BACKGROUND: Previous studies have reported that periderm (the outer ectodermal layer) in zebrafish partially expands into the mouth and pharyngeal pouches, but does not reach the medial endoderm, where the pharyngeal teeth develop. Instead, periderm-like cells, arising independently from the outer periderm, cover prospective tooth-forming epithelia and are crucial for tooth germ initiation. Here we test the hypothesis that restricted expansion of periderm is a teleost-specific character possibly related to the derived way of early embryonic development. To this end, we performed lineage tracing of the periderm in a non-teleost actinopterygian species possessing pharyngeal teeth, the sterlet sturgeon (Acipenser ruthenus), and a sarcopterygian species lacking pharyngeal teeth, the axolotl (Ambystoma mexicanum). RESULTS: In sturgeon, a stratified ectoderm is firmly established at the end of gastrulation, with minimally a basal ectodermal layer and a surface layer that can be homologized to a periderm. Periderm expands to a limited extent into the mouth and remains restricted to the distal parts of the pouches. It does not reach the medial pharyngeal endoderm, where pharyngeal teeth are located. Thus, periderm in sturgeon covers prospective odontogenic epithelium in the jaw region (oral teeth) but not in the pharyngeal region. In axolotl, like in sturgeon, periderm expansion in the oropharynx is restricted to the distal parts of the opening pouches. Oral teeth in axolotl develop long before mouth opening and possible expansion of the periderm into the mouth cavity. CONCLUSIONS: Restricted periderm expansion into the oropharynx appears to be an ancestral feature for osteichthyans, as it is found in sturgeon, zebrafish and axolotl. Periderm behavior does not correlate with presence or absence of oral or pharyngeal teeth, whose induction may depend on 'ectodermalized' endoderm. It is proposed that periderm assists in lumenization of the pouches to create an open gill slit. Comparison of basal and advanced actinopterygians with sarcopterygians (axolotl) shows that different trajectories of embryonic development converge on similar dynamics of the periderm: a restricted expansion into the mouth and prospective gill slits.

Department of Zoology Faculty of Science Charles University Vinicna 7 128 44 Prague Czech Republic

Research Group Evolutionary Developmental Biology Biology Department Ghent University K L Ledeganckstraat 35 9000 Ghent Belgium

Zobrazit více v PubMed

Hashimshony T, Feder M, Levin M, Hall BK, Yanai I. Spatiotemporal transcriptomics reveals the evolutionary history of the endoderm germ layer. Nature. 2015;519:219–22. PubMed DOI PMC

Steinmetz PRH, Aman A, Kraus JEM, Technau U. Gut-like ectodermal tissue in a sea anemone challenges germ layer homology. Nat Ecol Evol. 2017;1:1535–42. PubMed DOI PMC

Hirasawi T, Kuratani S. Evolution of the vertebrate skeleton: morphology, embryology, and development. Zool Lett. 2015;1:2. PubMed DOI PMC

Hall BK. Germ layers, the neural crest and emergent organization in development and evolution. Genesis. 2018;56: e23103. PubMed DOI

Teng CS, Cavin L, Maxson Jnr RE, Sanchez-Villagra M, Crump JG. Resolving homology in the face of shifting germ layer origins: lessons from a major skull vault boundary. Elife. 2019;8: e52814. PubMed DOI PMC

Krivanek J, Soldatov RA, Kastriti ME, Chontorotzea T, Herdina AN, Petersen J, et al. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat Commun. 2020;11:4816. PubMed DOI PMC

Huysseune A, Cerny R, Witten PE. The conundrum of pharyngeal teeth origin: the role of germ layers, pouches, and gill slits. Biol Rev. 2022;97:414–47. PubMed DOI PMC

Chen D, editor. Odontodes: the developmental and evolutionary building blocks of dentitions. 1st ed. Boca Raton: CRC Press; 2023.

