*Result*: Transcriptome analysis identifies key regulatory genes and temporal expression dynamics during embryonic development in the Japanese eel (Anguilla japonica).
Title:
Transcriptome analysis identifies key regulatory genes and temporal expression dynamics during embryonic development in the Japanese eel (Anguilla japonica).
Authors:
Zhong Z; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; College of Ocean and Earth Sciences, Xiamen University, Xiamen, 361005, China., Luo D; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China., Lu Y; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China., Chen Z; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China., Xi N; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China., Shi S; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China., Chen J; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China., Jiang Y; State Key Laboratory of Mariculture BreedingFisheries College, Jimei University, Xiamen, 361021, China. yhjiang1974@jmu.edu.cn.; Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen, 361021, China. yhjiang1974@jmu.edu.cn.
Source:
Molecular genetics and genomics : MGG [Mol Genet Genomics] 2026 Mar 06; Vol. 301 (1). Date of Electronic Publication: 2026 Mar 06.
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 101093320 Publication Model: Electronic Cited Medium: Internet ISSN: 1617-4623 (Electronic) Linking ISSN: 16174623 NLM ISO Abbreviation: Mol Genet Genomics Subsets: MEDLINE
Imprint Name(s):
Original Publication: Berlin : Springer-Verlag, c2001-
MeSH Terms:
References:
Akkers R, van Heeringen S, Jacobi U, Janssen-Megens E, Françoijs K, Stunnenberg H, Veenstra G (2009) A hierarchy of H3K4me3 and H3K27me3 acquisition in Spatial gene regulation in Xenopus embryos. Dev Cell 17:425–434. https://doi.org/10.1016/j.devcel.2009.08.005. (PMID: 10.1016/j.devcel.2009.08.005197585662746918)
Bicskei B, Taggart J, Glover K, Bron J (2016) Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression. Genet Select Evol 48:16. https://doi.org/10.1186/s12711-016-0200-6. (PMID: 10.1186/s12711-016-0200-6)
Bloomquist R, Fowler T, Sylvester J, Miro R, Streelman J (2017) A compendium of developmental gene expression in lake Malawi cichlid fishes. BMC Dev Biol 17:3. https://doi.org/10.1186/s12861-017-0146-0. (PMID: 10.1186/s12861-017-0146-0281589745291978)
Cheng X, Jiang W, Wang Q, Liu K, Dai W, Liu Y, Shao C, Li Q (2024) Unveiling gene expression dynamics during early mmbryogenesis in Cynoglossus semilaevis: a transcriptomic perspective. Life-Basel 14:13. https://doi.org/10.3390/life14040505. (PMID: 10.3390/life14040505)
Cheong A, Lingutla R, Mager J (2020) Expression analysis of mammalian mitochondrial ribosomal protein genes. Gene Expr Patterns 38:119147. https://doi.org/10.1016/j.gep.2020.119147. (PMID: 10.1016/j.gep.2020.119147329871547726062)
Cui J, Shen X, Zhao H, Nagahama Y (2011) Genome-wide analysis of Sox genes in Medaka (Oryzias latipes) and their expression pattern in embryonic development. Cytogenet Genome Res 134:283–294. https://doi.org/10.1159/000329480. (PMID: 10.1159/00032948021720154)
Fellous A, Earley R, Silvestre F (2019) Identification and expression of Mangrove rivulus (Kryptolebias marmoratus) histone deacetylase (HDAC) and lysine acetyltransferase (KAT) genes. Gene 691:56–69. https://doi.org/10.1016/j.gene.2018.12.057. (PMID: 10.1016/j.gene.2018.12.05730615915)
Fodor E, Zsigmond A, Horváth B, Molnár J, Nagy I, Tóth G, Wilson S, Varga M (2013) Full transcriptome analysis of early dorsoventral patterning in zebrafish. PLoS ONE 8:e70053. https://doi.org/10.1371/journal.pone.0070053. (PMID: 10.1371/journal.pone.0070053239228993726443)
Fu Y, Jia L, Shi Z, Zhang J, Li W (2017) Gene expression patterns regulating embryogenesis based on the integrated de Novo transcriptome assembly of the Japanese flounder. Comp Biochem Physiol D-Genomics Proteom 22:58–66. https://doi.org/10.1016/j.cbd.2017.01.003. (PMID: 10.1016/j.cbd.2017.01.003)
Gao J, Wang Z, Shao K, Fan L, Yang L, Song H, Liu M, Wang Z, Wang X, Zhang Q (2014) Identification and characterization of a Sox2 homolog in the Japanese flounder Paralichthys Olivaceus. Gene 544:165–176. https://doi.org/10.1016/j.gene.2014.04.062. (PMID: 10.1016/j.gene.2014.04.06224786216)
