The vertebrate pharynx is a key embryonic structure with crucial importance for the metameric organization of the head and face. The pharynx is primarily built upon progressive formation of paired pharyngeal pouches that typically develop in post-oral (mandibular, hyoid and branchial) domains. However, in the early embryos of non-teleost fishes, we have previously identified pharyngeal pouch-like outpocketings also in the pre-oral domain of the cranial endoderm. This pre-oral gut (POG) forms by early pouching of the primitive gut cavity, followed by the sequential formation of typical (post-oral) pharyngeal pouches. Here, we tested the pharyngeal nature of the POG by analysing expression patterns of selected core pharyngeal regulatory network genes in bichir and sturgeon embryos. Our comparison revealed generally shared expression patterns, including Shh, Pax9, Tbx1, Eya1, Six1, Ripply3 or Fgf8, between early POG and post-oral pharyngeal pouches. POG thus shares pharyngeal pouch-like morphogenesis and a gene expression profile with pharyngeal pouches and can be regarded as a pre-mandibular pharyngeal pouch. We further suggest that pre-mandibular pharyngeal pouches represent a plesiomorphic vertebrate trait inherited from our ancestor's pharyngeal metameric organization, which is incorporated in the early formation of the pre-chordal plate of vertebrate embryos.

Department of Zoology Comenius University in Bratislava Bratislava Slovakia

Department of Zoology Faculty of Science Charles University Prague 12844 Prague Czech Republic

Zobrazit více v PubMed

Hopwood N. 2015. Haeckel's embryos: images, evolution, and fraud. Chicago, IL: University of Chicago Press.

Kuratani S, Nobusada Y, Horigome N, Shigetani Y. 2001. Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Phil. Trans. R. Soc. B 356, 1615-1632. (10.1098/rstb.2001.0976) PubMed DOI PMC

Irie N, Kuratani S. 2011. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat. Commun. 2, 248. (10.1038/ncomms1248) PubMed DOI PMC

Piotrowski T, Nüsslein-Volhard C. 2000. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev. Biol. 225, 339-356. (10.1006/dbio.2000.9842) PubMed DOI

Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. 2002. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129, 1061-1073. (10.1242/dev.129.4.1061) PubMed DOI

Choe CP, Crump JG. 2015. Dynamic epithelia of the developing vertebrate face. Curr. Opin Genet. Dev. 32, 66-72. (10.1016/j.gde.2015.02.003) PubMed DOI PMC

Goodrich ES. 1930. Studies on the structure and development of vertebrates I. New York, NY: Dover.

De Beer GR. 1937. The development on the vertebrate skull. Oxford, UK: Clarendon Press.

Gans C, Northcutt RG. 1983. Neural crest and the origin of vertebrates: a new head. Science 220, 268-274. (10.1126/science.220.4594.268) PubMed DOI

Northcutt RG. 2005. The new head hypothesis revisited. J. Exp. Zool. B Mol. Dev. Evol. 304, 274-297. (10.1002/jez.b.21063) PubMed DOI

Satoh N. 2016. Chordate origins and evolution: The molecular evolutionary road to vertebrates. London, UK: Elsevier Inc.

Mallat J. 1996. Ventilation and the origin of jawed vertebrates: a new mouth. Zool. J. Linn. Soc. 117, 329-404. (10.1111/j.1096-3642.1996.tb01658.x) DOI

Shigetani Y, Sugahara F, Kuratani S. 2005. A new evolutionary scenario for the vertebrate jaw. Bioessays 27, 331-338. (10.1002/bies.20182) PubMed DOI

Cerny R, Cattell M, Sauka-Spengler T, Bronner-Fraser M, Yu F, Medeiros DM. 2010. Evidence for the prepattern/cooption model of vertebrate jaw evolution. Proc. Natl Acad. Sci. USA 107, 17 262-17 267. (10.1073/pnas.1009304107) PubMed DOI PMC

Square T, Jandzik D, Romášek M, Cerny R, Medeiros DM. 2017. The origin and diversification of the developmental mechanisms that pattern the vertebrate head skeleton. Dev. Biol. 427, 219-229. (10.1016/j.ydbio.2016.11.014) PubMed DOI

