Abstract
Germ cell-specific genes play an important role in establishing the reproductive system in sexual organisms and have been used as valuable markers for studying gametogenesis and sex differentiation. Previously, we isolated a vasa transcript as a germ cell marker to trace the origin and migration of germ cells in the oriental river prawn Macrobrachium nipponense. Here, we identified a new germ cell-specific marker MnTdrd RNA and assessed its temporal and spatial expression during oogenesis and embryogenesis. MnTdrd transcripts were expressed in high abundance in unfertilized eggs and embryos at cleavage stage and then dropped significantly during late embryogenesis, suggesting that MnTdrd mRNA is maternally inherited. In situ hybridization of ovarian tissue showed that MnTdrd mRNA was initially present in the cytoplasm of previtellogenic oocyte and localized to the perinuclear region as the accumulation of yolk in vitellogenic oocyte. Whole-mount in situ hybridization of embryos showed that MnTdrd-positive signals were only localized in one blastomere until 16-cell stage. In the blastula, there were approximately 16 MnTdrd-positive blastomeres. During embryonized-zoea stage, the MnTdrd-positive cells aggregated as a cluster and migrated to the genital rudiment which would develop into primordial germ cells (PGCs). The localized expression pattern of MnTdrd transcripts resembled that of the previously identified germ cell marker vasa, supporting the preformation mode of germ cell specification. Therefore, we concluded that MnTdrd, together with vasa, is a component of the germ plasm and might have critical roles in germ cell formation and differentiation in the prawn. Thus, MnTdrd can be used as a novel germ cell marker to trace the origin and migration of germ cells.
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References
Aoki Y, Nagao I, Saito D, Ebe Y, Kinjo M, Tanaka M (2008) Temporal and spatial localization of three germline-specific proteins in medaka. Dev Dyn 237:800–807. https://doi.org/10.1002/dvdy.21448
Arkov AL (2006) The role of Tudor domains in germline development and polar granule architecture. Development 133:4053–4062
Boswell RE, Mahowald AP (1985) Tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43:97–104
Chen C, Nott TJ, Jin J, Pawson T (2011) Deciphering arginine methylation: Tudor tells the tale. Nat Rev Mol Cell Biol 12:629–642
Chen Y, Zhu Q, Chen H, Zhu X, Cui Z, Qiu G (2012) The morphological and histological observation of embryonic development in the oriental river prawn Macrobrachium nipponense. J Shanghai Ocean Univ 21:33–37
Chuma S, Hiyoshi M, Yamamoto A, Hosokawa M, Takamune K, Nakatsuji N (2003) Mouse tudor repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech Dev 120:979–990. https://doi.org/10.1016/s0925-4773(03)00181-3
Chuma S et al (2006) Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc Natl Acad Sci U S A 103:15894–15899. https://doi.org/10.1073/pnas.0601878103
Fabioux C, Pouvreau S, Le Roux F, Huvet A (2004) The oyster vasa-like gene: a specific marker of the germline in Crassostrea gigas. Biochem Biophys Res Commun 315:897–904. https://doi.org/10.1016/j.bbrc.2004.01.145
Golumbeski GS, Bardsley A, Tax F, Boswell RE (1991) Tudor, a posterior-group gene of Drosophila melanogaster, encodes a novel protein and an mRNA localized during mid-oogenesis. Genes Dev 5:2060–2070. https://doi.org/10.1101/gad.5.11.2060
Han K, Chen S, Cai M, Jiang Y, Wang Y (2018) Nanos3 not nanos1 and nanos2 is a germ cell marker gene in large yellow croaker during embryogenesis. Comp Biochem Physiol B Biochem Mol Biol 218:13–22
Hosokawa M, Shoji M, Kitamura K, Tanaka T, Noce T, Chuma S, Nakatsuji N (2007) Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev Biol 301:38–52. https://doi.org/10.1016/j.ydbio.2006.10.046
Huang HY et al (2011) Tdrd1 acts as a molecular scaffold for Piwi proteins and piRNA targets in zebrafish. EMBO J 30:3298–3308. https://doi.org/10.1038/emboj.2011.228
Huang JQ, Chen SL, Liu Y, Shao CW, Lin F, Wang N, Hu QM (2014) Molecular characterization, sexually dimorphic expression, and functional analysis of 3'-untranslated region of vasa gene in half-smooth tongue sole (Cynoglossus semilaevis). Theriogenology 82:213–224. https://doi.org/10.1016/j.theriogenology.2014.03.017
Ito S et al (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333:1300–1303
Lasko P (2010) Tudor domain. Curr Biol 20:R666–R667
Li M et al (2011) Differential conservation and divergence of fertility genes boule and dazl in the rainbow trout. PLoS One 6. https://doi.org/10.1371/journal.pone.0015910
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Ma KY, Qiu GF, Feng JB, Li JL (2012) Transcriptome analysis of the Oriental River Prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS One 7:11. https://doi.org/10.1371/journal.pone.0039727