Garriock R, Warkman A, Meadows S, D’Agostino S, Krieg P (2007) Census of vertebrate Wnt genes: isolation and developmental expression of xenopus Wnt2, Wnt3, Wnt9a, Wnt9b, Wnt10a, and Wnt16. Dev Dyn 236:1249–1258. https://doi.org/10.1002/dvdy.21156. (PMID: 10.1002/dvdy.2115617436276)
Gutiérrez V, Arezo M, García G (2007) Characterization of partial hox gene sequences in annual fish of the subfamily cynolebiatinae (Cyprinodontiformes, Rivulidae). Genet Mol Biology 30:494–503. https://doi.org/10.1590/s1415-47572007000300031. (PMID: 10.1590/s1415-47572007000300031)
Hempel A, Kühl S (2014) Comparative expression analysis of cysteine-rich intestinal protein family members Crip 1, 2 and 3 during Xenopus laevis embryogenesis. Int J Dev Biol 58:841–849. https://doi.org/10.1387/ijdb.140270sk. (PMID: 10.1387/ijdb.140270sk26154325)
Henkel C, Dirks R, de Wijze D, Minegishi Y, Aoyama J, Jansen H, Turner B, Knudsen B, Bundgaard M, Hvam K, Boetzer M, Pirovano W, Weltzien F, Dufour S, Tsukamoto K, Spaink H, van den Thillart G (2012) First draft genome sequence of the Japanese eel, Anguilla Japonica. Gene 511:195–201. https://doi.org/10.1016/j.gene.2012.09.064. (PMID: 10.1016/j.gene.2012.09.06423026207)
Hu Z, Liu X (2023) Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of skeletal muscle development in Duck during embryonic stage. Int J Mol Sci 24:5214. https://doi.org/10.3390/ijms24065214. (PMID: 10.3390/ijms240652143698228910049352)
Hu Y, Wang B, Du H (2021) A review on Sox genes in fish. Rev Aquac 13:1986–2003. https://doi.org/10.1111/raq.12554. (PMID: 10.1111/raq.12554)
Huang J, Yang M, Liu J, Tang H, Fan X, Zhang W, Wen X, Luo J (2023) Transcriptome analysis of high mortality phenomena in polyploid fish embryos: an allotriploid embryo case study in hybrid grouper (Epinephelus fuscoguttatus ♀ x Epinephelus lanceolatus ♂). Aquaculture 571:739446. https://doi.org/10.1016/j.aquaculture.2023.739446. (PMID: 10.1016/j.aquaculture.2023.739446)
Ichikawa K, Kubota Y, Nakamura T, Weng J, Tomida T, Saito H, Takekawa M (2015) MCRIP1, an ERK substrate, mediates ERK-induced gene Silencing during epithelial-mesenchymal transition by regulating the co-repressor CtBP. Mol Cell 58:35–46. https://doi.org/10.1016/j.molcel.2015.01.023. (PMID: 10.1016/j.molcel.2015.01.02325728771)
Kawakami T, Yamada Y, Tanaka S, Tsukamoto K (2017) Prolongation of somitogenesis in two anguilliform species, the Japanese eel Anguilla Japonica and Pike eel Muraenesox cinereus, with refined descriptions of their early development. J Fish Biol 90:1533–1547. https://doi.org/10.1111/jfb.13249. (PMID: 10.1111/jfb.1324928097653)
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310. https://doi.org/10.1002/aja.1002030302. (PMID: 10.1002/aja.10020303028589427)
Li Z, Lin F, Zhong C, Wang S, Xue X, Shao Y (2022) Single-Cell sequencing to unveil the mystery of embryonic development. Adv Biol 6(2):2101151. https://doi.org/10.1002/adbi.202101151. (PMID: 10.1002/adbi.202101151)
Liu L, Zhang J, Guo F, Zhang T (2010) Biological characteristics of embryo and larval development in Japanese eel under artificial incubation. J Fish China 34:1800–1811 (in Chinese).
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2<sup>-∆∆CT</sup> method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262. (PMID: 10.1006/meth.2001.126211846609)
Luo M, Shi X, Guo J, Lin K, Zhu W, Fu J, Wang L, Dong Z (2023) Deep Spatiotemporal transcriptome analysis provides new insights into early development of Koi carp (Cyprinus Carpio var. Koi). Aquaculture 575:739767. https://doi.org/10.1016/j.aquaculture.2023.739767. (PMID: 10.1016/j.aquaculture.2023.739767)
Lyon R, Davis A, Scemama J (2013) Spatio-temporal expression patterns of anterior hox genes during nile tilapia (Oreochromis niloticus) embryonic development. Gene Expr Patterns 13:104–108. https://doi.org/10.1016/j.gep.2013.01.004. (PMID: 10.1016/j.gep.2013.01.00423376031)
Ma H, Martin K, Dixon D, Hernandez A, Weber G (2019) Transcriptome analysis of egg viability in rainbow trout, Oncorhynchus Mykiss. BMC Genom 20:319. https://doi.org/10.1186/s12864-019-5690-5. (PMID: 10.1186/s12864-019-5690-5310290846486991)
