The asymmetric localization of biomolecules is critical for body plan development. One of the most popular model organisms for early embryogenesis studies is Xenopus laevis but there is a lack of information in other animal species. Here, we compared the early development of two amphibian species-the frog X. laevis and the axolotl Ambystoma mexicanum. This study aimed to identify asymmetrically localized RNAs along the animal-vegetal axis during the early development of A. mexicanum. For that purpose, we performed spatial transcriptome-wide analysis at low resolution, which revealed dynamic changes along the animal-vegetal axis classified into the following categories: profile alteration, de novo synthesis and degradation. Surprisingly, our results showed that many of the vegetally localized genes, which are important for germ cell development, are degraded during early development. Furthermore, we assessed the motif presence in UTRs of degraded mRNAs and revealed the enrichment of several motifs in RNAs of germ cell markers. Our results suggest novel reorganization of the transcriptome during embryogenesis of A. mexicanum to converge to the similar developmental pattern as the X. laevis.

Department of Zoology Faculty of Science Charles University Prague Czechia

Laboratory of Gene Expression Institute of Biotechnology of the Czech Academy of Sciences Vestec Czechia

Zobrazit více v PubMed

Abe K., Funaya S., Tsukioka D., Kawamura M., Suzuki Y., Suzuki M., et al. (2018). Minor zygotic gene activation is essential for mouse preimplantation development. PNAS 115, E6780–E6788. 10.1073/pnas.1804309115 PubMed DOI PMC

Agius E., Oelgeschlager M., Wessely O., Kemp C., De Robertis E. M. (2000). Endodermal Nodal-related signals and mesoderm induction in Xenopus. Development 127, 1173–1183. 10.1242/dev.127.6.1173 PubMed DOI PMC

Aoki F., Worrad D. M., Schultz R. M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296–307. 10.1006/dbio.1996.8466 PubMed DOI

Bachvarova R. F., Masi T., Drum M., Parker N., Mason K., Patient R., et al. (2004). Gene expression in the axolotl germ line: axdazl, axvh, axoct-4, and axkit. Dev. Dyn. 231, 871–880. 10.1002/dvdy.20195 PubMed DOI

Bailey T. L. (2021). STREME: accurate and versatile sequence motif discovery. Bioinformatics 37, 2834–2840. 10.1093/bioinformatics/btab203 PubMed DOI PMC

Behnia R., Panic B., Whyte J. R. C., Munro S. (2004). Targeting of the arf-like GTPase Arl3p to the Golgi requires N-terminal acetylation and the membrane protein Sys1p. Nat. Cell Biol. 6, 405–413. 10.1038/ncb1120 PubMed DOI

Benoit Bouvrette L. P., Bovaird S., Blanchette M., Lécuyer E. (2020). oRNAment: a database of putative RNA binding protein target sites in the transcriptomes of model species. Nucleic Acids Res. 48, D166-D173–D173. 10.1093/nar/gkz986 PubMed DOI PMC

Biswas A., Brown C. M. (2014). Scan for motifs: a webserver for the analysis of post-transcriptional regulatory elements in the 3′ untranslated regions (3′ UTRs) of mRNAs. BMC Bioinforma. 15, 174. 10.1186/1471-2105-15-174 PubMed DOI PMC

Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC

Bordzilovskaya N. P., Dettlaff T. A. (1979). Table of stages of the normal development of axolotl embryos. 1-6. Axolotl Newsl. 7, 2–22.

Bouniol C., Nguyen E., Debey P. (1995). Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp. Cell Res. 218, 57–62. 10.1006/excr.1995.1130 PubMed DOI

Brannon M., Gomperts M., Sumoy L., Moon R. T., Kimelman D. (1997). A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 11, 2359–2370. 10.1101/gad.11.18.2359 PubMed DOI PMC

Bray N. L., Pimentel H., Melsted P., Pachter L. (2016). Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527. 10.1038/nbt.3519 PubMed DOI

Caulet S., Pelczar H., Andéol Y. (2010). Multiple sequences and factors are involved in stability/degradation of Awnt-1, Awnt-5A and Awnt-5B mRNAs during axolotl development. Development growth and differentiation 52 (2) 209–222. 10.1111/j.1440-169X.2009.01156.x PubMed DOI

