Skip to main content
SpringerLink
Log in

Genome-Wide Differential DNA Methylomes Provide Insights into the Infertility of Triploid Oysters

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

Abstract

Chromosomal incompatibility and gene expression changes would affect the development of polyploid gonad and gamete formation. The role of epigenetics like DNA methylation in reproductive development is fully demonstrated in diploid animals. The lack of polyploid species and the infertility of polyploid animals, especially the odd ploidy, limit the study of epigenetic regulation mechanism of polyploid reproduction. Fertile and infertile individuals exist in triploid Pacific oyster Crassostrea gigas, which provide an interesting model for studies on the effect of epigenetic regulation on gonadal development. The whole genome single base resolution DNA methylomes in gonads of triploid females α (F-3nα), triploid females β (F-3nβ), triploid males α (M-3nα), triploid hermaphrodite predominantly males (HPM-3n), diploid females (F-2n), and diploid males (M-2n) were generated by using bisulfite-sequencing. The overall DNA methylation profiles in gene regions and transposable regions of fertile and infertile triploid oysters were consistent with those of diploid oysters. The DNA methylation level of CG context decreased in infertile triploid oysters, with more hypomethylated than hypermethylated regions, and the opposite is true in fertile triploid oysters. Genes harbored with differentially methylated regions (DMRs) in infertile triploids were mainly related to the metabolism pathways and the signal pathways. Correlation analysis indicated that the expression of gene transcriptions was generally positively associated with DNA methylation in gene body regions, and DMRs in infertile triploid oysters played significant roles in gonadal development as a possible critical epigenetic regulator of gonadal development gene transcriptional activity. These findings indicate a potential relationship between DNA methylation variability and gene expression plasticity in newly formed polyploidy. As far as we know, this is the first study revealing the epigenetic regulation of gonadal development in invertebrates based on fertile and infertile models, meanwhile providing a new mentality to explore the regulatory mechanisms of infertility in triploids.

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
Fig. 6

Similar content being viewed by others

References

  • Amoyel M, Anderson J, Suisse A, Glasner J, Bach EA (2016) Socs36E controls niche competition by repressing MAPK signaling in the Drosophila testis. PLoS Genet 12:e1005815

  • Birchler JA, Yao H, Chudalayandi S (2007) Biological consequences of dosage dependent gene regulatory systems. Biochim Biophys Acta 1769:422–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bogani D, Siggers P, Brixey R, Warr N, Beddow S, Edwards J, Williams D, Wilhelm D, Koopman P, Flavell R A, Chi H, Ostrer H, Wells S, Cheeseman M, Greenfield A (2009) Loss of mitogen-activated protein kinase kinase kinase 4 (MAP3K4) reveals a requirement for MAPK signaling in mouse sex determination. PLoS Biol 7:e1000196

  • Bonasio R, Li Q, Lian J, Mutti NS, Jin L, Zhao H, Zhang P, Wen P, Xiang H, Ding Y, Jin Z, Shen SS, Wang Z, Wang W, Wang J, Berger SL, Liebig J, Zhang G, Reinberg D (2012) Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr Biol 22:1755–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busada JT, Niedenberger BA, Velte EK, Keiper BD, Geyer CB (2015) Mammalian target of rapamycin complex 1 (mTORC1) is required for mouse spermatogonial differentiation in vivo. Dev Biol 407:90–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavelier P, Cau J, Morin N, Delsert C (2017) Early gametogenesis in the Pacific oyster: new insights using stem cell and mitotic markers. J Exp Biol 220:3988–3996

    PubMed  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  CAS  PubMed  Google Scholar 

  • Conrad T, Akhtar A (2012) Dosage compensation in drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet 13:123–134

    Article  CAS  PubMed  Google Scholar 

  • Dong WL, Tan FQ, Yang WX (2015) Wnt signaling in testis development: unnecessary or essential?. Gene 565:155–165

    Article  CAS  PubMed  Google Scholar 

  • De Riso G, Fiorillo DFG, Fierro A, Cuomo M, Chiariotti L, Miele G, Cocozza S (2020) Modeling DNA methylation profiles through a dynamic equilibrium between methylation and demethylation. Biomolecules 10:1271

    Article  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

  • Elango N, Yi SV (2008) DNA methylation and structural and functional bimodality of vertebrate promoters. Mol Biol Evol 25:1602–1608

    Article  CAS  PubMed  Google Scholar 

  • Fontana R, Della Torre S (2016) The deep correlation between energy metabolism and reproduction: a view on the effects of nutrition for women fertility. Nutrients 8:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo X, Allen SKJR (1994) Reproductive potential and genetics of triploid Pacific oysters, Crassostrea gigas (Thunberg). Biol Bull 187:309–318