Martin K, Moravek C, Flannery J (2009) Embryonic staging series for the beach spawning, terrestrially incubating California Grunion Leuresthes tenuis with comparisons to other atherinomorpha. J Fish Biol 75:17–38. https://doi.org/10.1111/j.1095-8649.2009.02260.x. (PMID: 10.1111/j.1095-8649.2009.02260.x20738480)
Mendizábal-Castillero M, Merlo M, Rodríguez M, Arias-Pérez A, Cross I, Rebordinos L (2025) Differential expression pattern of hox genes between larval development and metamorphosis of Senegalese sole (Solea senegalensis, Kaup 1858). Aquaculture 609:742802. https://doi.org/10.1016/j.aquaculture.2025.742802. (PMID: 10.1016/j.aquaculture.2025.742802)
Nguyen T, Nguyen P, Quetin-Leclercq J, Muller M, Huong D, Pham H, Kestemont P (2021) Developmental toxicity of Clerodendrum Cyrtophyllum Turcz ethanol extract in zebrafish embryo. J Ethnopharmacol 267:113538. https://doi.org/10.1016/j.jep.2020.113538. (PMID: 10.1016/j.jep.2020.11353833144170)
Ohta H, Kagawa H, Tanaka H, Okuzawa K, Iinuma N, Hirose K (1997) Artificial induction of maturation and fertilization in the Japanese eel, Anguilla Japonica. Fish Physiol Biochem 17:163–169. https://doi.org/10.1023/a:1007720600588. (PMID: 10.1023/a:1007720600588)
Okamoto T, Kurokawa T, Gen K, Murashita K, Nomura K, Kim S, Matsubara H, Ohta H, Tanaka H (2009) Influence of salinity on morphological deformities in cultured larvae of Japanese eel, Anguilla japonica, at completion of yolk resorption. Aquaculture 293:113–118. https://doi.org/10.1016/j.aquaculture.2009.04.005. (PMID: 10.1016/j.aquaculture.2009.04.005)
Okamura A, Horie N, Mikawa N, Yamada Y, Tsukamoto K (2014) Recent advances in artificial production of glass Eels for conservation of Anguillid eel populations. Ecol Freshw Fish 23:95–110. https://doi.org/10.1111/eff.12086. (PMID: 10.1111/eff.12086)
Okoli A, Blix T, Myhr A, Xu W, Xu X (2022) Sustainable use of CRISPR/Cas in fish aquaculture: the biosafety perspective. Transgenic Res 31:1–21. https://doi.org/10.1007/s11248-021-00274-7. (PMID: 10.1007/s11248-021-00274-734304349)
Okuda Y, Yoda H, Uchikawa M, Furutani-Seiki M, Takeda H, Kondoh H, Kamachi Y (2006) Comparative genomic and expression analysis of group B1 Sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev Dyn 235:811–825. https://doi.org/10.1002/dvdy.20678. (PMID: 10.1002/dvdy.2067816408288)
Park K, Kwak I (2012) Gene expression of ribosomal protein mRNA in Chironomus riparius: effects of endocrine disruptor chemicals and antibiotics. Comp Biochem Physiol C-Toxicol Pharmacol 156:113–120. https://doi.org/10.1016/j.cbpc.2012.05.002. (PMID: 10.1016/j.cbpc.2012.05.002)
Politis S, Servili A, Mazurais D, Zambonino-Infante J, Miest J, Tomkiewicz J, Butts I (2018) Temperature induced variation in gene expression of thyroid hormone receptors and deiodinases of European eel (Anguilla anguilla) larvae. Gen Comp Endocrinol 259:54–65. https://doi.org/10.1016/j.ygcen.2017.11.003. (PMID: 10.1016/j.ygcen.2017.11.00329113916)
Postlethwait J, Yan Y, Desvignes T, Allard C, Titus T, Le François N, Detrich H (2016) Embryogenesis and early skeletogenesis in the Antarctic bullhead notothen, Notothenia coriiceps. Dev Dyn 245:1066–1080. https://doi.org/10.1002/dvdy.24437. (PMID: 10.1002/dvdy.24437275072125065385)
Sarmah S, Muralidharan P, Marrs J (2016) Embryonic ethanol exposure dysregulates BMP and Notch signaling, leading to persistent atrio-ventricular valve defects in zebrafish. PLoS ONE 11:e016120. https://doi.org/10.1371/journal.pone.0161205. (PMID: 10.1371/journal.pone.0161205)
Shaik A, Wee S, Li R, Li Z, Carney T, Mathavan S, Gunaratne J (2014) Functional mapping of the zebrafish early embryo proteome and transcriptome. J Proteome Res 13:5536–5550. https://doi.org/10.1021/pr5005136. (PMID: 10.1021/pr5005136)
Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303. (PMID: 10.1101/gr.123930314597658403769)
Shu L, Zhou Z, Zhou T, Deng M, Dong M, Chen Y, Fu Y, Jin Y, Zhou S, He Z (2015) Ectopic expression of Hoxb4a in hemangioblasts promotes hematopoietic development in early embryogenesis of zebrafish. Clin Exp Pharmacol Physiol 42:1275–1286. https://doi.org/10.1111/1440-1681.12483. (PMID: 10.1111/1440-1681.1248326743678)
Sudo R, Asakura T, Ishikawa T, Hatakeyama R, Fujiwara A, Inoue K, Mochida K, Nomura K (2024) Transcriptome analysis of the Japanese eel (Anguilla japonica) during larval metamorphosis. BMC Genom 25. https://doi.org/10.1186/s12864-024-10459-z.