Chan A. P., Kloc M., Etkin L. D. (1999). Fatvg encodes a new localized RNA that uses a 25-nucleotide element (FVLE1) to localize to the vegetal cortex of Xenopus oocytes. Development 126, 4943–4953. 10.1242/dev.126.22.4943 PubMed DOI

Chang P., Torres J., Lewis R. A., Mowry K. L., Houliston E., King M. L. (2004). Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol. Biol. Cell. 15, 4669–4681. 10.1091/mbc.e04-03-0265 PubMed DOI PMC

Chen Y., Wang X. (2020). miRDB: an online database for prediction of functional microRNA targets. Nucleic Acids Res. 48, D127-D131–D131. 10.1093/nar/gkz757 PubMed DOI PMC

Clauβen M., Tarbashevich K., Pieler T. (2011). Functional dissection of the RNA signal sequence responsible for vegetal localization of XGrip2.1 mRNA in Xenopus oocytes. RNA Biol. 8, 873–882. 10.4161/rna.8.5.16028 PubMed DOI

Cook K. B., Kazan H., Zuberi K., Morris Q., Hughes T. R. (2011). RBPDB: a database of RNA-binding specificities. Nucleic Acids Res. 39, D301–D308. 10.1093/nar/gkq1069 PubMed DOI PMC

Dassi E., Re A., Leo S., Tebaldi T., Pasini L., Peroni D., et al. (2014). AURA 2: empowering discovery of post-transcriptional networks. Transl. (Austin) 2, e27738. 10.4161/trla.27738 PubMed DOI PMC

De Domenico E., Owens N. D. L., Grant I. M., Gomes-Faria R., Gilchrist M. J. (2015). Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing. Dev. Biol. 408, 252–268. 10.1016/j.ydbio.2015.06.010 PubMed DOI PMC

Delarue M., Sáez F. J., Johnson K. E., Boucaut J. C. (1997). Fates of the blastomeres of the 32-cell stage Pleurodeles waltl embryo. Dev. Dyn. 210, 236–248. 10.1002/(SICI)1097-0177(199711)210:3<236::AID-AJA5>3.0.CO;2-H PubMed DOI

Deshler J. O., Highett M. I., Schnapp B. J. (1997). Localization of Xenopus Vg1 mRNA by vera protein and the endoplasmic reticulum. Science 276, 1128–1131. 10.1126/science.276.5315.1128 PubMed DOI

Dumont J. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–179. 10.1002/jmor.1051360203 PubMed DOI

Ems-McClung S. C., Emch M., Zhang S., Mahnoor S., Weaver L. N., Walczak C. E. (2019). RanGTP induces an effector gradient of XCTK2 and importin α/β for spindle microtubule cross-linking. J. Cell Biol. 219, e201906045. 10.1083/jcb.201906045 PubMed DOI PMC

Field C. M., Pelletier J. F., Mitchison T. J. (2019). Disassembly of actin and keratin networks by aurora B kinase at the midplane of cleaving Xenopus laevis eggs. Curr. Biol. 29, 1999–2008. 10.1016/j.cub.2019.05.016 PubMed DOI PMC

Flachsova M., Sindelka R., Kubista M. (2013). Single blastomere expression profiling of Xenopus laevis embryos of 8 to 32-cells reveals developmental asymmetry. Sci. Rep. 3, 2278. 10.1038/srep02278 PubMed DOI PMC

Forristall C., Pondel M., Chen L., King M. L. (1995). Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Dev 121, 201–208. 10.1242/dev.121.1.201 PubMed DOI

Fuentes R., Mullins M. C., Fernández J. (2018). Formation and dynamics of cytoplasmic domains and their genetic regulation during the zebrafish oocyte-to-embryo transition. Mech. Dev. 154, 259–269. 10.1016/j.mod.2018.08.001 PubMed DOI

Ge X., Grotjahn D., Welch E., Lyman-Gingerich J., Holguin C., Dimitrova E., et al. (2014). Hecate/Grip2a acts to reorganize the cytoskeleton in the symmetry-breaking event of embryonic Axis induction. PLOS Genet. 10, e1004422. 10.1371/journal.pgen.1004422 PubMed DOI PMC

