Skip to main content
SpringerLink
Log in

Discovery of Nanos1 and Nanos2/3 as Germ Cell Markers During Scallop Gonadal Development

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

Abstract

Nanos are conserved genes involved in germline cell specification and differentiation. However, little is known about the role of different members of Nanos family in germ cell development in mollusks. In the present study, we conducted genome-wide identification of Nanos family in an economically important scallop Patinopecten yessoensis, and detected their expression in adult tissues and during early development. Two Nanos genes (PyNanos1, PyNanos2/3) were identified, both of which have the N-terminal NOT1-interacting motif and C-terminal (CCHC)2 zinc finger domain. Expression profiles showed that PyNanos1 and PyNanos2/3 were primarily expressed in the gonads, with PyNanos1 being localized in the oogonia, oocytes, and spermatogonia, while PyNanos2/3 being specifically in spermatogonia. The results suggest that PyNanos are germ cell specific and may play crucial roles in gametogenesis in the scallop. PyNanos1 is a maternal gene, which is distributed uniformly at early cleavage, and restricted to 2–3 cell clusters from blastulae to trochophore larvae, suggesting its potential role in the formation of PGCs. Zygotically expressed PyNanos2/3 displayed a similar signal with PyNanos1 in the trochophore larvae, suggesting it may also participate in the formation and/or maintenance of PGCs. This study will benefit germplasm exploitation and conservation in bivalves, and facilitate a better understanding of the evolution of Nanos family and the role of different Nanos in germ cell development in mollusks.

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

  • Bhandari D, Raisch T, Weichenrieder O, Jonas S, Izaurralde E (2014) Structural basis for the Nanos-mediated recruitment of the CCR4-NOT complex and translational repression. Genes Dev 28:888–901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Keuckelaere E, Hulpiau P, Saeys Y, Berx G, van Roy F (2018) Nanos genes and their role in development and beyond. Cell Mol Life Sci 75:1929–1946

    Article  PubMed  Google Scholar 

  • de Siqueira-Silva DH, Saito T, dos Santos-Silva AP, da Silva CR, Psenicka M, Yasui GS (2018) Biotechnology applied to fish reproduction: tools for conservation. Fish Physiol Biochem 44:1469–1485

    Article  PubMed  Google Scholar 

  • Draper BW, McCallum CM, Moens CB (2007) Nanos1 is required to maintain oocyte production in adult zebrafish. Dev Biol 305:589–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ewen-Campen B, Schwager EE, Extavour CGM (2010) The molecular machinery of germ line specification. Mol Reprod Dev 77:3–18

    Article  CAS  PubMed  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  CAS  PubMed  Google Scholar 

  • Extavour CGM (2007) Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr Comp Biol 47:770–785

    Article  PubMed  Google Scholar 

  • Fabioux C, Huvet A, Lelong C, Robert R, Pouvreau S, Daniel JY, Minguant C, Le Pennec M (2004) Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem Biophys Res Commun 320:592–598

    Article  CAS  PubMed  Google Scholar 

  • Gjedrem T, Rye M (2018) Selection response in fish and shellfish: a review. Rev Aquac 10:168–179

    Article  Google Scholar 

  • Haraguchi S, Tsuda M, Kitajima S, Sasaoka Y, Nomura-Kitabayashi A, Kurokawa K, Saga Y (2003) Nanos1: a mouse nanos gene expressed in the central nervous system is dispensable for normal development. Mech Dev 120:721–731

    Article  CAS  PubMed  Google Scholar 

  • Kranz AM, Tollenaere A, Norris BJ, Degnani BM, Degnani SM (2010) Identifying the germline in an equally cleaving mollusc: vasa and nanos expression during embryonic and larval development of the vetigastropod Haliotis asinina. J Exp Zool B Mol Dev Evol 314B:267–279

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li R, Zhang L, Li W, Zhang Y, Li Y, Zhang M, Zhao L, Hu X, Wang S, Bao Z (2018) FOXL2 and DMRT1L are Yin and Yang genes for determining timing of sex differentiation in the bivalve mollusk Patinopecten yessoensis. Front Physiol 9:1166

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zhang L, Li R, Zhang M, Li Y, Wang H, Wang S, Bao Z (2019) Systematic identification and validation of the reference genes from 60 RNA-Seq libraries in the scallop Mizuhopecten yessoensis. BMC Genom 20:288

    Article  Google Scholar 

  • Li Y, Zhang L, Sun Y, Ma X, Wang J, Li R, Zhang M, Wang S, Hu X, Bao Z (2016) Transcriptome sequencing and comparative analysis of ovary and testis identifies potential key sex-related genes and pathways in scallop Patinopecten yessoensis. Mar Biotechnol 18:453–546

    Article  CAS  Google Scholar 

  • Lolicato F, Marino R, Paronetto MP, Pellegrini M, Doici S, Geremia R, Grimaldi P (2008) Potential role of Nanos3 in maintaining the undifferentiated spermatogonia population. Dev Biol 313:725–738

    Article  CAS  PubMed  Google Scholar 

  • Nakao H, Matsumoto T, Oba Y, Niimi T, Yaginuma T (2008) Germ cell specification and early embryonic patterning in Bombyx mori as revealed by nanos orthologues. Evol Dev 10:546–554

    Article  CAS  PubMed  Google Scholar 

  • Osada M, Takamura T, Sato H, Mori K (2003) Vitellogenin synthesis in the ovary of scallop Patinopecten yessoensis: control by estradiol-17 beta and the central nervous system. J Exp Zool A Ecol Integr Physiol 299A:172–179