Gillis JA, Tidswell ORA. The origin of vertebrate gills. Curr Biol. 2017;27:729–32. PubMed DOI PMC

Sagai T, Amano T, Maeno A, Kimura T, Nakamoto M, Takehana Y, et al. Evolution of Shh endoderm enhancers during morphological transition from ventral lungs to dorsal gas bladder. Nat Commun. 2017;8:14300. PubMed DOI PMC

Barlow LA. Progress and renewal in gustation: new insights into taste bud development. Development. 2015;142:3620–9. PubMed DOI PMC

Fabian P, Tseng K-C, Smeeton J, Lancman JJ, Dong PDS, Cerny R, et al. Lineage analysis reveals an endodermal contribution to the vertebrate pituitary. Science. 2020;370:463–7. PubMed DOI PMC

Boehm T, Bleul CC. The evolutionary history of lymphoid organs. Nat Immunol. 2007;8:131–5. PubMed DOI

Soukup V, Epperlein HH, Horácek I, Cerny R. Dual epithelial origin of vertebrate oral teeth. Nature. 2008;455:795–8. PubMed DOI

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

Rothova M, Thompson H, Lickert H, Tucker AS. Lineage tracing of the endoderm during oral development. Dev Dyn. 2012;241:1183–91. PubMed DOI

Rosa JT, Oralová V, Larionova D, Eisenhoffer GT, Witten PE, Huysseune A. Periderm invasion contributes to epithelial formation in the teleost pharynx. Sci Rep. 2019;9:10082. PubMed DOI PMC

Grevellec A, Tucker AS. The pharyngeal pouches and clefts: development, evolution, structure and derivatives. Semin Cell Dev Biol. 2010;21:325–32. PubMed DOI

Soukup V, Horácek I, Cerny R. Development and evolution of the vertebrate primary mouth. J Anat. 2013;222:79–99. PubMed DOI PMC

Frisdal A, Trainor PA. Development and evolution of the pharyngeal apparatus. WIREs Dev Biol. 2014;3:403–18. PubMed DOI PMC

Shone V, Graham A. Endodermal/ectodermal interfaces during pharyngeal segmentation in vertebrates. J Anat. 2014;225:479–91. PubMed DOI PMC

Huysseune A, Cerny R, Witten PE. The conquest of the oropharynx by odontogenic epithelia. In: Chen D, editor. Odontodes: the developmental and evolutionary building blocks of dentitions. Boca Raton: CRC Press; 2023. p. 49–67.

Kimmel CB, Warga RM, Schilling TF. Origin and organization of the zebrafish fate map. Development. 1990;108:581–94. PubMed DOI

Oralová V, Rosa JT, Larionova D, Witten PE, Huysseune A. Multiple epithelia are required to form teeth deep in the pharynx. Proc Natl Acad Sci USA. 2020;117:11503–12. PubMed DOI PMC

Huysseune A, Sire J-Y, Witten PE. Evolutionary and developmental origins of the vertebrate dentition. J Anat. 2009;214:465–76. PubMed DOI PMC

Huysseune A, Sire J-Y, Witten PE. A revised hypothesis on the evolutionary origin of the vertebrate dentition. J Appl Ichthyol. 2010;26:152–5. DOI

Rücklin M, Giles S, Janvier P, Donoghue PCJ. Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate PubMed DOI

Rücklin M, Donoghue PCJ, Johanson Z, Trinajstic K, Marone F, Stampanoni M. Development of teeth and jaws in the earliest jawed vertebrates. Nature. 2012;491:748–51. PubMed DOI

Murdock DJE, Dong X-P, Repetski JE, Marone F, Stampanoni M, Donoghue PCJ. The origin of conodonts and of vertebrate mineralized skeletons. Nature. 2013;502:546–9. PubMed DOI

Donoghue PCJ, Rücklin M. The ins and outs of the evolutionary origin of teeth. Evol Dev. 2016;18:19–30. PubMed DOI

Collazo A, Bolker JA, Keller R. A phylogenetic perspective on teleost gastrulation. Am Nat. 1994;144:133–52. DOI

Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253–310. PubMed DOI

Cooper MS, Virta VC. Evolution of gastrulation in the ray-finned (actinopterygian) fishes. J Exp Zool (Mol Dev Evol). 2007;308B:591–608. PubMed DOI

Ballard WW, Ginsburg AS. Morphogenetic movements in acipenserid embryos. J Exp Zool. 1980;213:69–103. DOI

