Vertebrate dentitions arise at various places within the oropharyngeal cavity including the jaws, the palate, or the pharynx. These dentitions develop in a highly organized way, where new tooth germs are progressively added adjacent to the initiator center, the first tooth. At the same time, the places where dentitions develop house the contact zones between the outer ectoderm and the inner endoderm, and this colocalization has instigated various suggestions on the roles of germ layers for tooth initiation and development. Here, we study development of the axolotl dentition, which is a complex of five pairs of tooth fields arranged into the typically tetrapod outer and inner dental arcades. By tracking the expression patterns of odontogenic genes, we reason that teeth of both dental arcades originate from common tooth-competent zones, one present on the mouth roof and one on the mouth floor. Progressive compartmentalization of these zones and a simultaneous addition of new tooth germs distinct for each prospective tooth field subsequently control the final shape and composition of the axolotl dentition. Interestingly, by following the fate of the GFP-labeled oral ectoderm, we further show that, in three out of five tooth field pairs, the first tooth develops right at the ecto-endodermal boundary. Our results thus indicate that a single tooth-competent zone gives rise to both dental arcades of a complex tetrapod dentition. Further, we propose that the ecto-endodermal boundary running through this zone should be accounted for as a potential source of instruction factors instigating the onset of the odontogenic program.

Center for Regenerative Therapies Technische Universität Dresden Dresden Germany

Department of Anatomy Technische Universität Dresden Dresden Germany

Department of Zoology Faculty of Science Charles University Prague Czechia

Max Planck Institute of Molecular Cell Biology and Genetics Dresden Germany

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Balic A. M. (2019). Concise review: cellular and molecular mechanisms of regulation of tooth initiation. PubMed DOI

Barlow L. A. (2000). “Taste buds in ectoderm are induced by endoderm: implications for mechanisms governing taste bud development,” in

Barlow L. A., Northcutt R. G. (1995). Embryonic origin of amphibian taste buds. PubMed DOI

Barlow L. A., Northcutt R. G. (1997). Taste buds develop autonomously from endoderm without induction by cephalic neural crest or paraxial mesoderm. PubMed

Bordzilovskaya N. P., Dettlaff T. A., Duhon S. T., Malacinski G. M. (1989). “Developmental-stage series of axolotl embryos,” in

Cardona A., Saalfeld S., Schindelin J., Arganda-Carreras I., Preibisch S., Longair M., et al. (2012). TrakEM software for neural circuit reconstruction. PubMed DOI PMC

Chen D., Blom H., Sanchez S., Tafforeau P., Märss T., Ahlberg P. E. (2020). The developmental relationship between teeth and dermal odontodes in the most primitive bony fish Lophosteus. PubMed DOI PMC

Clemen G. (1978). Aufbau und Veränderungen der Gaumenzahnleisten beim larvalen und metamorphosierenden DOI

Clemen G., Greven H. (1977). Morphologische Untersuchungen an der Mundhöhle von Urodelen III.

Clemen G., Greven H. (1994). The buccal cavity of larval and metamorphosed

Cobourne M. T., Miletich I., Sharpe P. T. (2004). Restriction of sonic hedgehog signalling during early tooth development. PubMed DOI

Cooper R. L., Thiery A. P., Fletscher A. G., Delbarre D. J., Rasch L. J., Fraser G. J. (2018). An ancient Turing-like patterning mechanism regulates skin denticle development in sharks. PubMed DOI PMC

Dassule H. R., Lewis P., Bei M., Maas R., McMahon A. P. (2000). Sonic hedgehog regulates growth and morphogenesis of the tooth. PubMed

Deban S. M., Wake D. B. (2000).