Stundl J, Pospisilova A, Jandzik D, Fabian P, Dobiasova B, Minarik M, Metscher BD, Soukup V, Cerny R. 2019. Bichir external gills arise via heterochronic shift that accelerates hyoid arch development. eLife 8, e43531. (10.7554/eLife.43531) PubMed DOI PMC

Grevellec A, Tucker AS. 2010. The pharyngeal pouches and clefts: development, evolution, structure and derivatives. Semin. Cell Dev. Biol. 21, 325-332. (10.1016/j.semcdb.2010.01.022) PubMed DOI

Shone V, Graham A. 2014. Endodermal/ectodermal interfaces during pharyngeal segmentation in vertebrates. J. Anat. 225, 479-491. (10.1111/joa.12234) PubMed DOI PMC

Graham A, Smith A. 2001. Patterning the pharyngeal arches. Bioessays 23, 54-61. (10.1002/1521-1878(200101)23:1<54::AID-BIES1007>3.0.CO;2-5) PubMed DOI

Willey A. 1891. The later larval development of amphioxus. J. Cell Sci. 44, 183-234. (10.1242/jcs.s2-32.126.183) DOI

Gillis JA, Fritzenwanker JH, Lowe CJ. 2012. A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc. R. Soc. B 279, 237-246. (10.1098/rspb.2011.0599) PubMed DOI PMC

Koop D, Chen J, Theodosiou M, Carvalho JE, Alvarez S, de Lera AR, Holland LZ, Schubert M. 2014. Roles of retinoic acid and Tbx1/10 in pharyngeal segmentation: amphioxus and the ancestral chordate condition. EvoDevo 5, 1-16. (10.1186/2041-9139-5-36) PubMed DOI PMC

Yoshida K, Nakahata A, Treen N, Sakuma T, Yamamoto T, Sasakura Y. 2017. Hox-mediated endodermal identity patterns pharyngeal muscle formation in the chordate pharynx. Development 144, 1629-1634. PubMed

Horigome N, Myojin M, Ueki T, Hirano S, Aizawa S, Kuratani S. 1999. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev. Biol. 207, 287-308. (10.1006/dbio.1998.9175) PubMed DOI

Cerny R, Lwigale P, Ericsson R, Meulemans D, Epperlein HH, Bronner-Fraser M. 2004. Developmental origins and evolution of jaws: new interpretation of ‘maxillary’ and ‘mandibular’. Dev. Biol. 276, 225-236. (10.1016/j.ydbio.2004.08.046) PubMed DOI

Stundl J, Pospisilova A, Matějková T, Psenicka M, Bronner ME, Cerny R. 2020. Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes. Dev. Biol. 467, 14-29. (10.1016/j.ydbio.2020.08.007) PubMed DOI PMC

Veitch E, Begbie J, Schilling TF, Smith MM, Graham A. 1999. Pharyngeal arch patterning in the absence of neural crest. Curr. Biol. 9, 1481-1484. (10.1016/S0960-9822(00)80118-9) PubMed DOI

Simakov O, et al. 2015. Hemichordate genomes and deuterostome origins. Nature 527, 459-465. (10.1038/nature16150) PubMed DOI PMC

Xu PX, Zheng W, Laclef C, Maire P, Maas RL, Peters H, Xu X. 2002. Eya1 is required for the morphogenesis of mammalian thymus, parathyroid and thyroid. Development 129, 3033-3044. (10.1242/dev.129.13.3033) PubMed DOI PMC

Graham A, Richardson J. 2012. Developmental and evolutionary origins of the pharyngeal apparatus. EvoDevo. 3, 24. (10.1186/2041-9139-3-24) PubMed DOI PMC

Ogasawara M, Wada H, Peters H, Satoh N. 1999. Developmental expression of Pax1/9 genes in urochordate and hemichordate gills: insight into function and evolution of the pharyngeal epithelium. Dev. Camb. Engl. 126, 2539-2550. PubMed