Gerber W. V., Yatskievych T. A., Antin P. B., Correia K. M., Conlon R. A., Krieg P. A. (1999). The RNA-binding protein gene, hermes, is expressed at high levels in the developing heart. Mech. Dev. 80, 77–86. 10.1016/s0925-4773(98)00195-6 PubMed DOI

Grant C. E., Bailey T. L., Noble W. S. (2011). FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018. 10.1093/bioinformatics/btr064 PubMed DOI PMC

Guarracino A., Pepe G., Ballesio F., Adinolfi M., Pietrosanto M., Sangiovanni E., et al. (2021). BRIO: a web server for RNA sequence and structure motif scan. Nucleic Acids Res. 49, W67–W71. 10.1093/nar/gkab400 PubMed DOI PMC

Gupta S., Stamatoyannopoulos J. A., Bailey T. L., Noble W. S. (2007). Quantifying similarity between motifs. Genome Biol. 8, R24. 10.1186/gb-2007-8-2-r24 PubMed DOI PMC

Hamatani T., Carter M. G., Sharov A. A., Ko M. S. H. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117–131. 10.1016/s1534-5807(03)00373-3 PubMed DOI

Hashimoto Y., Maegawa S., Nagai T., Yamaha E., Suzuki H., Yasuda K., et al. (2004). Localized maternal factors are required for zebrafish germ cell formation. Dev. Biol. 268, 152–161. 10.1016/j.ydbio.2003.12.013 PubMed DOI

Heasman J., Quarmby J., Wylie C. C. (1984). The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev. Biol. 105, 458–469. 10.1016/0012-1606(84)90303-8 PubMed DOI

Horvay K., Claußen M., Katzer M., Landgrebe J., Pieler T. (2006). Xenopus Dead end mRNA is a localized maternal determinant that serves a conserved function in germ cell development. Dev. Biol. 291, 1–11. 10.1016/j.ydbio.2005.06.013 PubMed DOI

Houston D. W., Zhang J., Maines J. Z., Wasserman S. A., King M. L. (1998). A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development 125, 171–180. 10.1242/dev.125.2.171 PubMed DOI

Howley C., Ho R. K. (2000). mRNA localization patterns in zebrafish oocytes. Mech. Dev. 92, 305–309. 10.1016/s0925-4773(00)00247-1 PubMed DOI

Iegorova V., Naraine R., Psenicka M., Zelazowska M., Sindelka R. (2022). Comparison of RNA localization during oogenesis within Acipenser ruthenus and Xenopus laevis . Front. Cell. Dev. Biol. 10, 982732. 10.3389/fcell.2022.982732 PubMed DOI PMC

Ikenishi K., Nieuwkoop P. D. (1978). Location and ultrastructure of primordial germ cells (PGCs) in Ambystoma mexicanum . Dev. Growth Differ. 20, 1–9. 10.1111/j.1440-169X.1978.00001.x PubMed DOI

Jiang P., Nelson J. D., Leng N., Collins M., Swanson S., Dewey C. N., et al. (2017). Analysis of embryonic development in the unsequenced axolotl: waves of transcriptomic upheaval and stability. Dev. Biol. Xenopus Genomes 426, 143–154. 10.1016/j.ydbio.2016.05.024 PubMed DOI PMC

Johnson A. D., Bachvarova R. F., Drum M., Masi T. (2001). Expression of axolotl DAZL RNA, a marker of germ plasm: widespread maternal RNA and onset of expression in germ cells approaching the gonad. Dev. Biol. 234, 402–415. 10.1006/dbio.2001.0264 PubMed DOI

Kirilenko P., Weierud F. K., Zorn A. M., Woodland H. R. (2008). The efficiency of Xenopus primordial germ cell migration depends on the germplasm mRNA encoding the PDZ domain protein Grip2. Differentiation 76, 392–403. 10.1111/j.1432-0436.2007.00229.x PubMed DOI

Kloc M., Etkin L. D. (1995). Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121, 287–297. 10.1242/dev.121.2.287 PubMed DOI

Knaut H., Pelegri F., Bohmann K., Schwarz H., Nüsslein-Volhard C. (2000). Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J. Cell Biol. 149, 875–888. 10.1083/jcb.149.4.875 PubMed DOI PMC

