Skip to main content
SpringerLink
Log in

Expression and DNA methylation pattern of reproduction-related genes in partially fertile triploid Pacific oysters Crassostrea gigas

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Partial or complete sterility is an obvious feature in triploid Pacific oyster (Crassostrea gigas) which contributes to improving rearing performances. Despite the significance of sterility, the molecular mechanism behind it remains elusive and related research was limited. This study focused on six reproduction-related genes and compared their different behavior in gene expression and DNA methylation pattern between triploid and diploid oysters in order to provide more molecular information. The gonadal development of triploid oyster was examined by histology before molecular analysis. Gametogenesis disturbance was observed in triploid oysters at different development stages (stage II and III) with more serious impairment in females. QPCR showed significant gene expression difference between diploid and triploid in two genes: putative Vg and cgER. Gene expression of putative Vg was delayed in triploids while for cgER triploid oyster showed higher expression and the difference was significant at stage III. DNA methylation pattern of these two genes were further investigated by bisulfite sequencing. Between diploid and triploid oysters, no difference was observed in total methylation level but some individual loci showed different patterns: significantly high methylation rate of loci 2284 in cgER was observed in triploid oyster which has a higher expression of this gene. This study indicated that putative Vg and cgER might play a role in partial sterile in triploid C. gigas. Gene expression could be regulated by the methylation pattern at specific individual locus, which deserves equivalent attention as well as total DNA methylation level.

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
Fig. 5

Similar content being viewed by others

References

  • Allen SK, Downing SL (1986) Performance of triploid Pacific oysters, Crassostrea gigas (Thunberg). I. Survival, growth, glycogen content, and sexual maturation in yearlings. J Exp Mar Biol Ecol 102:197–208

    Article  Google Scholar 

  • Berthelin CH, Laisney J, Espinosa J, Martin O, Hernandez G, Mathieu M, Kellner K (2001) Storage and reproductive strategy in Crassostrea gigas from two different growing areas (Normandy and the Atlantic coast, France). Invertebr Reprod Dev 40:79–86

    Article  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dheilly NM, Jouaux A, Boudry P, Favrel P, Lelong C (2014) Transcriptomic profiling of gametogenesis in triploid Pacific oysters Crassostrea gigas: towards an understanding of partial sterility associated with triploidy. PLOS ONE 9:e112094

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding Y, He F, Wen H, Li J, Ni M, Chi M, Qian K, Bu Y, Zhang D, Si Y, Zhao J (2013) DNA methylation status of cyp17-II gene correlated with its expression pattern and reproductive endocrinology during ovarian development stages of Japanese flounder (Paralichthys olivaceus). Gene 527:82–88

    Article  CAS  PubMed  Google Scholar 

  • Garnier-Géré PH, Naciri-Graven Y, Bougrier S, Magoulas A, Heral M, Kotoulas G, Hawkins A, Gérard A (2002) Influences of triploidy, parentage and genetic diversity on growth of the Pacific oyster Crassostrea gigas reared in contrasting natural environments. Mol Ecol 11:1499–1514

    Article  PubMed  Google Scholar 

  • Guo X (2004) Oyster breeding and the use of biotechnology. Bull Aquac Assoc Can 104:26–33

    Google Scholar 

  • Hubert S, Cognard E, Hedgecock D (2009) Centromere mapping in triploid families of the Pacific oyster Crassostrea gigas (Thunberg). Aquaculture 288:172–183

    Article  CAS  Google Scholar 

  • Jiang Q, Li Q, Yu H, Kong L (2016) Inheritance and variation of genomic DNA methylation in diploid and triploid Pacific oyster (Crassostrea gigas). Mar Biotechnol 18:124–132

    Article  CAS  PubMed  Google Scholar 

  • Jouaux A, Heude-Berthelin C, Sourdaine P, Mathieu M, Kellner K (2010) Gametogenic stages in triploid oysters Crassostrea gigas: irregular locking of gonial proliferation and subsequent reproductive effort. J Exp Mar Biol Ecol 395:162–170

    Article  Google Scholar 

  • Keay J, Bridgham JT, Thornton JW (2006) The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 147:3861–3869

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Yu H, Yu R (2006) Genetic variability assessed by microsatellites in cultured populations of the Pacific oyster (Crassostrea gigas) in China. Aquaculture 259:95–102

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto T, Nakamura AM, Mori K, Akiyama I, Hirose H, Takahashi Y (2007) Oyster estrogen receptor: cDNA cloning and immunolocalization. Gen Comp Endocrinol 151:195–201

    Article  CAS  PubMed  Google Scholar 

  • Naimi A, Martinez A-S, Specq M-L, Diss B, Mathieu M, Sourdaine P (2009a) Molecular cloning and gene expression of Cg-Foxl2 during the development and the adult gametogenetic cycle in the oyster Crassostrea gigas. Comp Biochem Phys B 154:134–142