Debiais-Thibaud M., Chiori R., Enault S., Oulion S., Germont I., Martinand-Mari C., et al. (2015). Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system. PubMed DOI PMC

Dequéant M. L., Pourquié O. (2008). Segmental patterning of the vertebrate embryonic axis. PubMed DOI

Eberhart J. K., Swartz M. E., Crump J. G., Kimmel C. B. (2006). Early Hedgehog signaling from neural to oral epithelium organizes anterior craniofacial development. PubMed DOI

Ellis N. A., Donde N. N., Miller C. T. (2016). Early development and replacement of the stickleback dentition. PubMed DOI PMC

Fraser G. J., Bloomquist R. F., Streelman J. T. (2008). A periodic pattern generator for dental diversity. PubMed DOI PMC

Fraser G. J., Cerny R., Soukup V., Bronner-Fraser M., Streelman J. T. (2010). The odontode explosion: the origin of tooth-like structures in vertebrates. PubMed DOI PMC

Fraser G. J., Graham A., Smith M. M. (2004). Conserved deployment of genes during odontogenesis across osteichthyans. PubMed DOI PMC

Gibert Y., Samarut E., Ellis M. K., Jackman W. R., Laudet V. (2019). The first formed tooth serves as a signalling centre to induce the formation of the dental row in zebrafish. PubMed DOI PMC

Graham A. (2008). Deconstructing the pharyngeal metamere. PubMed DOI

Graveson A. C., Smith M. M., Hall B. K. (1997). Neural crest potential for tooth development in a urodele amphibian: developmental and evolutionary significance. PubMed DOI

Helms J. A., Kim C. H., Hu D., Minkoff R., Thaller C., Eichele G. (1997). PubMed DOI

Huysseune A., Sire J. Y., Witten P. E. (2009). Evolutionary and developmental origins of the vertebrate dentition. PubMed DOI PMC

Huysseune A., Sire J. Y., Witten P. E. (2010). A revised hypothesis on the evolutionary origin of the vertebrate dentition. DOI

Huysseune A., Witten P. E. (2006). Developmental mechanisms underlying tooth patterning in continuously replacing osteichthyan dentitions. PubMed DOI

Jackman W. R., Yoo J. J., Stock D. W. (2010). Hedgehog signaling is required at multiple stages of zebrafish tooth development. PubMed DOI PMC

Jernvall J., Thesleff I. (2000). Reiterative signaling and patterning during mammalian tooth morphogenesis. PubMed DOI

Jung H. S., Francis-West P. H., Widelitz R. B., Jiang T. X., Ting-Berreth S., Tickle C., et al. (1998). Local inhibitory action of BMPs and their relationships with activators in feather formation: implication for periodic patterning. PubMed DOI

Keränen S. V. E., Kettunen P., Aberg T., Thesleff I., Jernvall J. (1999). Gene expression patterns associated with suppression of odontogenesis in mouse and vole diastema regions. PubMed DOI

Lin C. R., Kioussi C., O’Connel S., Briata P., Szeto D., Liu F., et al. (1999). Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. PubMed DOI

Martin K. J., Rasch L. J., Cooper R. L., Metscher B. D., Johanson Z., Fraser G. J. (2016). Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles. PubMed DOI PMC

Matsumoto R., Evans S. E. (2017). The palatal dentition of tetrapods and its functional significance. PubMed DOI PMC

Northcutt R. G., Barlow L. A., Braun C. B., Catania K. C. (2000). Distribution and innervation of taste buds in the axolotl. PubMed DOI

Ohazama A., Haworth K. E., Ota M. S., Khonsari R. H., Sharpe P. T. (2010). Ectoderm, endoderm, and the evolution of heterodont dentitions. PubMed DOI

Oralová V., Rosa J. T., Soenes M., Bek J. W., Willaert A., Witten P. E., et al. (2020). Multiple epithelia are required to develop teeth deep inside the pharynx. PubMed DOI PMC

Osborn J. W. (1978). “Morphogenetic gradients: field versus clones,” in

Pospisilova A., Brejcha J., Miller V., Holcman R., Šanda R., Stundl J. (2019). Embryonic and larval development of the northern pike: an emerging fish model system for evo-devo research. PubMed

Prochazka J., Pantalacci S., Churava S., Rothova M., Lambert A., Lesot H., et al. (2010). Patterning by heritage in mouse molar row development. PubMed DOI PMC

Rasch L. J., Cooper R. L., Underwood C., Dillard W. A., Thiery A. P., Fraser G. J. (2020). Development and regeneration of the crushing dentition in skates (Rajidae). PubMed DOI

Rasch L. J., Martin K., Cooper R. L., Metscher B. D., Underwood C. J., Fraser G. J. (2016). An ancient dental gene set governs development and continuous regeneration of teeth in sharks. PubMed DOI

Rothova M., Thompson H., Lickert H., Tusker A. S. (2012). Lineage tracing of the endoderm during oral development. PubMed DOI