Takai Y, Chen K, Yoshitake S, Ogino Y, Tashiro K, Shimasaki Y, Oshima Y (2019) Maternal transcriptome analysis of Medaka (Oryzias latipes) embryos by use of mRNA-seq. J Fac Agric Kyushu Univ 64:275–280. https://doi.org/10.5109/2340933. (PMID: 10.5109/2340933)
Tsukamoto K (1992) Discovery of the spawning area for Japanese eel. Nature 356:789–791. https://doi.org/10.1038/356789a0. (PMID: 10.1038/356789a0)
Wang Y, Lou S (2006) Structural and expression analysis of hepatic vitellogenin gene during ovarian maturation in Anguilla Japonica. J Steroid Biochem Mol Biol 100:193–201. https://doi.org/10.1016/j.jsbmb.2006.04.011. (PMID: 10.1016/j.jsbmb.2006.04.01116854581)
Wang H, Wan H, Wu B, Jian J, Ng A, Chung C, Chow E, Zhang J, Wong A, Lai K, Chan T, Zhang E, Wong C (2022) A chromosome-level assembly of the Japanese eel genome, insights into gene duplication and chromosomal reorganization. Gigascience 11:giac120. https://doi.org/10.1093/gigascience/giac120. (PMID: 10.1093/gigascience/giac120364800309730501)
Wu L, Sun W, Zhou J, Li Y, Li J, Song Z, Song C, Xu S, Yue X, Li X (2024) Comparative transcriptome analysis reveals growth and molecular pathway of body color regulation in turbot (Scophthalmus maximus) exposed to different light spectrum. Comp Biochem Physiol D-Genomics Proteom 49:12. https://doi.org/10.1016/j.cbd.2023.101165. (PMID: 10.1016/j.cbd.2023.101165)
Wylie A, Fleming J, Whitener A, Lekven A (2014) Post-transcriptional regulation of wnt8a is essential to zebrafish axis development. Dev Biol 386:53–63. https://doi.org/10.1016/j.ydbio.2013.12.003. (PMID: 10.1016/j.ydbio.2013.12.00324333179)
Xu E, Mager E, Grosell M, Stieglitz J, Hazard E, Hardiman G, Schlenk D (2017) Developmental transcriptomic analyses for mechanistic insights into critical pathways involved in embryogenesis of pelagic Mahimahi (Coryphaena hippurus). PLoS ONE 12. https://doi.org/10.1371/journal.pone.0180454.
Yamada K, Maeno A, Araki S, Kikuchi M, Suzuki M, Ishizaka M, Satoh K, Akama K, Kawabe Y, Suzuki K, Kobayashi D, Hamano N, Kawamura A (2021) An atlas of seven zebrafish hox cluster mutants provides insights into sub/neofunctionalization of vertebrate Hox clusters. Development 148(11):dev198325. https://doi.org/10.1242/dev.198325. (PMID: 10.1242/dev.19832534096572)
Yokoi H, Nishimatsu A, Ozato K, Yoda K (2003) Cloning and embryonic expression of six Wnt genes in the Medaka (Oryzias latipes) with special reference to expression of Wnt5a in the pectoral fin buds. Dev Growth Differ 45:51–61. https://doi.org/10.1046/j.1440-169X.2003.00674.x. (PMID: 10.1046/j.1440-169X.2003.00674.x12630946)
Yu G, Wang L, Han Y, He Q (2012) ClusterProfiler: an R package for comparing biological themes among gene clusters. Omics-a J Integr Biol 16:284–287. https://doi.org/10.1089/omi.2011.0118. (PMID: 10.1089/omi.2011.0118)
Zhang Z, Luo J, Liu H, Wang S, An X, Li X, Wang W (2024) Sonic Hedgehog (shh) gene from Pseudopleuronectes Yokohamae (Teleostei: Pleuronectidae): molecular cloning, characterization, and expression profile during early embryonic, juvenile, and adult stages. J Fish Biol 105:1314–1326. https://doi.org/10.1111/jfb.15839. (PMID: 10.1111/jfb.1583938965864)
Zhao L, Zhu Y, Wu Y, Pi S, Shen L, Fan H (2022a) Nuclear poly(A) binding protein 1 (PABPN1) mediates zygotic genome activation-dependent maternal mRNA clearance during mouse early embryonic development. Nucleic Acids Res 50:458–472. https://doi.org/10.1093/nar/gkab1213. (PMID: 10.1093/nar/gkab1213349046648855302)
Zhao X, Feng B, Wang Q, Tang L, Liu Q, Ma W, Li C, Shao C (2022b) Cloning of the maternal effector gene org and its regulation by LncRNA ORG-AS in Chinese tongue sole (Cynoglossus semilaevis). Int J Mol Sci 23(15):8605. https://doi.org/10.3390/ijms23158605. (PMID: 10.3390/ijms23158605359557399369028)
Zhao Y, Li X, Song G, Li Q, Yan H, Cui Z (2022c) Comparative transcriptome analysis provides novel molecular events for the differentiation and maturation of hepatocytes during the liver development of zebrafish. Biomedicines 10:2264. https://doi.org/10.3390/biomedicines10092264. (PMID: 10.3390/biomedicines10092264361403659496063)
Bicskei B, Taggart J, Glover K, Bron J (2016) Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression. Genet Select Evol 48:16. https://doi.org/10.1186/s12711-016-0200-6. (PMID: 10.1186/s12711-016-0200-6)
Bloomquist R, Fowler T, Sylvester J, Miro R, Streelman J (2017) A compendium of developmental gene expression in lake Malawi cichlid fishes. BMC Dev Biol 17:3. https://doi.org/10.1186/s12861-017-0146-0. (PMID: 10.1186/s12861-017-0146-0281589745291978)
Cheng X, Jiang W, Wang Q, Liu K, Dai W, Liu Y, Shao C, Li Q (2024) Unveiling gene expression dynamics during early mmbryogenesis in Cynoglossus semilaevis: a transcriptomic perspective. Life-Basel 14:13. https://doi.org/10.3390/life14040505. (PMID: 10.3390/life14040505)