Koebernick K., Loeber J., Arthur P. K., Tarbashevich K., Pieler T. (2010). Elr-type proteins protect Xenopus Dead end mRNA from miR-18-mediated clearance in the soma. PNAS 107, 16148–16153. 10.1073/pnas.1004401107 PubMed DOI PMC

Kofron M., Demel T., Xanthos J., Lohr J., Sun B., Sive H., et al. (1999). Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors. Development 126, 5759–5770. 10.1242/dev.126.24.5759 PubMed DOI

Kopylova E., Noé L., Touzet H. (2012). SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217. 10.1093/bioinformatics/bts611 PubMed DOI

Kosaka K., Kawakami K., Sakamoto H., Inoue K. (2007). Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech. Dev. 124, 279–289. 10.1016/j.mod.2007.01.003 PubMed DOI

Lai W. S., Carballo E., Strum J. R., Kennington E. A., Phillips R. S., Blackshear P. J. (1999). Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol. Cell Biol. 19, 4311–4323. 10.1128/mcb.19.6.4311 PubMed DOI PMC

Lai W. S., Kennington E. A., Blackshear P. J. (2003). Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly(A) ribonuclease. Mol. Cell Biol. 23, 3798–3812. 10.1128/mcb.23.11.3798-3812.2003 PubMed DOI PMC

Laurent M. N., Blitz I. L., Hashimoto C., Rothbächer U., Cho K. W. (1997). The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann’s organizer. Development 124, 4905–4916. 10.1242/dev.124.23.4905 PubMed DOI

Lechner M., Findeiss S., Steiner L., Marz M., Stadler P. F., Prohaska S. J. (2011). Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinforma. 12, 124. 10.1186/1471-2105-12-124 PubMed DOI PMC

Lefresne J., Andéol Y., Signoret J. (1998). Evidence for introduction of a variable G1 phase at the midblastula transition during early development in axolotl. Dev. Growth Differ. 40, 497–508. 10.1046/j.1440-169x.1998.t01-3-00004.x PubMed DOI

Leise W. F., Mueller P. R. (2002). Multiple Cdk1 inhibitory kinases regulate the cell cycle during development. Dev. Biol. 249, 156–173. 10.1006/dbio.2002.0743 PubMed DOI

Levin M., Thorlin T., Robinson K. R., Nogi T., Mercola M. (2002). Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Development 111 (1) 77–89. 10.1016/S0092-8674(02)00939-X PubMed DOI

Litvinov S. V., Velders M. P., Bakker H. A., Fleuren G. J., Warnar S. O. (1994). Ep-CAM: a human epithelial antigen is a homophilic cell-cell adhesion molecule. J. Cell Biol. 125, 437–446. 10.1083/jcb.125.2.437 PubMed DOI PMC

Love M. I., Huber W., Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. 10.1186/s13059-014-0550-8 PubMed DOI PMC

Lu F.-I., Thisse C., Thisse B. (2011). Identification and mechanism of regulation of the zebrafish dorsal determinant. Proc. Natl. Acad. Sci. 108, 15876–15880. 10.1073/pnas.1106801108 PubMed DOI PMC

Lund E., Liu M., Hartley R. S., Sheets M. D., Dahlberg J. E. (2009). Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos. RNA 15, 2351–2363. 10.1261/rna.1882009 PubMed DOI PMC

Lundmark C. (1986). Role of bilateral zones of ingressing superficial cells during gastrulation of Ambystoma mexicanum . Development 97, 47–62. 10.1242/dev.97.1.47 PubMed DOI

Lustig K. D., Kroll K. L., Sun E. E., Kirschner M. W. (1996). Expression cloning of a Xenopus T-related gene (Xombi) involved in mesodermal patterning and blastopore lip formation. Development 122, 4001–4012. 10.1242/dev.122.12.4001 PubMed DOI

McLeay R. C., Bailey T. L. (2010). Motif enrichment analysis: a unified framework and an evaluation on ChIP data. BMC Bioinforma. 11, 165. 10.1186/1471-2105-11-165 PubMed DOI PMC