    CAS  Google Scholar 

  • Rabinowitz JS, Chan XY, Kingsley EP, Duan Y, Lambert JD (2008) Nanos is required in somatic blast cell lineages in the posterior of a mollusk embryo. Curr Biol 18:331–336

    Article  CAS  PubMed  Google Scholar 

  • Reitzel AM, Pang K, Martindale MQ (2016) Developmental expression of “germline”- and “sex determination”- related genes in the ctenophore Mnemiopsis leidyi. EvoDevo 7:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Rivers N, Daly J, Temple-Smith P (2020) New directions in assisted breeding techniques for fish conservation. Reprod Fertil Dev 32:807–821

    Article  PubMed  Google Scholar 

  • Saba R, Kato Y, Saga Y (2014) NANOS2 promotes male germ cell development independent of meiosis suppression. Dev Biol 385:32–40

    Article  CAS  PubMed  Google Scholar 

  • Sada A, Suzuki A, Suzuki H, Saga Y (2009) The rna-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325:1394–1398

    Article  CAS  PubMed  Google Scholar 

  • Suzuki A, Saga Y (2008) Nanos2 suppresses meiosis and promotes male germ cell differentiation. Genes Dev 22:430–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y (2003) Conserved role of nanos proteins in germ cell development. Science 301:1239–1241

    Article  CAS  PubMed  Google Scholar 

  • Wagner GP, Kin K, Lynch VJ (2012) Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci 131:281–285

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Wang Z (2008) Science of marine shellfish culture. Ocean Univ, China Press

    Google Scholar 

  • Wang S, Zhang JB, Jiao WQ, Li J, Xun XG, Sun Y, Guo XM, Huan P, Dong B, Zhang LL, Hu XL, Sun XQ, Wang J, Zhao CT, Wang YF, Wang DW, Huang XT, Wang RJ, Lv J, Li YL, Zhang ZF, Liu BZ, Lu W, Hui YY, Liang J, Zhou ZC, Hou R, Li X, Liu YC, Li HD, Ning XH, Lin Y, Zhao L, Xing Q, Dou JZ, Li YP, Mao JX, Guo HB, Dou HQ, Li TQ, Mu C, Jiang WK, Fu Q, Fu XT, Miao Y, Liu J, Yu Q, Li RJ, Liao H, Li X, Kong YF, Jiang Z, Chourrout D, Li RQ, Bao ZM (2017) Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol 1:0120

    Article  Google Scholar 

  • Wang Z, Lin HF (2004) Nanos maintains germline stem cell self-renewal by preventing differentiation. Science 303:2016–2019

    Article  CAS  PubMed  Google Scholar 

  • Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu R, Li Q, Yu H, Kong L (2018) Oocyte maturation and origin of the germline as revealed by the expression of Nanos-like in the Pacific oyster Crassostrea gigas. Gene 663:41–50

    Article  CAS  PubMed  Google Scholar 

  • Zeng F, Huang F, Guo J, Hu X, Liu C, Wang H (2015) Emerging methods to generate artificial germ cells from stem cells. Biol Reprod 92:89

    Article  PubMed  Google Scholar 

  • Zhang J, Han X, Wang J, Liu B-Z, Wei J-L, Zhang W-J, Sun Z-H, Chang Y-Q (2019) Molecular cloning and sexually dimorphic expression analysis of nanos2 in the sea urchin Mesocentrotus nudus. Int J Mol Sci 20:2705

    Article  CAS  PubMed Central  Google Scholar 

  • Zhang M, Wei H, Liu T, Li W, Li Y, Wang S, Xing Q, Hu X, Zhang L, Bao Z (2020) Potential GnRH and steroidogenesis pathways in the scallop Patinopecten yessoensis. J Steroid Biochem Mol Biol 204:105756

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was funded by the National Key Research and Development Project (2018YFD0900200), National Natural Science Foundation of China (32172967 and 31871499), Project of Sanya Yazhouwan Science and Technology City Management Foundation (SKJC-KJ-2019KY01), and Taishan Scholar Project Fund of Shandong Province of China.

Author information

Authors and Affiliations

  1. MOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao, China

    Liangjie Liu, Tian Liu, Shaoxuan Wu, Yajuan Li, Huilan Wei, Lijing Zhang, Ya Shu, Yaxin Yang, Qiang Xing, Shi Wang & Lingling Zhang

  2. Laboratory for Marine Biology and Biotechnology & Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, China

    Qiang Xing, Shi Wang & Lingling Zhang

  3. Laboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya, China

    Shi Wang

Authors
  1. Liangjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaoxuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yajuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huilan Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lijing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ya Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yaxin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qiang Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lingling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Liangjie Liu: investigation, formal analysis, and writing — original draft; Lingling Zhang: conceptualization, supervision, writing — review & editing; Shaoxuan Wu, Yajuan Li, Huilan Wei: investigation. Tian Liu, Lijing Zhang, Ya Shu, Yaxin Yang, Qiang Xing: resources; Shi Wang: project administration.

Corresponding author

Correspondence to Lingling Zhang.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, L., Liu, T., Wu, S. et al. Discovery of Nanos1 and Nanos2/3 as Germ Cell Markers During Scallop Gonadal Development. Mar Biotechnol 24, 408–416 (2022). https://doi.org/10.1007/s10126-022-10124-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-022-10124-0

Keywords

Search

Navigation