Cheong A, Lingutla R, Mager J (2020) Expression analysis of mammalian mitochondrial ribosomal protein genes. Gene Expr Patterns 38:119147. https://doi.org/10.1016/j.gep.2020.119147. (PMID: 10.1016/j.gep.2020.119147329871547726062)
Cui J, Shen X, Zhao H, Nagahama Y (2011) Genome-wide analysis of Sox genes in Medaka (Oryzias latipes) and their expression pattern in embryonic development. Cytogenet Genome Res 134:283–294. https://doi.org/10.1159/000329480. (PMID: 10.1159/00032948021720154)
Fellous A, Earley R, Silvestre F (2019) Identification and expression of Mangrove rivulus (Kryptolebias marmoratus) histone deacetylase (HDAC) and lysine acetyltransferase (KAT) genes. Gene 691:56–69. https://doi.org/10.1016/j.gene.2018.12.057. (PMID: 10.1016/j.gene.2018.12.05730615915)
Fodor E, Zsigmond A, Horváth B, Molnár J, Nagy I, Tóth G, Wilson S, Varga M (2013) Full transcriptome analysis of early dorsoventral patterning in zebrafish. PLoS ONE 8:e70053. https://doi.org/10.1371/journal.pone.0070053. (PMID: 10.1371/journal.pone.0070053239228993726443)
Fu Y, Jia L, Shi Z, Zhang J, Li W (2017) Gene expression patterns regulating embryogenesis based on the integrated de Novo transcriptome assembly of the Japanese flounder. Comp Biochem Physiol D-Genomics Proteom 22:58–66. https://doi.org/10.1016/j.cbd.2017.01.003. (PMID: 10.1016/j.cbd.2017.01.003)
Gao J, Wang Z, Shao K, Fan L, Yang L, Song H, Liu M, Wang Z, Wang X, Zhang Q (2014) Identification and characterization of a Sox2 homolog in the Japanese flounder Paralichthys Olivaceus. Gene 544:165–176. https://doi.org/10.1016/j.gene.2014.04.062. (PMID: 10.1016/j.gene.2014.04.06224786216)
Garriock R, Warkman A, Meadows S, D’Agostino S, Krieg P (2007) Census of vertebrate Wnt genes: isolation and developmental expression of xenopus Wnt2, Wnt3, Wnt9a, Wnt9b, Wnt10a, and Wnt16. Dev Dyn 236:1249–1258. https://doi.org/10.1002/dvdy.21156. (PMID: 10.1002/dvdy.2115617436276)
Gutiérrez V, Arezo M, García G (2007) Characterization of partial hox gene sequences in annual fish of the subfamily cynolebiatinae (Cyprinodontiformes, Rivulidae). Genet Mol Biology 30:494–503. https://doi.org/10.1590/s1415-47572007000300031. (PMID: 10.1590/s1415-47572007000300031)
Hempel A, Kühl S (2014) Comparative expression analysis of cysteine-rich intestinal protein family members Crip 1, 2 and 3 during Xenopus laevis embryogenesis. Int J Dev Biol 58:841–849. https://doi.org/10.1387/ijdb.140270sk. (PMID: 10.1387/ijdb.140270sk26154325)
Henkel C, Dirks R, de Wijze D, Minegishi Y, Aoyama J, Jansen H, Turner B, Knudsen B, Bundgaard M, Hvam K, Boetzer M, Pirovano W, Weltzien F, Dufour S, Tsukamoto K, Spaink H, van den Thillart G (2012) First draft genome sequence of the Japanese eel, Anguilla Japonica. Gene 511:195–201. https://doi.org/10.1016/j.gene.2012.09.064. (PMID: 10.1016/j.gene.2012.09.06423026207)
Hu Z, Liu X (2023) Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of skeletal muscle development in Duck during embryonic stage. Int J Mol Sci 24:5214. https://doi.org/10.3390/ijms24065214. (PMID: 10.3390/ijms240652143698228910049352)
Hu Y, Wang B, Du H (2021) A review on Sox genes in fish. Rev Aquac 13:1986–2003. https://doi.org/10.1111/raq.12554. (PMID: 10.1111/raq.12554)
Huang J, Yang M, Liu J, Tang H, Fan X, Zhang W, Wen X, Luo J (2023) Transcriptome analysis of high mortality phenomena in polyploid fish embryos: an allotriploid embryo case study in hybrid grouper (Epinephelus fuscoguttatus ♀ x Epinephelus lanceolatus ♂). Aquaculture 571:739446. https://doi.org/10.1016/j.aquaculture.2023.739446. (PMID: 10.1016/j.aquaculture.2023.739446)
Ichikawa K, Kubota Y, Nakamura T, Weng J, Tomida T, Saito H, Takekawa M (2015) MCRIP1, an ERK substrate, mediates ERK-induced gene Silencing during epithelial-mesenchymal transition by regulating the co-repressor CtBP. Mol Cell 58:35–46. https://doi.org/10.1016/j.molcel.2015.01.023. (PMID: 10.1016/j.molcel.2015.01.02325728771)
Kawakami T, Yamada Y, Tanaka S, Tsukamoto K (2017) Prolongation of somitogenesis in two anguilliform species, the Japanese eel Anguilla Japonica and Pike eel Muraenesox cinereus, with refined descriptions of their early development. J Fish Biol 90:1533–1547. https://doi.org/10.1111/jfb.13249. (PMID: 10.1111/jfb.1324928097653)
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310. https://doi.org/10.1002/aja.1002030302. (PMID: 10.1002/aja.10020303028589427)
Li Z, Lin F, Zhong C, Wang S, Xue X, Shao Y (2022) Single-Cell sequencing to unveil the mystery of embryonic development. Adv Biol 6(2):2101151. https://doi.org/10.1002/adbi.202101151. (PMID: 10.1002/adbi.202101151)
Liu L, Zhang J, Guo F, Zhang T (2010) Biological characteristics of embryo and larval development in Japanese eel under artificial incubation. J Fish China 34:1800–1811 (in Chinese).
