Migration of Primordial Germ Cells and Their Relationship of PGCs with Sex Development in Transgenic Germline-specific Fluorescent Freshwater Angelfish (Pterophyllum Scalare)

Overview

Journal Sci Rep

Date 2025 Jan 8

PMID 39779963

Authors

Wai-Kwan Chu

Shih-Chin Huang

Ching-Fong Chang

Jen-Leih Wu

Hong-Yi Gong

Affiliations

Soon will be listed here.

Abstract

Primordial germ cells (PGCs), the progenitors of gametes, are essential for teleost reproduction. While their formation is conserved across teleosts, the activation, migration routes, and localization periods vary among species. In this study, we developed a novel transgenic line, Tg(ddx4:TcCFP13-nanos3), based on the Nile tilapia genome, to label PGCs with clear fluorescent signals in the freshwater angelfish (Pterophyllum scalare). Our findings reveal a complex, multistage PGCs migration process in angelfish, with a significantly extended localization period (168 hpf) compared to zebrafish (24 hpf). Notably, individual differences in PGCs abundance were observed during early somite development. Analysis of PGCs counts and subsequent sexual maturation demonstrate a potential correlation between PGCs abundance and sex determination: 90% of PGCs-reduced individuals developed as males, while 83% of PGCs-rich individuals developed as females. This study provides a foundation for understanding PGCs migration and sex development in freshwater angelfish, offering valuable insights into reproductive biology and ornamental fish species. Furthermore, this in vivo PGCs tracking system for Cichlids provides a versatile tool for advancing research and applications in germ cell biology.

Citing Articles

Review of Methods for Studying Viruses in the Environment and Organisms.

Wang X, Ma T, Chen Z, Liu Y, Wang K, Liu G Viruses. 2025; 17(1).

PMID: 39861875 PMC: 11769461. DOI: 10.3390/v17010086.

References

Jin Y, Robledo D, Hickey J, McGrew M, Houston R . Surrogate broodstock to enhance biotechnology research and applications in aquaculture. Biotechnol Adv. 2021; 49:107756. PMC: 8192414. DOI: 10.1016/j.biotechadv.2021.107756. View

Presslauer C, Bizuayehu T, Razmi K, Fernandes J, Babiak I . See-Thru-Gonad zebrafish line: developmental and functional validation. Reproduction. 2016; 152(5):507-17. DOI: 10.1530/REP-16-0328. View

Kobayashi T, Honryo T, Agawa Y, Sawada Y, Tapia I, Macias K . Gonadogenesis and slow proliferation of germ cells in juveniles of cultured yellowfin tuna, Thunnus albacares. Reprod Biol. 2015; 15(2):106-12. DOI: 10.1016/j.repbio.2015.01.003. View

Ge S, Dan C, Xiong Y, Gong G, Mei J, Guo W . Identifying difference in primordial germ cells between XX female and XY male yellow catfish embryos. Gene. 2020; 761:145037. DOI: 10.1016/j.gene.2020.145037. View

Tzung K, Goto R, Saju J, Sreenivasan R, Saito T, Arai K . Early Depletion of Primordial Germ Cells in Zebrafish Promotes Testis Formation. Stem Cell Reports. 2017; 5(1):156. PMC: 4618446. DOI: 10.1016/j.stemcr.2015.07.001. View

Fan L, Moon J, Wong T, Crodian J, Collodi P . Zebrafish primordial germ cell cultures derived from vasa::RFP transgenic embryos. Stem Cells Dev. 2008; 17(3):585-97. PMC: 2741329. DOI: 10.1089/scd.2007.0178. View

Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T . Stages of embryonic development of the zebrafish. Dev Dyn. 1995; 203(3):253-310. DOI: 10.1002/aja.1002030302. View

Kawakami K . Tol2: a versatile gene transfer vector in vertebrates. Genome Biol. 2007; 8 Suppl 1:S7. PMC: 2106836. DOI: 10.1186/gb-2007-8-s1-s7. View

Aalto A, Olguin-Olguin A, Raz E . Zebrafish Primordial Germ Cell Migration. Front Cell Dev Biol. 2021; 9:684460. PMC: 8260996. DOI: 10.3389/fcell.2021.684460. View

10.

Li M, Tan X, Jiao S, Wang Q, Wu Z, You F . A new pattern of primordial germ cell migration in olive flounder (Paralichthys olivaceus) identified using nanos3. Dev Genes Evol. 2015; 225(4):195-206. DOI: 10.1007/s00427-015-0503-6. View

11.

Liu W, Li S, Li Z, Wang Y, Li X, Zhong J . 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. 2015; 16:971. PMC: 4652418. DOI: 10.1186/s12864-015-2130-z. View

12.

Zhou L, Feng Y, Wang F, Dong X, Jiang L, Liu C . Generation of all-male-like sterile zebrafish by eliminating primordial germ cells at early development. Sci Rep. 2018; 8(1):1834. PMC: 5789895. DOI: 10.1038/s41598-018-20039-3. View

13.

Knaut H, Steinbeisser H, Schwarz H, Nusslein-Volhard C . An evolutionary conserved region in the vasa 3'UTR targets RNA translation to the germ cells in the zebrafish. Curr Biol. 2002; 12(6):454-66. DOI: 10.1016/s0960-9822(02)00723-6. View

14.

Avdesh A, Chen M, Martin-Iverson M, Mondal A, Ong D, Rainey-Smith S . Regular care and maintenance of a zebrafish (Danio rerio) laboratory: an introduction. J Vis Exp. 2012; (69):e4196. PMC: 3916945. DOI: 10.3791/4196. View

15.

Ye D, Zhu L, Zhang Q, Xiong F, Wang H, Wang X . Abundance of Early Embryonic Primordial Germ Cells Promotes Zebrafish Female Differentiation as Revealed by Lifetime Labeling of Germline. Mar Biotechnol (NY). 2019; 21(2):217-228. PMC: 6441407. DOI: 10.1007/s10126-019-09874-1. View

16.

Raz E . Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet. 2003; 4(9):690-700. DOI: 10.1038/nrg1154. View

17.

Schartl M, Schories S, Wakamatsu Y, Nagao Y, Hashimoto H, Bertin C . Sox5 is involved in germ-cell regulation and sex determination in medaka following co-option of nested transposable elements. BMC Biol. 2018; 16(1):16. PMC: 5789577. DOI: 10.1186/s12915-018-0485-8. View

18.

Zhu J, Thompson C . Metabolic regulation of cell growth and proliferation. Nat Rev Mol Cell Biol. 2019; 20(7):436-450. PMC: 6592760. DOI: 10.1038/s41580-019-0123-5. View

19.

Doitsidou M, Reichman-Fried M, Stebler J, Koprunner M, Dorries J, Meyer D . Guidance of primordial germ cell migration by the chemokine SDF-1. Cell. 2002; 111(5):647-59. DOI: 10.1016/s0092-8674(02)01135-2. View

20.

Slanchev K, Stebler J, Goudarzi M, Cojocaru V, Weidinger G, Raz E . Control of Dead end localization and activity--implications for the function of the protein in antagonizing miRNA function. Mech Dev. 2008; 126(3-4):270-7. DOI: 10.1016/j.mod.2008.10.006. View