    Article  Google Scholar 

  • Naimi A, Martinez A-S, Specq M-L, Mrac A, Diss B, Mathieu M, Sourdaine P (2009b) Identification and expression of a factor of the DM family in the oyster Crassostrea gigas. Comp Biochem Phys A 152:189–196

    Article  Google Scholar 

  • Nell JA (2002) Farming triploid oysters. Aquaculture 210:69–88

    Article  Google Scholar 

  • Normand J, Le Pennec M, Boudry P (2008) Comparative histological study of gametogenesis in diploid and triploid Pacific oysters (Crassostrea gigas) reared in an estuarine farming site in France during the 2003 heatwave. Aquaculture 282:124–129

    Article  Google Scholar 

  • Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257

    Article  CAS  PubMed  Google Scholar 

  • Olson CE, Roberts SB (2014) Genome-wide profiling of DNA methylation and gene expression in Crassostrea gigas male gametes. Front Physiol 5:1–7

    Article  Google Scholar 

  • Pakdel F, Feon S, Le Gac F, Le Menn F, Valotaire Y (1991) In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout. Mol Cell Endocrinol 75:205–212

    Article  CAS  PubMed  Google Scholar 

  • Puinean AM, Labadie P, Hill EM, Osada M, Kishida M, Nakao R, Novillo A, Callard IP, Rotchell JM (2006) Laboratory exposure to 17 beta-estradiol fails to induce vitellogenin and estrogen receptor gene expression in the marine invertebrate Mytilus edulis. Aquat Toxicol 79:376–383

    Article  CAS  PubMed  Google Scholar 

  • Que H, Guo X, Zhang F, Allen SK (1997) Chromosome segregation in fertilized eggs from triploid Pacific oysters, Crassostrea gigas (Thunberg), following inhibition of polar body 1. Biol Bull 193:14–19

    Article  CAS  PubMed  Google Scholar 

  • Renault T, Faury N, Barbosa-Solomieu V, Moreau K (2011) Suppression substractive hybridisation (SSH) and real time PCR reveal differential gene expression in the Pacific cupped oyster, Crassostrea gigas, challenged with Ostreid herpesvirus 1. Dev Comp Immunol 35:725–735

    Article  CAS  PubMed  Google Scholar 

  • Riviere G, Wu G-C, Fellous A, Goux D, Sourdaine P, Favrel P (2013) DNA methylation is crucial for the early development in the Oyster C. gigas. Mar Biotechnol 15:739–753

    Article  CAS  PubMed  Google Scholar 

  • Santerre C, Sourdaine P, Adeline B, Martinez A-S (2014) Cg-SoxE and Cg--catenin, two new potential actors of the sex-determining pathway in a hermaphrodite lophotrochozoan, the Pacific oyster Crassostrea gigas. Comp Biochem Phys A 167:68–76

    Article  CAS  Google Scholar 

  • Strömqvist M, Tooke N, Brunström B (2010) DNA methylation levels in the 5′ flanking region of the vitellogenin I gene in liver and brain of adult zebrafish (Danio rerio)—Sex and tissue differences and effects of 17-ethinylestradiol exposure. Aquat Toxicol 98:275–281

    Article  PubMed  Google Scholar 

  • Thornton JW, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714–1717

    Article  CAS  PubMed  Google Scholar 

  • Wang CD, Croll RP (2003) Effects of sex steroids on in vitro gamete release in the sea scallop, Placopecten magellanicus. Invertebr Reprod Dev 44:89–100

    Article  CAS  Google Scholar 

  • Wang C, Croll RP (2007) Estrogen binding sites in the sea scallop: characterization and possible involvement in reproductive regulation. Comp Biochem Phys B 148:303–313

    Article  Google Scholar 

  • Wen AY, You F, Sun P, Li J, Xu DD, Wu ZH, Ma DY, Zhang PJ (2014) CpG methylation of dmrt1 and cyp19a promoters in relation to their sexual dimorphic expression in the Japanese flounder Paralichthys olivaceus. J Fish Biol 84:193–205

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the grants from National Natural Science Foundation of China (31372524), Shandong Seed Project, and Shandong Province (2014GHY115002).

Author information

Authors and Affiliations

  1. The Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Qun Jiang, Qi Li, Hong Yu & Lingfeng Kong

  2. College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Qun Jiang

Authors
  1. Qun Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lingfeng Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qi Li.

Ethics declarations

Conflict of interest

Qun Jiang declares that she does not have conflict of interest. Qi Li declares that he does not have conflict of interest. Hong Yu declares that she does not have conflict of interest. Lingfeng Kong declares that he does not have conflict of interest.

Ethical approval

The research was conducted in the absence of any ethical issue on aquatic animal research.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, Q., Li, Q., Yu, H. et al. Expression and DNA methylation pattern of reproduction-related genes in partially fertile triploid Pacific oysters Crassostrea gigas . Genes Genom 39, 997–1006 (2017). https://doi.org/10.1007/s13258-017-0563-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-017-0563-2

Keywords

Search

Navigation