MacArthur H., Houston D. W., Bubunenko M., Mosquera L., King M. L. (2000). DEADSouth is a germ plasm specific DEAD-box RNA helicase in Xenopus related to eIF4A. Mech. Dev. 95, 291–295. 10.1016/s0925-4773(00)00357-9 PubMed DOI

Mahowald A. P., Hennen S. (1971). Ultrastructure of the “germ plasm” in eggs and embryos of Rana pipiens . Dev. Biol. 24, 37–53. 10.1016/0012-1606(71)90045-5 PubMed DOI

Malm D., Nilssen Ø. (2008). Alpha-mannosidosis. Orphanet J. Rare Dis. 3, 21. 10.1186/1750-1172-3-21 PubMed DOI PMC

Mattei E., Pietrosanto M., Ferrè F., Helmer-Citterich M. (2015). Web-beagle: a web server for the alignment of RNA secondary structures. Nucleic Acids Res. 43, W493–W497. 10.1093/nar/gkv489 PubMed DOI PMC

Melton D. A. (1987). Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328, 80–82. 10.1038/328080a0 PubMed DOI

Moody S. A. (1987a). Fates of the blastomeres of the 16-cell stage Xenopus embryo. Dev. Biol. 119, 560–578. 10.1016/0012-1606(87)90059-5 PubMed DOI

Moody S. A. (1987b). Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev. Biol. 122, 300–319. 10.1016/0012-1606(87)90296-x PubMed DOI

Naraine R., Iegorova V., Abaffy P., Franek R., Soukup V., Psenicka M., et al. (2022). Evolutionary conservation of maternal RNA localization in fishes and amphibians revealed by TOMO-Seq. Dev. Biol. 489, 146–160. 10.1016/j.ydbio.2022.06.013 PubMed DOI

Nath K., Boorech J. L., Beckham Y. M., Burns M. M., Elinson R. P. (2005). Status of RNAs, localized in Xenopus laevis oocytes, in the frogs Rana pipiens and Eleutherodactylus coqui. J. Exp. Zool. 304B, 28–39. 10.1002/jez.b.21020 PubMed DOI

Nishita M., Hashimoto M. K., Ogata S., Laurent M. N., Ueno N., Shibuya H., et al. (2000). Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann’s organizer. Nature 403, 781–785. 10.1038/35001602 PubMed DOI

Nowoshilow S., Tanaka E. M. (2020). Introducing www.axolotl-omics.org – an integrated -omics data portal for the axolotl research community. Exp. Cell Res 394 (1) 112143. 10.1016/j.yexcr.2020.112143 PubMed DOI

O’Brien J., Hayder H., Zayed Y., Peng C. (2018). Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. 9, 402. 10.3389/fendo.2018.00402 PubMed DOI PMC

Oeffinger M., Dlakić M., Tollervey D. (2004). A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev. 18, 196–209. 10.1101/gad.285604 PubMed DOI PMC

Paillard L., Omilli F., Legagneux V., Bassez T., Maniey D., Osborne H. B. (1998). EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos. EMBO J. 17, 278–287. 10.1093/emboj/17.1.278 PubMed DOI PMC

Pantano L., Hutchinson J., Barrera V., Piper M., Khetani R., Daily K., et al. (2023). DEGreport: Report of DEG analysis. Available at: http://lpantano.github.io/DEGreport/ .

Pietrosanto M., Adinolfi M., Casula R., Ausiello G., Ferrè F., Helmer-Citterich M. (2018). BEAM web server: a tool for structural RNA motif discovery. Bioinformatics 34, 1058–1060. 10.1093/bioinformatics/btx704 PubMed DOI PMC

Rapley J., Nicolàs M., Groen A., Regué L., Bertran M. T., Caelles C., et al. (2008). The NIMA-family kinase Nek6 phosphorylates the kinesin Eg5 at a novel site necessary for mitotic spindle formation. J. Cell Sci. 121, 3912–3921. 10.1242/jcs.035360 PubMed DOI PMC

Raudvere U., Kolberg L., Kuzmin I., Arak T., Adler P., Peterson H., et al. (2019). g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 47, W191-W198–W198. 10.1093/nar/gkz369 PubMed DOI PMC