Holland ND, Holland LZ, Kozmik Z. 1995. An amphioxus Pax gene, AmphiPax-1, expressed in embryonic endoderm, but not in mesoderm: implications for the evolution of class I paired box genes. Mol. Mar. Biol. Biotechnol. 4, 206-214. (10.1007/BF02921616) PubMed DOI

Kozmik Z, et al. 2007. Pax–Six–Eya–Dach network during amphioxus development: Conservation in vitro but context specificity in vivo. Dev. Biol. 306, 143-159. (10.1016/j.ydbio.2007.03.009) PubMed DOI

Ogasawara M, Shigetani Y, Hirano S, Satoh N, Kuratani S. 2000. Pax1/Pax9-related genes in an Agnathan Vertebrate, Lampetra japonica: expression pattern of LjPax9 implies sequential evolutionary events toward the gnathostome body plan. Dev. Biol. 223, 399-410. (10.1006/dbio.2000.9756) PubMed DOI

Adachi N, Takechi M, Hirai T, Kuratani S. 2012. Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head. Evol. Dev. 14, 257-276. (10.1111/j.1525-142X.2012.00543.x) PubMed DOI

Mise T, Iijima M, Inohaya K, Kudo A, Wada H. 2008. Function of Pax1 and Pax9 in the sclerotome of medaka fish. Genesis 46, 185-192. (10.1002/dvg.20381) PubMed DOI

Sánchez RS, Sánchez SS. 2013. Characterization of pax1, pax9, and uncx sclerotomal genes during Xenopus laevis embryogenesis. Dev. Dyn. 242, 572-579. PubMed

Müller TS, Ebensperger C, Neubüser A, Koseki H, Balling R, Christ B, Wilting J. 1996. Expression of Avian Pax1 and Pax9 Is intrinsically regulated in the pharyngeal endoderm, but depends on environmental influences in the paraxial mesoderm. Dev. Biol. 178, 403-417. (10.1006/dbio.1996.0227) PubMed DOI

Peters H, Neubüser A, Kratochwil K, Balling R. 1998. Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev. 12, 2735-2747. (10.1101/gad.12.17.2735) PubMed DOI PMC

Sato S, Ikeda K, Shioi G, Nakao K, Yajima H, Kawakami K. 2012. Regulation of Six1 expression by evolutionarily conserved enhancers in tetrapods. Dev. Biol. 368, 95-108. (10.1016/j.ydbio.2012.05.023) PubMed DOI

Ishihara T, Ikeda K, Sato S, Yajima H, Kawakami K. 2008. Differential expression of Eya1 and Eya2 during chick early embryonic development. Gene Expr. Patterns 8, 357-367. (10.1016/j.gep.2008.01.003) PubMed DOI

Yamagishi H, Maeda J, Hu T, McAnally J, Conway SJ, Kume T, Meyers EN, Yamagishi C, Srivastava D. 2003. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 17, 269-281. (10.1101/gad.1048903) PubMed DOI PMC

Mahadevan NR, Horton AC, Gibson-Brown JJ. 2004. Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome. Dev. Genes Evol. 214, 559-566. (10.1007/s00427-004-0433-1) PubMed DOI

Sauka-Spengler T, Le Mentec C, Lepage M, Mazan S. 2002. Embryonic expression of Tbx1, a DiGeorge syndrome candidate gene, in the lamprey Lampetrafluviatilis. Gene Expr. Patterns. 2, 99-103. (10.1016/S0925-4773(02)00301-5) PubMed DOI

Choe CP, Crump JG. 2014. Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a. Dev. Camb. 141, 3583-3593. PubMed PMC

Ataliotis P, Ivins S, Mohun TJ, Scambler PJ. 2005. XTbx1 is a transcriptional activator involved in head and pharyngeal arch development in Xenopus laevis. Dev. Dyn. 232, 979-991. (10.1002/dvdy.20276) PubMed DOI

Garg V, Yamagishi C, Hu T, Kathiriya IS, Yamagishi H, Srivastava D. 2001. Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol. 235, 62-73. (10.1006/dbio.2001.0283) PubMed DOI

