E, Laroche J (2006) Molecular identification and expression of differentially regulated genes of the European flounder, Platichthys flesus, submitted to pesticide exposure. Mar Biotechnol 8:275–294

    Article  CAS  PubMed  Google Scholar 

  • Moya A, Tambutté S, Béranger G, Gaume B, Scimeca JC, Allemand D, Zoccola D (2008) Cloning and use of a coral 36B4 gene to study the differential expression of coral genes between light and dark conditions. Mar Biotechnol 10:653–663

    Article  CAS  PubMed  Google Scholar 

  • Reusch TB, Veron AS, Preuss C, Weiner J, Wissler L, Beck A, Klages S, Kube M, Reinhardt R, Bornberg-Bauer E (2008) Comparative analysis of expressed sequence tag(EST) libraries in the seagrass Zostera marina subjected to temperature stress. Mar Biotechnol 10:297–309

    Article  CAS  PubMed  Google Scholar 

  • Schünemann D (2004) Structure and function of the chloroplast signal recognition particle. Curr Genet 44:295–304

    Article  PubMed  Google Scholar 

  • Shen JM, Liu SJ, Shun YD, Zhang C, Luo KK, Tao M, Zeng C, Liu Y (2006) A new type of triploid crucian carp-red crucian carp (♀) X allotetroploid (♂). Prog Nat Sci 16:1348–1352

    Article  CAS  Google Scholar 

  • Su JY, Maller JL (1995) Cloning and expression of a Xenopus gene that prevents, mitotic catastrophe in fission yeast. Mol Gen Genet 246:387–396

    Article  CAS  PubMed  Google Scholar 

  • Sun YD, Liu SJ, Zhang C, Li JZ, Huang WR, Zhang J, Luo KK, Zhou GJ, Liu Y (2003) The chromosome number and gonadal structure of F9–F11 allotetraploid crucian-carp. Acta Genet Sin 30:414–418

    CAS  PubMed  Google Scholar 

  • Tsoi SCM, Ewart KV, Penny S, Melville K, Liebscher RS, Brown LL, Douglas SE (2004) Identification of immune-relevant genes from Atlantic Salmon using suppression subtractive hybridization. Mar Biotechnol 6:199–214

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Li F, Dong B, Zhang X, Zhang C, Xiang J (2006) Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Mar Biotechnol 8:491–500

    Article  PubMed  Google Scholar 

  • Wang B, Li F, Luan W, Xie Y, Zhang C, Luo Z, Gui L, Yan H, Xiang J (2008) Comparison of gene expression profiles of Fenneropenaeus chinensis challenged with WSSV and Vibrio. Mar Biotechnol 10:664–675

    Article  CAS  PubMed  Google Scholar 

  • Wong QW, Mak WY, Chu KH (2008) Differential gene expression in hepatopancreas of the shrimp Metapenaeus ensis during ovarian maturation. Mar Biotechnol 10:91–98

    Article  CAS  PubMed  Google Scholar 

  • Wynne JW, O'Sullivan MG, Cook MT, Stone G, Nowak BF, Lovell DR, Elliott NG (2008) Transcriptome analyses of amoebic gill disease- affected Atlantic salmon (Salmo salar) tissues reveal localized host gene suppression. Mar Biotechnol 10:388–403

    Article  CAS  PubMed  Google Scholar 

  • Xie J, Wen JJ, Chen B, Gui JF (2001) Differential gene expression in fully-grown oocytes between gynogenetic and gonochoristic crucian carps. Gene 271:109–116

    Article  CAS  PubMed  Google Scholar 

  • Yan JP, Liu SJ, Sun YD, Zhang C, Liu Y (2005) RAPD analysis of diploid gynogen populations of allotetraploid hybrids of red crucian carp (♀) × common carp (♂). Acta Hydrobiol Sin 29:259–265

    CAS  Google Scholar 

  • Zeng C, Tao M, Liu SJ, Liu Y (2006) Comparative analysis of transcriptional level in ovaries with different ploidy level. J Nat Sci Hunan Normal Univ 29:73–76

    CAS  Google Scholar 

  • Zhang YB, Shi YH, Gui JF (2003) Construction of antiviral subtractive cDNA library of cultured fish cells. Acta Hydrobiol Sin 27:113–118

    CAS  Google Scholar 

  • Zhang C, Sun YD, Liu SJ, Liu Y (2005) Evidence of the unreduced diploid eggs generated from the diploid gynogenetic progeny of allotetraploid hybrids. Acta Genet Sin 32:136–144

    PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the National Natural Science Fund for Distinguished Young Scholars (30725028), the National Basic Research Program of China (973) (2007CB109200), and specially appointed Professor for Furong Scholars of Hunan Province.

Author information

Authors and Affiliations

  1. Key Laboratory of Protein Chemistry and Fish Developmental Biology of the Education Ministry of China, College of Life Sciences, Hunan Normal University, Changsha, 410081, People’s Republic of China

    Dong Liu, Shaojun Liu, Cuiping You, Lin Chen, Zhen Liu, Liangguo Liu, Jing Wang & Yun Liu

Authors
  1. Dong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaojun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cuiping You
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Liangguo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shaojun Liu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, D., Liu, S., You, C. et al. Identification and Expression Analysis of Genes Involved in Early Ovary Development in Diploid Gynogenetic Hybrids of Red Crucian Carp × Common Carp. Mar Biotechnol 12, 186–194 (2010). https://doi.org/10.1007/s10126-009-9212-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-009-9212-3

Keywords

Search

Navigation