Ray D., Kazan H., Cook K. B., Weirauch M. T., Najafabadi H. S., Li X., et al. (2013). A compendium of RNA-binding motifs for decoding gene regulation. Nature 499, 172–177. 10.1038/nature12311 PubMed DOI PMC

Samwer M., Dehne H.-J., Spira F., Kollmar M., Gerlich D. W., Urlaub H., et al. (2013). The nuclear F-actin interactome of Xenopus oocytes reveals an actin-bundling kinesin that is essential for meiotic cytokinesis. EMBO J. 32, 1886–1902. 10.1038/emboj.2013.108 PubMed DOI PMC

Schreckenberg G. M., Jacobson A. G. (1975). Normal stages of development of the axolotl. Ambystoma mexicanum . Dev. Biol. 42, 391–400. 10.1016/0012-1606(75)90343-7 PubMed DOI

Sekula M., Datta S., Datta S. (2017). optCluster: an R Package for determining the optimal clustering algorithm. Bioinformation 13, 101–103. 10.6026/97320630013101 PubMed DOI PMC

Sindelka R., Abaffy P., Qu Y., Tomankova S., Sidova M., Naraine R., et al. (2018). Asymmetric distribution of biomolecules of maternal origin in the Xenopus laevis egg and their impact on the developmental plan. Sci. Rep. 8, 8315. 10.1038/s41598-018-26592-1 PubMed DOI PMC

Sindelka R., Jonák J., Hands R., Bustin S. A., Kubista M. (2008). Intracellular expression profiles measured by real-time PCR tomography in the Xenopus laevis oocyte. Nucleic Acids Res. 36, 387–392. 10.1093/nar/gkm1024 PubMed DOI PMC

Sindelka R., Sidova M., Svec D., Kubista M. (2010). Spatial expression profiles in the Xenopus laevis oocytes measured with qPCR tomography. Methods, Xenopus Oocytes as Exp. Syst. 51, 87–91. 10.1016/j.ymeth.2009.12.011 PubMed DOI

Skirkanich J., Luxardi G., Yang J., Kodjabachian L., Klein P. S. (2011). An essential role for transcription before the MBT in Xenopus laevis . Dev. Biol. 357, 478–491. 10.1016/j.ydbio.2011.06.010 PubMed DOI PMC

Škugor A., Tveiten H., Johnsen H., Andersen Ø. (2016). Multiplicity of Buc copies in Atlantic salmon contrasts with loss of the germ cell determinant in primates, rodents and axolotl. BMC Evol. Biol. 16, 232. 10.1186/s12862-016-0809-7 PubMed DOI PMC

Soukup V., Tazaki A., Yamazaki Y., Pospisilova A., Epperlein H.-H., Tanaka E. M., et al. (2021). Oral and palatal dentition of axolotl arises from a common tooth-competent zone along the ecto-endodermal boundary. Front. Cell. Dev. Biol. 8, 622308. 10.3389/fcell.2020.622308 PubMed DOI PMC

Stennard F., Carnac G., Gurdon J. B. (1996). The Xenopus T-box gene, Antipodean, encodes a vegetally localised maternal mRNA and can trigger mesoderm formation. Development 122, 4179–4188. 10.1242/dev.122.12.4179 PubMed DOI

Supek F., Bošnjak M., Škunca N., Šmuc T. (2011). REVIGO summarizes and visualizes long lists of gene ontology terms. PLOS ONE 6, e21800. 10.1371/journal.pone.0021800 PubMed DOI PMC

Tam P. P., Zhou S. X. (1996). The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124–132. 10.1006/dbio.1996.0203 PubMed DOI

Tarbashevich K., Koebernick K., Pieler T. (2007). XGRIP2.1 is encoded by a vegetally localizing, maternal mRNA and functions in germ cell development and anteroposterior PGC positioning in Xenopus laevis . Dev. Biol. 311, 554–565. 10.1016/j.ydbio.2007.09.012 PubMed DOI

Theusch E. V., Brown K. J., Pelegri F. (2006). Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm. Dev. Biol. 292, 129–141. 10.1016/j.ydbio.2005.12.045 PubMed DOI