Chapman DL, et al. 1996. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev. Dyn. 206, 379-390. (10.1002/(SICI)1097-0177(199608)206:4<379::AID-AJA4>3.0.CO;2-F) PubMed DOI

Hitachi K, Danno H, Tazumi S, Aihara Y, Uchiyama H, Okabayashi K, Kondow A, Asashima M. 2009. The Xenopus Bowline/Ripply family proteins negatively regulate the transcriptional activity of T-box transcription factors. Int. J. Dev. Biol. 53, 631-639. (10.1387/ijdb.082823kh) PubMed DOI

Okubo T, Kawamura A, Takahashi J, Yagi H, Morishima M, Matsuoka R, Takada S. 2011. Ripply3, a Tbx1 repressor, is required for development of the pharyngeal apparatus and its derivatives in mice. Development 138, 339-348. (10.1242/dev.054056) PubMed DOI

Okada K, Inohaya K, Mise T, Kudo A, Takada S, Wada H. 2016. Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka. Development 143, 1800-1810. PubMed

Bertrand S, Camasses A, Somorjai I, Belgacem MR, Chabrol O, Escande ML, Pontarotti P, Escriva H. 2011. Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc. Natl Acad. Sci. USA 108, 9160-9165. (10.1073/pnas.1014235108) PubMed DOI PMC

Jandzik D, Hawkins MB, Cattell MV, Cerny R, Square TA, Medeiros DM. 2014. Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head. Development 141, 629-638. (10.1242/dev.097261) PubMed DOI

Walshe J, Mason I. 2003. Fgf signalling is required for formation of cartilage in the head. Dev. Biol. 264, 522-536. (10.1016/j.ydbio.2003.08.010) PubMed DOI

Mahmood R, Kiefer P, Guthrie S, Dickson C, Mason I. 1995. Multiple roles for FGF-3 during cranial neural development in the chicken. Development 121, 1399-1410. (10.1242/dev.121.5.1399) PubMed DOI

Stolte D, Huang R, Christ B. 2002. Spatial and temporal pattern of Fgf-8 expression during chicken development. Anat. Embryol. (Berl) 205, 1-6. (10.1007/s00429-002-0227-z) PubMed DOI

Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB. 2004. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Dev. Camb. Engl. 131, 5703-5716. PubMed

Moore-Scott BA, Manley NR. 2005. Differential expression of Sonic hedgehog along the anterior-posterior axis regulates patterning of pharyngeal pouch endoderm and pharyngeal endoderm-derived organs. Dev. Biol. 278, 323-335. (10.1016/j.ydbio.2004.10.027) PubMed DOI

Stundl J, et al. 2022. Efficient CRISPR mutagenesis in sturgeon demonstrates its utility in large, slow-maturing vertebrates. Front. Cell Dev. Biol. 10, 750833. (10.3389/fcell.2022.750833) PubMed DOI PMC

Minarik M, et al. 2017. Pre-oral gut contributes to facial structures in non-Teleost fishes. Nature 547, 209-212. (10.1038/nature23008) PubMed DOI

Satoh N, et al. 2014. On a possible evolutionary link of the stomochord of hemichordates to pharyngeal organs of chordates. Genesis 52, 925-934. (10.1002/dvg.22831) PubMed DOI PMC

Yu JK, Holland LZ, Jamrich M, Blitz IL, Hollan ND. 2002. AmphiFoxE4, an amphioxus winged helix/forkhead gene encoding a protein closely related to vertebrate thyroid transcription factor-2: expression during pharyngeal development. Evol. Dev. 4, 9-15. (10.1046/j.1525-142x.2002.01057.x) PubMed DOI

Dettlaff TA, Ginsburg AS, Schmalhausen OI. 1993. Sturgeon fishes. Developmental biology and aquaculture. Berlin, Germany: Springer.