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2<sup>-∆∆CT</sup> method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262. (PMID: 10.1006/meth.2001.126211846609)
Luo M, Shi X, Guo J, Lin K, Zhu W, Fu J, Wang L, Dong Z (2023) Deep Spatiotemporal transcriptome analysis provides new insights into early development of Koi carp (Cyprinus Carpio var. Koi). Aquaculture 575:739767. https://doi.org/10.1016/j.aquaculture.2023.739767. (PMID: 10.1016/j.aquaculture.2023.739767)
Lyon R, Davis A, Scemama J (2013) Spatio-temporal expression patterns of anterior hox genes during nile tilapia (Oreochromis niloticus) embryonic development. Gene Expr Patterns 13:104–108. https://doi.org/10.1016/j.gep.2013.01.004. (PMID: 10.1016/j.gep.2013.01.00423376031)
Ma H, Martin K, Dixon D, Hernandez A, Weber G (2019) Transcriptome analysis of egg viability in rainbow trout, Oncorhynchus Mykiss. BMC Genom 20:319. https://doi.org/10.1186/s12864-019-5690-5. (PMID: 10.1186/s12864-019-5690-5310290846486991)
Martin K, Moravek C, Flannery J (2009) Embryonic staging series for the beach spawning, terrestrially incubating California Grunion Leuresthes tenuis with comparisons to other atherinomorpha. J Fish Biol 75:17–38. https://doi.org/10.1111/j.1095-8649.2009.02260.x. (PMID: 10.1111/j.1095-8649.2009.02260.x20738480)
Mendizábal-Castillero M, Merlo M, Rodríguez M, Arias-Pérez A, Cross I, Rebordinos L (2025) Differential expression pattern of hox genes between larval development and metamorphosis of Senegalese sole (Solea senegalensis, Kaup 1858). Aquaculture 609:742802. https://doi.org/10.1016/j.aquaculture.2025.742802. (PMID: 10.1016/j.aquaculture.2025.742802)
Nguyen T, Nguyen P, Quetin-Leclercq J, Muller M, Huong D, Pham H, Kestemont P (2021) Developmental toxicity of Clerodendrum Cyrtophyllum Turcz ethanol extract in zebrafish embryo. J Ethnopharmacol 267:113538. https://doi.org/10.1016/j.jep.2020.113538. (PMID: 10.1016/j.jep.2020.11353833144170)
Ohta H, Kagawa H, Tanaka H, Okuzawa K, Iinuma N, Hirose K (1997) Artificial induction of maturation and fertilization in the Japanese eel, Anguilla Japonica. Fish Physiol Biochem 17:163–169. https://doi.org/10.1023/a:1007720600588. (PMID: 10.1023/a:1007720600588)
Okamoto T, Kurokawa T, Gen K, Murashita K, Nomura K, Kim S, Matsubara H, Ohta H, Tanaka H (2009) Influence of salinity on morphological deformities in cultured larvae of Japanese eel, Anguilla japonica, at completion of yolk resorption. Aquaculture 293:113–118. https://doi.org/10.1016/j.aquaculture.2009.04.005. (PMID: 10.1016/j.aquaculture.2009.04.005)
Okamura A, Horie N, Mikawa N, Yamada Y, Tsukamoto K (2014) Recent advances in artificial production of glass Eels for conservation of Anguillid eel populations. Ecol Freshw Fish 23:95–110. https://doi.org/10.1111/eff.12086. (PMID: 10.1111/eff.12086)
Okoli A, Blix T, Myhr A, Xu W, Xu X (2022) Sustainable use of CRISPR/Cas in fish aquaculture: the biosafety perspective. Transgenic Res 31:1–21. https://doi.org/10.1007/s11248-021-00274-7. (PMID: 10.1007/s11248-021-00274-734304349)
Okuda Y, Yoda H, Uchikawa M, Furutani-Seiki M, Takeda H, Kondoh H, Kamachi Y (2006) Comparative genomic and expression analysis of group B1 Sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev Dyn 235:811–825. https://doi.org/10.1002/dvdy.20678. (PMID: 10.1002/dvdy.2067816408288)
Park K, Kwak I (2012) Gene expression of ribosomal protein mRNA in Chironomus riparius: effects of endocrine disruptor chemicals and antibiotics. Comp Biochem Physiol C-Toxicol Pharmacol 156:113–120. https://doi.org/10.1016/j.cbpc.2012.05.002. (PMID: 10.1016/j.cbpc.2012.05.002)