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

Diedhiou S, Bartsch P. Staging of the early development of

Ostaszewska T, Dabrowski K. Early development of

Wegner A, Ostaszewska T, Rozek W. The ontogenetic development of the digestive tract and accessory glands of sterlet ( DOI

Minarik M, Stundl J, Fabian P, Jandzik D, Metscher BD, Psenicka M, et al. Pre-oral gut contributes to facial structures in non-teleost fishes. Nature. 2017;547:209–12. PubMed DOI

Pospisilova A, Stundl J, Brejcha J, Metscher BD, Psenicka M, Cerny R, et al. The remarkable dynamics in the establishment, rearrangement, and loss of dentition during the ontogeny of the sterlet sturgeon. Dev Dyn. 2022;251:826–45. PubMed DOI

Cerny R, Meulemans D, Berger J, Wilsch-Bräuninger M, Kurth T, Bronner-Fraser M, et al. Combined intrinsic and extrinsic influences pattern cranial neural crest migration and pharyngeal arch morphogenesis in axolotl. Dev Biol. 2004;266:252–69. PubMed DOI

Adams AE. An experimental study of the development of the mouth in the amphibian embryo. J Exp Zool. 1924;40:311–79. DOI

Berkovitz B, Shellis P. The teeth of non-mammalian vertebrates. Amsterdam: Academic Press, Elsevier; 2017.

Saadatfar Z, Shahsavani D, Fatemi FS. Study of epidermis development in sturgeon ( PubMed DOI

Shooraki HF, Saadatfar Z, Shahsavani D. Skin development in DOI

Zeiske E, Kasumyan A, Bartsch P, Hansen A. Early development of the olfactory organ in sturgeons of the genus PubMed DOI

Shute L, Huebner E, Anderson WG. Microscopic identification of novel cell types in the integument of larval Lake Sturgeon, PubMed DOI

Slack JMW. Regional biosynthetic markers in the early amphibian embryo. J Embryol Exp Morphol. 1984;80:289–319. PubMed

Stigson M, Kjellén L. Large disulfide-stabilized proteoglycan complexes synthesized by the epidermis of axolotl embryos. Archs Biochem Biophys. 1991;290:391–6. PubMed DOI

Jarial MS. Fine structure of the epidermal Leydig cells in the axolotl PubMed PMC

Gerling S, D’haese J, Greven H. Number and distribution of Leydig cells (LC) in the epidermis of the growing axolotl, DOI

Bordzilovskaya NP, Dettlaff TA, Duhon S, Malacinski G. Developmental stage series of axolotl embryos. In: Armstrong JB, Malacinski GM, editors. Developmental biology of the axolotl. New York: Oxford University Press; 1989.

Seifert AW, Cook AB, Shaw D. Inhibiting fibroblast aggregation in skin wounds unlocks developmental pathway to regeneration. Dev Biol. 2019;455:60–72. PubMed DOI

Northcutt RG, Catania KC, Criley BB. Development of lateral line organs in the axolotl. J Comp Neurol. 1994;340:480–514. PubMed DOI

Shi D-L, Riou J-F, Darribère T, Boucaut J-C. A study of cell interactions involved in PubMed DOI

Richardson MK, Carl TF, Hanken J, Elinson RP, Cope C, Bagley P. Limb development and evolution: a frog embryo with no apical ectodermal ridge (AER). J Anat. 1998;192:379–90. PubMed DOI PMC

Furlow JD, Berry DL, Wang Z, Brown DD. A set of novel tadpole specific genes expressed only in the epidermis are down-regulated by thyroid hormone during PubMed DOI

Page RB, Monaghan JR, Walker JA, Voss SR. A model of transcriptional and morphological changes during thyroid hormone-induced metamorphosis of the axolotl. Gen Comp Endocrinol. 2009;162:219–32. PubMed DOI PMC

Stubbs JL, Davidson L, Keller R, Kintner C. Radial intercalation of ciliated cells during PubMed DOI

Walentek P, Quigley IK. What we can learn from a tadpole about ciliopathies and airway diseases: using systems biology in PubMed DOI PMC

Tomankova S, Abaffy P, Sindelka R. The role of nitric oxide during embryonic epidermis development of PubMed PMC