    Article  CAS  PubMed  Google Scholar 

  • Guo X, DeBrosse GA, Allen SK (1996) All-triploid Pacific oysters (Crassostrea gigas Thunberg) produced by mating tetraploids and diploids. Aquaculture 142:149–161

    Article  Google Scholar 

  • Hegarty MJ, Batstone T, Barker GL, Edwards KJ, Abbott RJ, Hiscock SJ (2011) Nonadditive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae). Mol Ecol 20:105–113

    Article  CAS  PubMed  Google Scholar 

  • Johnson MT, Freeman EA, Gardner DK, Hunt PA (2007) Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol Reprod 77:2–8

    Article  CAS  PubMed  Google Scholar 

  • Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492

    Article  CAS  PubMed  Google Scholar 

  • Jouaux A, Blin JL, Adeline B, Heude-Berthelin C, Sourdaine P, Mathieu M, Kellner K (2013) Impact of energy storage strategies on gametogenesis and reproductive effort in diploid and triploid Pacific oysters Crassostrea gigas - involvement of insulin signaling. Aquaculture 388–391:173–181

    Article  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 

  • Lang Z, Wang Y, Tang K, Tang D, Datsenka T, Cheng J, Zhang Y, Handa AK, Zhu JK (2017) Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc Natl Acad Sci USA 114:E4511–E4519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Wang M, Wang L, Guo Q, Liang G (2018) Extensive genetic and DNA methylation variation contribute to heterosis in triploid loquat hybrids. Genome 61:437–447

    Article  CAS  PubMed  Google Scholar 

  • Mable BK (2004) ‘Why polyploidy is rarer in animals than in plants’: myths and mechanisms. Biol J Linn Soc 82:453–466

    Article  Google Scholar 

  • Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity (edinb) 110:99–104

    Article  CAS  Google Scholar 

  • Manor ML, Weber GM, Cleveland BM, Yao J, Kenney PB (2015) Expression of genes associated with fatty acid metabolism during maturation in diploid and triploid female rainbow trout. Aquaculture 435:178–186

    Article  CAS  Google Scholar 

  • Mao X, Tao CJGO, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

  • Matsui Y, Hayashi K (2007) Epigenetic regulation for the induction of meiosis. Cell Mol Life Sci 64:257–262

    Article  CAS  PubMed  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 5:224

    Article  PubMed  PubMed Central  Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437

    Article  CAS  PubMed  Google Scholar 

  • Pala I, Coelho MM, Schartl M (2008) Dosage compensation by gene-copy silencing in a triploid hybrid fish. Curr Biol 18:1344–1348

    Article  CAS  PubMed  Google Scholar 

  • Piferrer F, Beaumont A, Falguière JC, Flajšhans M, Haffray P, Colombo L (2009) Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 293:125–156

    Article  Google Scholar 

  • Ribas L, Vanezis K, Imues MA, Piferrer F (2017) Treatment with a DNA methyltransferase inhibitor feminizes zebrafish and induces long-term expression changes in the gonads. Epigenetics Chromatin 10:59

    Article  PubMed  PubMed Central  Google Scholar 

  • Riviere G (2014) Epigenetic features in the oyster Crassostrea gigas suggestive of functionally relevant promoter DNA methylation in invertebrates. Front Physiol 5:129

    PubMed  PubMed Central  Google Scholar 

  • Riviere G, He Y, Tecchio S, Crowell E, Gras M, Sourdaine P, Guo X, Favrel P (2017) Dynamics of DNA methylomes underlie oyster development. PLoS Genet 13:e1006807

  • Roberts SB, Gavery MR (2012) Is there a relationship between DNA methylation and phenotypic plasticity in invertebrates?. Front Physiol 2:116

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarda S, Zeng J, Hunt BG, Yi SV (2012) The evolution of invertebrate gene body methylation. Mol Biol Evol 29:1907–1916

    Article  CAS  PubMed  Google Scholar 

  • Schultz MD, He Y, Whitaker JW, Hariharan M, Mukamel EA, Leung D, Rajagopal N, Nery JR, Urich MA, Chen H, Lin S, Lin Y, Jung I, Schmitt AD, Selvaraj S, Ren B, Sejnowski TJ, Wang W, Ecker JR (2015) Human body epigenome maps reveal noncanonical DNA methylation variation. Nature 523:212–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegfried Z, Simon I (2010) DNA methylation and gene expression. Wiley Interdiscip Rev Syst Biol Med 2:362–371