Politis S, Servili A, Mazurais D, Zambonino-Infante J, Miest J, Tomkiewicz J, Butts I (2018) Temperature induced variation in gene expression of thyroid hormone receptors and deiodinases of European eel (Anguilla anguilla) larvae. Gen Comp Endocrinol 259:54–65. https://doi.org/10.1016/j.ygcen.2017.11.003. (PMID: 10.1016/j.ygcen.2017.11.00329113916)
Postlethwait J, Yan Y, Desvignes T, Allard C, Titus T, Le François N, Detrich H (2016) Embryogenesis and early skeletogenesis in the Antarctic bullhead notothen, Notothenia coriiceps. Dev Dyn 245:1066–1080. https://doi.org/10.1002/dvdy.24437. (PMID: 10.1002/dvdy.24437275072125065385)
Sarmah S, Muralidharan P, Marrs J (2016) Embryonic ethanol exposure dysregulates BMP and Notch signaling, leading to persistent atrio-ventricular valve defects in zebrafish. PLoS ONE 11:e016120. https://doi.org/10.1371/journal.pone.0161205. (PMID: 10.1371/journal.pone.0161205)
Shaik A, Wee S, Li R, Li Z, Carney T, Mathavan S, Gunaratne J (2014) Functional mapping of the zebrafish early embryo proteome and transcriptome. J Proteome Res 13:5536–5550. https://doi.org/10.1021/pr5005136. (PMID: 10.1021/pr5005136)
Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303. (PMID: 10.1101/gr.123930314597658403769)
Shu L, Zhou Z, Zhou T, Deng M, Dong M, Chen Y, Fu Y, Jin Y, Zhou S, He Z (2015) Ectopic expression of Hoxb4a in hemangioblasts promotes hematopoietic development in early embryogenesis of zebrafish. Clin Exp Pharmacol Physiol 42:1275–1286. https://doi.org/10.1111/1440-1681.12483. (PMID: 10.1111/1440-1681.1248326743678)
Sudo R, Asakura T, Ishikawa T, Hatakeyama R, Fujiwara A, Inoue K, Mochida K, Nomura K (2024) Transcriptome analysis of the Japanese eel (Anguilla japonica) during larval metamorphosis. BMC Genom 25. https://doi.org/10.1186/s12864-024-10459-z.
Takai Y, Chen K, Yoshitake S, Ogino Y, Tashiro K, Shimasaki Y, Oshima Y (2019) Maternal transcriptome analysis of Medaka (Oryzias latipes) embryos by use of mRNA-seq. J Fac Agric Kyushu Univ 64:275–280. https://doi.org/10.5109/2340933. (PMID: 10.5109/2340933)
Tsukamoto K (1992) Discovery of the spawning area for Japanese eel. Nature 356:789–791. https://doi.org/10.1038/356789a0. (PMID: 10.1038/356789a0)
Wang Y, Lou S (2006) Structural and expression analysis of hepatic vitellogenin gene during ovarian maturation in Anguilla Japonica. J Steroid Biochem Mol Biol 100:193–201. https://doi.org/10.1016/j.jsbmb.2006.04.011. (PMID: 10.1016/j.jsbmb.2006.04.01116854581)
Wang H, Wan H, Wu B, Jian J, Ng A, Chung C, Chow E, Zhang J, Wong A, Lai K, Chan T, Zhang E, Wong C (2022) A chromosome-level assembly of the Japanese eel genome, insights into gene duplication and chromosomal reorganization. Gigascience 11:giac120. https://doi.org/10.1093/gigascience/giac120. (PMID: 10.1093/gigascience/giac120364800309730501)
Wu L, Sun W, Zhou J, Li Y, Li J, Song Z, Song C, Xu S, Yue X, Li X (2024) Comparative transcriptome analysis reveals growth and molecular pathway of body color regulation in turbot (Scophthalmus maximus) exposed to different light spectrum. Comp Biochem Physiol D-Genomics Proteom 49:12. https://doi.org/10.1016/j.cbd.2023.101165. (PMID: 10.1016/j.cbd.2023.101165)
Wylie A, Fleming J, Whitener A, Lekven A (2014) Post-transcriptional regulation of wnt8a is essential to zebrafish axis development. Dev Biol 386:53–63. https://doi.org/10.1016/j.ydbio.2013.12.003. (PMID: 10.1016/j.ydbio.2013.12.00324333179)
Xu E, Mager E, Grosell M, Stieglitz J, Hazard E, Hardiman G, Schlenk D (2017) Developmental transcriptomic analyses for mechanistic insights into critical pathways involved in embryogenesis of pelagic Mahimahi (Coryphaena hippurus). PLoS ONE 12. https://doi.org/10.1371/journal.pone.0180454.