Sadier A., Jaclman W. R., Laudet V., Gibert Y. (2020). The vertebrate tooth row: is it initiated by a single organizing tooth? PubMed DOI

Sadier A., Twarogowska M., Steklikova K., Hayden L., Lambert A., Schneder P., et al. (2019). Modeling Edar expression reveals the hidden dynamics of tooth signaling center patterning. PubMed DOI PMC

Salomies L., Eymann J., Khan I., Di-Poï N. (2019). The alternative regenerative strategy of bearded dragon unveils the key processes underlying vertebrate tooth renewal. PubMed PMC

Sarkar L., Cobourne M., Naylor S., Smalley M., Dale T., Sharpe P. T. (2000). Wnt/Shh interactions regulate ectodermal boundary formation during mammalian tooth development. PubMed DOI PMC

Schilling T. F. (2008). Anterior-posterior patterning and segmentation of the vertebrate head. PubMed DOI PMC

Schindelin J., Arganda-Carreras I., Frise E., Kyanig V., Longair M., Pietzsch T., et al. (2012). Fiji: an open-source platform for biological-image analysis. PubMed DOI PMC

Schindelin J., Rueden C. T., Hiner M. C., Eliceiri K. W. (2015). The ImageJ ecosystem: an open platform for biomedical image analysis. PubMed DOI PMC

Schneider C. A., Rasband W. S., Eliceiri K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. PubMed DOI PMC

Schweickert A., Steinbeisser H., Blum M. (2001). Differential gene expression of PubMed DOI

Sharpe P. T. (1995). Homeobox genes and orofacial development. PubMed DOI

Smith M. M. (2003). Vertebrate dentitions at the origin of jaws: when and how pattern evolved. PubMed DOI

Sobkow L., Epperlein H. H., Herklotz S., Straube W. L., Tanaka E. M. (2006). A germline GFP transgenic axolotl and its use to track cell fate: dual origin of the fin mesenchyme during development and the fate of blood cells during regeneration. PubMed DOI

Soukup V., Epperlein H. H., Horácek I., Cerny R. (2008). Dual epithelial origin of vertebrate oral teeth. PubMed DOI

Soukup V., Horácek I., Cerny R. (2013). Development and evolution of the vertebrate primary mouth. PubMed DOI PMC

Stock D. W., Jackman W. R., Trapani J. (2006). Developmental genetic mechanisms of evolutionary tooth loss in cypriniform fishes. PubMed DOI

Streelman J. T., Webb J. F., Albertson R. C., Kocher T. D. (2003). The cusp of evolution and development: a model of cichlid tooth shape diversity. PubMed DOI

Stundl J., Pospisilova A., Jandzik D., Fabian P., Dobiasova B., Minarik M., et al. (2019). Bichir external gills arise via heterochronic shift that accelerates hyoid arch development. PubMed PMC

Stundl J., Pospisilova A., Matějková T., Psenicka M., Bronner M. E., Cerny R. (2020). Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes. PubMed DOI PMC

Takata C. (1960). The differentiation DOI

Thiery A. P., Shono T., Kurokawa D., Britz R., Johanson Z., Fraser G. J. (2017). Spatially restricted dental regeneration drives pufferfish beak development. PubMed PMC

Tucker A., Sharpe P. (2004). The cutting-edge of mammalian development; how the embryo makes teeth. PubMed

Van der heyden C., Huysseune A. (2000). Dynamics of tooth formation and replacement in the zebrafish ( PubMed DOI

Wilde C. E. (1955). The urodele neuroepithelium I, The differentiation in vitro of the cranial neural crest. DOI

Yu W., Sun Z., Sweat Y., Sweat M., Venugopalan S. R., Eliason S., et al. (2020). Pitx2-Sox2-Lef-1 interactions specify progenitor oral/dental epithelial cell signaling centers. PubMed DOI PMC

Zhang Z., Lan Y., Chai Y., Jiang R. (2009). Antagonistic actions of Msx1 and Osr2 pattern mammalian teeth into a single row. PubMed DOI PMC

Periderm fate and independence of tooth formation are conserved across osteichthyans

RNA localization during early development of the axolotl

The conundrum of pharyngeal teeth origin: the role of germ layers, pouches, and gill slits