Diedhiou S, Bartsch P. 2009. Staging of the early development of Polypterus (Cladistia: actinopterygii). In: Development of non-Teleost fishes (eds YW Kunz-Ramsay, CA Leur, BG Kapoor), pp. 104-109. Enfield: Science Publishers. (https://www.researchgate.net/publication/280713312_Staging_of_The_Early_Development_of_Polypterus_Cladistia_Actinopterygii)

Quinlan R, Martin P, Graham A. 2004. The role of actin cables in directing the morphogenesis of the pharyngeal pouches. Development 131, 593-599. (10.1242/dev.00950) PubMed DOI

Schlosser G. 2021. Vertebrate cranial placodes, 1st edn. New York, NY: CRC Press.

Gibbs MA, Northcutt RG. 2004. Development of the lateral line system in the shovelnose sturgeon. Brain Behav. Evol. 64, 70-84. (10.1159/000079117) PubMed DOI

Lowe CJ, Clarke DN, Medeiros DM, Rokhsar DS, Gerhart J. 2015. The deuterostome context of chordate origins. Nature 520, 456-465. (10.1038/nature14434) PubMed DOI

Cameron CB. 2005. A phylogeny of the hemichordates based on morphological characters. Can. J. Zool. 83, 196-215. (10.1139/z04-190) DOI

Röttinger E, Lowe CJ. 2012. Evolutionary crossroads in developmental biology: hemichordates. Dev. Camb. Engl. 139, 2463-2475. PubMed

Holland ND, Holland LZ, Holland PWH. 2015. Scenarios for the making of vertebrates. Nature 520, 450-455. (10.1038/nature14433) PubMed DOI

Yasui K, Kaji T. 2008. The lancelet and ammocoete mouths. Zoolog. Sci. 25, 1012-1019. (10.2108/zsj.25.1012) PubMed DOI

Hatschek B. 1881. Studien über Entwicklung des Amphioxus. In Arbeiten aus dem zoologischen Institut der Universität Wien und der Zoologischen Station Triest, pp. 1-88. Vienna, Austria.

Holland ND, Paris M, Koop D. 2009. The club-shaped gland of amphioxus: export of secretion to the pharynx in pre-metamorphic larvae and apoptosis during metamorphosis. Acta Zool. 90, 372-379. (10.1111/j.1463-6395.2008.00379.x) DOI

Goodrich ES. 1917. ‘Proboscis pores’ in craniate vertebrates, a suggestion concerning the premandibular somites and hypophysis. Q. J. Microsc. Sci. 62, 539-553.

Stach T. 2002. Minireview: On the homology of the protocoel in Cephalochordata and ‘lower’ Deuterostomia. Acta Zool. 83, 25-31. (10.1046/j.1463-6395.2002.00097.x) DOI

MacBride EW. 1898. The early development of amphioxus. Q. J. Microsc. Sci. s2–40, 589-612.

Tian Q, Zhao F, Zeng H, Zhu M, Jiang B. 2022. Ultrastructure reveals ancestral vertebrate pharyngeal skeleton in yunnanozoans. Science 377, 218-222. (10.1126/science.abm2708) PubMed DOI

Hirschberger C, Gillis JA. 2022. The pseudobranch of jawed vertebrates is a mandibular arch-derived gill. Development 149, dev200184. (10.1242/dev.200184) PubMed DOI PMC

Thiruppathy M, Fabian P, Gillis JA, Crump JG. 2022. Gill developmental program in the teleost mandibular arch. eLife 11, e78170. (10.7554/eLife.78170) PubMed DOI PMC

Dickinson AJG, Sive H. 2006. Development of the primary mouth in Xenopus laevis. Dev. Biol. 295, 700-713. (10.1016/j.ydbio.2006.03.054) PubMed DOI

Dickinson AJG, Sive HL. 2009. The Wnt antagonists Frzb-1 and crescent locally regulate basement membrane dissolution in the developing primary mouth. Development 136, 1071-1081. (10.1242/dev.032912) PubMed DOI PMC

Christiaen L, Jaszczyszyn Y, Kerfant M, Kano S, Thermes V, Joly JS. 2007. Evolutionary modification of mouth position in deuterostomes. Semin. Cell Dev. Biol. 18, 502-511. (10.1016/j.semcdb.2007.06.002) PubMed DOI