Kurth T, Weiche S, Vorkel D, Kretschmar S, Menge A. Histology of plastic embedded amphibian embryos and larvae. Genesis. 2012;50:235–50. PubMed DOI

Fukazawa C, Santiago C, Park KM, Deery WJ, de la Torre Canny SG, Holterhoff CK, et al. PubMed DOI PMC

Fischer B, Metzger M, Richardson R, Knyphausen P, Ramezani T, Franzen R, et al. p53 and TAp63 promote keratinocyte proliferation and differentiation in breeding tubercles of the zebrafish. PLoS Genet. 2014;10: e1004048. PubMed DOI PMC

Lee RTH, Asharani PV, Carney TJ. Basal keratinocytes contribute to all strata of the adult zebrafish dermis. PLoS ONE. 2014;9(1): e84858. PubMed DOI PMC

Warga RM, Kane DA. Wilson cell origin for Kupffer’s vesicle in the zebrafish. Dev Dyn. 2018;247:1057–69. PubMed DOI

Dettlaff TA. Evolution of the histological and functional structure of ectoderm, chordamesoderm and their derivatives in Anamnia. Roux’s Arch Dev Biol. 1993;203:3–9. PubMed DOI

Chan KY, Yan C-CS, Roan H-Y, Hsu S-C, Tseng T-L, Hsiao C-D, et al. Skin cells undergo asynthetic fission to expand body surfaces in zebrafish. Nature. 2022;605:119–25. PubMed DOI

Walck-Shannon E, Hardin J. Cell intercalation from top to bottom. Nat Rev Mol Cell Biol. 2014;15:34–48. PubMed DOI PMC

Rauzi M. Cell intercalation in a simple epithelium. Philos Trans R Soc B. 2020;375:20190552. PubMed DOI PMC

Richardson R, Metzger M, Knyphausen P, Ramezani T, Slanchev K, Kraus C, et al. Re-epithelialization of cutaneous wounds in adult zebrafish combines mechanisms of wound closure in embryonic and adult mammals. Development. 2016;143:2077–88. PubMed PMC

M’Boneko V, Merker H-J. Development and morphology of the periderm of mouse embryos. Acta Anat. 1988;133:325–36. PubMed DOI

Lan Y, Xu J, Jiang R. Cellular and molecular mechanisms of palatogenesis. Curr Top Dev Biol. 2015;115:59–84. PubMed DOI PMC

Hammond NL, Dixon J, Dixon MJ. Periderm: life-cycle and function during orofacial and epidermal development. Semin Cell Dev Biol. 2019;91:75–83. PubMed DOI

Kashgari G, Meinecke L, Gordon W, Ruiz B, Yang J, Ma AL, et al. Epithelial migration and non-adhesive periderm are required for digit separation during mammalian development. Dev Cell. 2020;52(6):764–78. PubMed DOI PMC

Rees JM, Palmer MA, Gillis JA. Fgf signalling is required for gill slit formation in the skate, PubMed DOI PMC

Jafari NV, Rohn JL. The urothelium: a multi-faceted barrier against a harsh environment. Muc Immunol. 2022;15:1127–42. PubMed DOI PMC

Hayashi H. Opening mechanism of stomodeum cavity and transformation of yolk platelet proteins to various subcellular structures in developing newt embryos,

Brand M, Granato M, Nüsslein-Volhard C. Keeping and raising zebrafish. In: Nüsslein-Volhard C, Dahm R, editors. Zebrafish: a practical approach. Oxford: Oxford University Press; 2002.

Huysseune A, Soenens M, Sire J-Y, Witten PE. High resolution histology for craniofacial studies on zebrafish and other teleost models. Meth Mol Biol. 2022;2403:249–62. PubMed DOI

Oralová V, Rosa JT, Soenens M, Bek JW, Willaert A, Witten PE, et al. Beyond the whole-mount phenotype: high-resolution imaging in fluorescence-based applications on zebrafish. Biol Open. 2019;8(5):UNSP bio042374. PubMed DOI PMC

Kopinke D, Sasine J, Swift J, Stephens WZ, Piotrowski T. Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification. Dev Dyn. 2006;235:2695–709. PubMed DOI