Yamada K, Maeno A, Araki S, Kikuchi M, Suzuki M, Ishizaka M, Satoh K, Akama K, Kawabe Y, Suzuki K, Kobayashi D, Hamano N, Kawamura A (2021) An atlas of seven zebrafish hox cluster mutants provides insights into sub/neofunctionalization of vertebrate Hox clusters. Development 148(11):dev198325. https://doi.org/10.1242/dev.198325. (PMID: 10.1242/dev.19832534096572)
Yokoi H, Nishimatsu A, Ozato K, Yoda K (2003) Cloning and embryonic expression of six Wnt genes in the Medaka (Oryzias latipes) with special reference to expression of Wnt5a in the pectoral fin buds. Dev Growth Differ 45:51–61. https://doi.org/10.1046/j.1440-169X.2003.00674.x. (PMID: 10.1046/j.1440-169X.2003.00674.x12630946)
Yu G, Wang L, Han Y, He Q (2012) ClusterProfiler: an R package for comparing biological themes among gene clusters. Omics-a J Integr Biol 16:284–287. https://doi.org/10.1089/omi.2011.0118. (PMID: 10.1089/omi.2011.0118)
Zhang Z, Luo J, Liu H, Wang S, An X, Li X, Wang W (2024) Sonic Hedgehog (shh) gene from Pseudopleuronectes Yokohamae (Teleostei: Pleuronectidae): molecular cloning, characterization, and expression profile during early embryonic, juvenile, and adult stages. J Fish Biol 105:1314–1326. https://doi.org/10.1111/jfb.15839. (PMID: 10.1111/jfb.1583938965864)
Zhao L, Zhu Y, Wu Y, Pi S, Shen L, Fan H (2022a) Nuclear poly(A) binding protein 1 (PABPN1) mediates zygotic genome activation-dependent maternal mRNA clearance during mouse early embryonic development. Nucleic Acids Res 50:458–472. https://doi.org/10.1093/nar/gkab1213. (PMID: 10.1093/nar/gkab1213349046648855302)
Zhao X, Feng B, Wang Q, Tang L, Liu Q, Ma W, Li C, Shao C (2022b) Cloning of the maternal effector gene org and its regulation by LncRNA ORG-AS in Chinese tongue sole (Cynoglossus semilaevis). Int J Mol Sci 23(15):8605. https://doi.org/10.3390/ijms23158605. (PMID: 10.3390/ijms23158605359557399369028)
Zhao Y, Li X, Song G, Li Q, Yan H, Cui Z (2022c) Comparative transcriptome analysis provides novel molecular events for the differentiation and maturation of hepatocytes during the liver development of zebrafish. Biomedicines 10:2264. https://doi.org/10.3390/biomedicines10092264. (PMID: 10.3390/biomedicines10092264361403659496063)
Grant Information:
2024YFD2401002 National Key R&D Program of China; 42476103 National Natural Science Foundation of China; 2024J01704 Natural Science Foundation of Fujian Province; 3502Z202473056 Natural Science Foundation of Xiamen Municipality
Contributed Indexing:
Keywords: Anguilla japonica; Differentially expressed genes; Embryonic development; Gene regulatory network; Transcriptome analysis
Substance Nomenclature:
0 (Fish Proteins)
Entry Date(s):
Date Created: 20260305 Date Completed: 20260307 Latest Revision: 20260307
Update Code:
20260308
DOI:
10.1007/s00438-026-02367-6
PMID:
41787119
Database:
MEDLINE
*Further Information*
*The Japanese eel (Anguilla japonica), a commercially important species, has experienced severe population declines in the wild, underscoring the urgent need to improve artificial breeding techniques. However, the complexity of embryonic development and the limited understanding of its molecular regulatory mechanisms have constrained progress in artificial reproduction. To elucidate the dynamics of gene expression during early development, we conducted a comprehensive transcriptomic analysis of eight key embryonic stages using RNA-Seq. A total of 16,728 differentially expressed genes (DEGs) were identified, with the most pronounced pluripotency-related changes observed during the multicellular-blastula and differentiation-related changes in gastrula-embryo body transitions. Functional enrichment revealed distinct stage-specific pathways: early stages (multicellular) dominated by Notch and Wnt signaling, involved early developmental decisions; mid-stages (blastula to gastrula), with enriched pathways like Cell cycle, supporting rapid cell division; mid-late stages (embryo-body-formation to somite appearance) featured extracellular matrix receptor (ECM-receptor) interaction and focal adhesion, contributing to cell connectivity and tissue morphogenesis; and late stages (muscle-effect to newly-hatched-larvae) highlighted calcium signaling and metabolic pathways, providing signaling and energy support for organogenesis and functional maturation. Weighted gene co-expression network analysis (WGCNA) identified four stage-specific modules that correlated with developmental progression. Additionally, key members of the Sox, Hox, and Wnt transcription factor families were screened and found to exhibit dynamic, stage-specific expression patterns. These factors likely form a synergistic regulatory network that coordinates the entire developmental progression. Collectively, these findings delineate the molecular landscape of A. japonica embryogenesis and establish a crucial baseline transcriptomic resource that will facilitate future investigations into the molecular regulation of early development in this species.
(© 2026. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)*
*Declarations. Conflict of interest: The authors declare that they have no competing interests, either financial or personal, that could have influenced the work reported in this paper. All authors discussed the study design, agreed upon their respective roles, and consented to participate in the study. Declarations of generative AI use: The authors affirm that the entire creative process of this work, including ideation, literature review, data analysis, drafting, and revision, was conducted without the assistance of any generative artificial intelligence technologies.*