Tran L. D., Hino H., Quach H., Lim S., Shindo A., Mimori-Kiyosue Y., et al. (2012). Dynamic microtubules at the vegetal cortex predict the embryonic axis in zebrafish. Development 139, 3644–3652. 10.1242/dev.082362 PubMed DOI

Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B. C., Remm M., et al. (2012). Primer3--new capabilities and interfaces. Nucleic Acids Res. 40, e115. 10.1093/nar/gks596 PubMed DOI PMC

Van Etten J., Schagat T. L., Hrit J., Weidmann C. A., Brumbaugh J., Coon J. J., et al. (2012). Human Pumilio proteins recruit multiple deadenylases to efficiently repress messenger RNAs. J. Biol. Chem. 287, 36370–36383. 10.1074/jbc.M112.373522 PubMed DOI PMC

Vaur S., Montreau N., Dautry F., Andeol Y. (2003). Differential post-transcriptional regulations of wnt mRNAs upon axolotl meiotic maturation. Int. J. Dev. Biol. 46, 731–739. PubMed

Venkatarama T., Lai F., Luo X., Zhou Y., Newman K., King M. L. (2010). Repression of zygotic gene expression in the Xenopus germline. Development 137, 651–660. 10.1242/dev.038554 PubMed DOI PMC

Vincent J.-P., Oster G. F., Gerhart J. C. (1986). Kinematics of gray crescent formation in Xenopus eggs: the displacement of subcortical cytoplasm relative to the egg surface. Dev. Biol. 113, 484–500. 10.1016/0012-1606(86)90184-3 PubMed DOI

Vincent J.-P., Scharf S. R., Gerhart J. C. (1987). Subcortical rotation in Xenopus eggs: A preliminary study of its mechanochemical basis. Cell Motil. 8, 143–154. 10.1002/cm.970080206 PubMed DOI

Vinot S., Le T., Ohno S., Pawson T., Maro B., Louvet-Vallée S. (2005). Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev. Biol. 282, 307–319. 10.1016/j.ydbio.2005.03.001 PubMed DOI

Voeltz G. K., Steitz J. A. (1998). AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol. Cell. Biol. 18, 7537–7545. 10.1128/mcb.18.12.7537 PubMed DOI PMC

Weidinger G., Stebler J., Slanchev K., Dumstrei K., Wise C., Lovell-Badge R., et al. (2003). dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr. Biol. 13, 1429–1434. 10.1016/s0960-9822(03)00537-2 PubMed DOI

Welch E., Pelegri F. (2015). Cortical depth and differential transport of vegetally localized dorsal and germ line determinants in the zebrafish embryo. BioArchitecture 5, 13–26. 10.1080/19490992.2015.1080891 PubMed DOI PMC

Whitington P. M. D., Dixon K. E. (1975). Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis . Development 33, 57–74. 10.1242/dev.33.1.57 PubMed DOI

Willems P. J., Seo H.-C., Coucke P., Tonlorenzi R., O’Brien J. S. (1999). Spectrum of mutations in fucosidosis. Eur. J. Hum. Genet. 7, 60–67. 10.1038/sj.ejhg.5200272 PubMed DOI

Wong K., Cantley L. C. (1994). Cloning and characterization of a human phosphatidylinositol 4-kinase. J. Biol. Chem. 269, 28878–28884. 10.1016/s0021-9258(19)61989-7 PubMed DOI

Yang J., Tan C., Darken R. S., Wilson P. A., Klein P. S. (2002). Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. Development 129, 5743–5752. 10.1242/dev.00150 PubMed DOI

Zearfoss N. R., Chan A. P., Wu C. F., Kloc M., Etkin L. D. (2004). Hermes is a localized factor regulating cleavage of vegetal blastomeres in Xenopus laevis . Dev. Biol. 267, 60–71. 10.1016/j.ydbio.2003.10.032 PubMed DOI

Zhang J., King M. L. (1996). Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development 122, 4119–4129. 10.1242/dev.122.12.4119 PubMed DOI

Zhou Y., King M. L. (1996). Localization of Xcat-2 RNA, a putative germ plasm component, to the mitochondrial cloud in Xenopus stage I oocytes. Development 122, 2947–2953. 10.1242/dev.122.9.2947 PubMed DOI