    Article  CAS  PubMed  Google Scholar 

  • Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14:348–352

    Article  CAS  PubMed  Google Scholar 

  • Spangenberg V, Arakelyan M, Galoyan E, Matveevsky S, Petrosyan R, Bogdanov Y, Danielyan F, Kolomiets O (2017) Reticulate evolution of the rock lizards: meiotic chromosome dynamics and spermatogenesis in diploid and triploid males of the genus Darevskia. Genes (basel) 8:149

    Article  Google Scholar 

  • Suzuki MM, Kerr AR, De Sousa D, Bird A (2007) CpG methylation is targeted to transcription units in an invertebrate genome. Genome Res 17:625–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd EV, Ortega-Recalde O, Liu H, Lamm MS, Rutherford KM, Cross H, Black MA, Kardailsky O, Marshall Graves JA, Hore TA, Godwin JR, Gemmell NJ (2019) Stress, novel sex genes, and epigenetic reprogramming orchestrate socially controlled sex change. Sci Adv 5:eaaw7006

  • Wang X, Li Q, Lian J, Li L, Jin L, Cai H, Xu F, Qi H, Zhang L, Wu F, Meng J, Que H, Fang X, Guo X, Zhang G (2014) Genome-wide and single-base resolution DNA methylomes of the Pacific oyster Crassostrea gigas provide insight into the evolution of invertebrate CpG methylation. BMC Genomics 15:1119

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Li A, Wang W, Que H, Zhang G, Li L (2021) DNA methylation mediates differentiation in thermal responses of Pacific oyster (Crassostrea gigas) derived from different tidal levels. Heredity (edinb) 126:10–22

    Article  CAS  Google Scholar 

  • Wertheim B, Beukeboom LW, van de Zande L (2013) Polyploidy in animals: effects of gene expression on sex determination, evolution and ecology. Cytogenet Genome Res 140:256–269

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Song C, Liu S, Tao M, Hu J, Wang J, Liu W, Zeng M, Liu Y (2013) DNA methylation analysis of allotetraploid hybrids of red crucian carp (Carassius auratus red var.) and common carp (Cyprinus carpio L.). PLoS One 8:e56409

  • Xi Y, Li W (2009) BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 10:232

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi S, Hong K, Liu R, Shen L, Inoue A, Diep D, Zhang K, Zhang Y (2012) Tet1 controls meiosis by regulating meiotic gene expression. Nature 492:443–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan H, Bombarely A, Xu B, Wu B, Frazier TP, Zhang X, Chen J, Chen P, Sun M, Feng G, Wang C, Cui C, Li Q, Zhao B, Huang L (2019) Autopolyploidization in switchgrass alters phenotype and flowering time via epigenetic and transcription regulation. J Exp Bot 70:5673–5686

    Article  CAS  PubMed  Google Scholar 

  • Yue C, Li Q, Yu H (2018) Gonad transcriptome analysis of the Pacific oyster Crassostrea gigas identifies potential genes regulating the sex determination and differentiation process. Mar Biotechnol 20:206–219

    Article  CAS  Google Scholar 

  • Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhu JK (2012) Active DNA demethylation in plants and animals. Cold Spring Harb Symp Quant Biol 77:161–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Li Q, Kong L, Yu H (2018) DNA methylation frequency and epigenetic variability of the Pacific oyster Crassostrea gigas in relation to the gametogenesis. Fish Sci 84:789–797

    Article  CAS  Google Scholar 

  • Zhang X, Nie Y, Cai S, Ding S, Fu B, Wei H, Chen L, Liu X, Liu M, Yuan R, Qiu B, He Z, Cong P, Chen Y, Mo D (2019) Earlier demethylation of myogenic genes contributes to embryonic precocious terminal differentiation of myoblasts in miniature pigs. FASEB J 33:9638–9655

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by grants from National Key R&D Program of China (2018YFD0900200) and National Natural Science Foundation of China (31672649).

Author information

Author notes

  1. Dongfang Sun and Hong Yu contributed equally to this work.

Authors and Affiliations

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

    Dongfang Sun, Hong Yu & Qi Li

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Hong Yu & Qi Li

Authors
  1. Dongfang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qi Li
    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

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, D., Yu, H. & Li, Q. Genome-Wide Differential DNA Methylomes Provide Insights into the Infertility of Triploid Oysters. Mar Biotechnol 24, 18–31 (2022). https://doi.org/10.1007/s10126-021-10083-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-021-10083-y

Keywords

Search

Navigation