Ma KY, Tian XQ, Liu ZQ, Qiu GF (2019) Observations on the embryonic development of the oriental river prawn Macrobrachium nipponense (De Haan, 1849) (Decapoda: Caridea: Palaemonidae). J Crustac Biol 39:261–266. https://doi.org/10.1093/jcbiol/ruz006
Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP (2003) The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 28:69–74. https://doi.org/10.1016/s0968-0004(03)00004-5
Mishima Y, Giraldez AJ, Takeda Y, Fujiwara T, Sakamoto H, Schier AF, Inoue K (2006) Differential regulation of germline mRNAs in soma and germ cells by Zebrafish miR-430. Curr Biol 16:2135–2142
Olsen LC, Aasland R, Fjose A (1997) A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66:95–105
Pan J (2005) RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis. Development 132:4029–4039
Pek JW, Anand A, Kai T (2012) Tudor domain proteins in development. Development 139:2255–2266
Peng JX, Xie JL, Zhou L, Hong YH, Gui JF (2009) Evolutionary conservation of Dazl genomic organization and its continuous and dynamic distribution throughout germline development in gynogenetic Gibel carp. J Exp Zool Part B Mol Dev Evolut 312B:855–871. https://doi.org/10.1002/jez.b.21301
Presslauer C, Nagasawa K, Fernandes JMO, Babiak I (2012) Expression of vasa and nanos3 during primordial germ cell formation and migration in Atlantic cod (Gadus morhua L.). Theriogenology 78:1262–1277. https://doi.org/10.1016/j.theriogenology.2012.05.022
Qiu GF, Chen Y, Cui Z, Zhu XL (2013) Localization of germline marker vasa homolog RNA to a single blastomere at early cleavage stages in the oriental river prawn Macrobrachium nipponense: evidence for germ cell specification by preformation. Gene 513:53–62. https://doi.org/10.1016/j.gene.2012.10.079
Saga Y (2008) Mouse germ cell development during embryogenesis. Curr Opin Genet Dev 18:337–341
Santos AC, Lehmann R (2004) Germ cell specification and migration in Drosophila and beyond. Curr Biol 14:R578–R589
Sellars MJ, Trewin C, McWilliam SM, Glaves RSE, Hertzler PL (2015) Transcriptome profiles of Penaeus (Marsupenaeus) japonicus animal and vegetal half-embryos: identification of sex determination, germ line, mesoderm, and other developmental genes. Mar Biotechnol 17:252–265. https://doi.org/10.1007/s10126-015-9613-4
Shih TW (1995) Reproductive cycle of ovarian development and vitellogenin profiles in the freshwater prawns, Macrobrachium rosenbergii. Invertebr Reprod Dev 27:11–20
Shoji M et al (2009) The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell 17:775–787. https://doi.org/10.1016/j.devcel.2009.10.012
Siomi MC, Mannen T, Siomi H (2010) How does the royal family of Tudor rule the PIWI-interacting RNA pathway? Genes Dev 24:636–646
Strasser MJ, Mackenzie NC, Dumstrei K, Nakkrasae LI, Stebler J, Raz E (2008) Control over the morphology and segregation of Zebrafish germ cell granules during embryonic development. BMC Dev Biol 8:58. https://doi.org/10.1186/1471-213x-8-58
Ubeda-Manzanaro M, Rebordinos L, Sarasquete C (2014) Cloning and characterization of Vasa gene expression pattern in adults of the Lusitanian toadfish Halobatrachus didactylus. Aquat Biol 21:37−47. https://doi.org/10.3354/ab00565
Vasileva A, Tiedau D, Firooznia A, Müller-Reichert T, Jessberger R (2009) Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Curr Biol 19:630–639
Wu HR, Chen YT, Su YH, Luo YJ, Holland LZ, Yu JK (2011) Asymmetric localization of germline markers Vasa and Nanos during early development in the amphioxus Branchiostoma floridae. Dev Biol 353:147–159. https://doi.org/10.1016/j.ydbio.2011.02.014
Yabuta Y, Ohta H, Abe T, Kurimoto K, Chuma S, Saitou M (2011) TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J Cell Biol 192:781–795. https://doi.org/10.1083/jcb.201009043
Zhang QJ, Luo YJ, Wu HR, Chen YT, Yu JK (2013) Expression of germline markers in three species of amphioxus supports a preformation mechanism of germ cell development in cephalochordates. Evodevo 4. https://doi.org/10.1186/2041-9139-4-17
Zhao J, Wang B, Yu H, Wang Y, Liu X, Zhang Q (2018) tdrd1 is a germline-specific and sexually dimorphically expressed gene in Paralichthys olivaceus. Gene 673:61–69. https://doi.org/10.1016/j.gene.2018.06.043
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This research was funded by the National Key R & D Program of China (project number 2018YFD0900201).
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Yao-Ting Dong, Hai-Yang Feng, and Xiao-Qing Tian are the co-first authors.
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Dong, YT., Feng, HY., Tian, XQ. et al. Identification of a novel germ cell marker MnTdrd from the oriental river prawn Macrobrachium nipponense. Dev Genes Evol 231, 11–19 (2021). https://doi.org/10.1007/s00427-020-00671-8
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DOI: https://doi.org/10.1007/s00427-020-00671-8