Veeman MT, Newman-Smith E, El-Nachef D, Smith WC. 2010. The ascidian mouth opening is derived from the anterior neuropore: reassessing the mouth/neural tube relationship in chordate evolution. Dev. Biol. 344, 138-149. (10.1016/j.ydbio.2010.04.028) PubMed DOI

Kuratani S, Adachi N, Wada N, Oisi Y, Sugahara F. 2013. Developmental and evolutionary significance of the mandibular arch and prechordal/premandibular cranium in vertebrates: revising the heterotopy scenario of gnathostome jaw evolution. J. Anat. 222, 41-55. (10.1111/j.1469-7580.2012.01505.x) PubMed DOI PMC

Soukup V, Horácek I, Cerny R. 2013. Development and evolution of the vertebrate primary mouth. J. Anat. 222, 79-99. (10.1111/j.1469-7580.2012.01540.x) PubMed DOI PMC

von Kupffer C. 1894. Studien zur vergleichenden Entwicklungsgeschichte des Kopfes der Kranioten. München, Germany: J.F. Lehmann.

Parker KM. 1917. The development of the hypophysis cerebri, pre-oral gut, and related structures in the Marsupialia. J. Anat. 51, 181-249. PubMed PMC

Allis EP. 1938. Concerning the development of the prechordal portion of the vertebrate head. J. Anat. 72, 584-607. PubMed PMC

Huettner AF. 1941. Fundamentals of comparative embryology of the vertebrates. Revised edition. New York, NY: Macmillan Co.

Kuratani S, Horigome N, Hirano S. 1999. Developmental morphology of the head mesoderm and reevaluation of segmental theories of the vertebrate head: evidence from embryos of an Agnathan vertebrate, Lampetra japonica. Dev. Biol. 210, 381-400. (10.1006/dbio.1999.9266) PubMed DOI

Adachi N, Kuratani S. 2012. Development of head and trunk mesoderm in the dogfish, Scyliorhinus torazame: I. Embryology and morphology of the head cavities and related structures. Evol. Dev. 14, 234-256. (10.1111/j.1525-142X.2012.00542.x) PubMed DOI

Seessel A. 1877. Zur Entwicklungsgeschichte des Vorderdarmes. Arch Für Anat Entwickelungsgeschichte 1, 449-467.

Zeleny C. 1901. The early development of the hypophysis in chelonia. Biol. Bull. 2, 267-281. (10.2307/1535704) DOI

Adelmann H. 1922. The significance of the prechordal plate: an interpretative study. Am. J. Anat. 31, 55-101. (10.1002/aja.1000310104) DOI

Seifert R, Jacob M, Jacob HJ. 1993. The avian prechordal head region: a morphological study. J. Anat. 183, 75-89. PubMed PMC

Ferran JL, Irimia M, Puelles L. 2022. Is there a prechordal region and an acroterminal domain in amphioxus? Brain Behav. Evol. 96, 334-352. (10.1159/000521966) PubMed DOI

Sambasivan R, Kuratani S, Tajbakhsh S. 2011. An eye on the head: the development and evolution of craniofacial muscles. Dev. Camb. Engl. 138, 2401-2415. PubMed

Kuratani S, Adachi N. 2016. What are head cavities? — a history of studies on vertebrate head segmentation. Zoolog. Sci. 33, 213-228. (10.2108/zs150181) PubMed DOI

Adelmann HB. 1932. The development of the prechordal plate and mesoderm of Amblystoma punctatum. J. Morphol. 54, 1-67. (10.1002/jmor.1050540102) DOI

Horackova A, Pospisilova A, Stundl J, Minarik M, Jandzik D, Cerny R. 2023. Pre-mandibular pharyngeal pouches in early non-teleost fish embryos. Figshare. (10.6084/m9.figshare.c.6806561) PubMed DOI PMC

Pre-mandibular pharyngeal pouches in early non-teleost fish embryos

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.c.6806561