New genomic and fossil data illuminate the origin of enamel

Abstract

Enamel, the hardest vertebrate tissue, covers the teeth of almost all sarcopterygians (lobe-finned bony fishes and tetrapods) as well as the scales and dermal bones of many fossil lobe-fins1,2,3,4,5. Enamel deposition requires an organic matrix containing the unique enamel matrix proteins (EMPs) amelogenin (AMEL), enamelin (ENAM) and ameloblastin (AMBN)6. Chondrichthyans (cartilaginous fishes) lack both enamel and EMP genes7,8. Many fossil and a few living non-teleost actinopterygians (ray-finned bony fishes) such as the gar, Lepisosteus, have scales and dermal bones covered with a proposed enamel homologue called ganoine1,9. However, no gene or transcript data for EMPs have been described from actinopterygians10,11. Here we show that Psarolepis romeri, a bony fish from the the Early Devonian period, combines enamel-covered dermal odontodes on scales and skull bones with teeth of naked dentine, and that Lepisosteus oculatus (the spotted gar) has enam and ambn genes that are expressed in the skin, probably associated with ganoine formation. The genetic evidence strengthens the hypothesis that ganoine is homologous with enamel. The fossil evidence, further supported by the Silurian bony fish Andreolepis, which has enamel-covered scales but teeth and odontodes on its dermal bones made of naked dentine12,13,14,15,16, indicates that this tissue originated on the dermal skeleton, probably on the scales. It subsequently underwent heterotopic expansion across two highly conserved patterning boundaries (scales/head–shoulder and dermal/oral) within the odontode skeleton.

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Figure 1: Phylogeny of odontode surface tissues.
Figure 2: P/Q-rich SCPP gene cluster.
Figure 3: Sagittal section (IVPP V17756.3) of the cranial roof and transverse section (IVPP V19360.1) of the lower jaw of P. romeri.
Figure 4: Scenarios about the early evolution of enamel.

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Acknowledgements

This project was inspired in part by initial discussions with K. Kawasaki, whom we gratefully acknowledge. We thank the Broad Institute Genomics Platform and Vertebrate Genome Biology group, Spotted Gar Genome Consortium and K. Lindblad-Toh for making the data for L. oculatus available. We thank W. Zhang and S. Zhang for technical help with thin sections and SEM. The work was supported by the Knut and Alice Wallenberg Foundation through a Wallenberg Scholarship awarded to P.E.A., and by Vetenskapsrådet (Swedish Research Council) through a Young Researcher Grant awarded to T.H. M.Z. was funded by the National Basic Research Programme of China (2012CB821902).

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Authors

Contributions

Q.Q. and T.H. initiated the project. Q.Q. collected and analysed the palaeontological data, and produced Fig. 3 and Extended Data Figs 2, 3, 4, 5. T.H. collected and analysed the genomic data, and produced Figs 2, 4a, Extended Data Fig. 1, Extended Data Table 1 and Supplementary Information. M.Z. provided material of Psarolepis. P.E.A. led the writing process, and produced Figs 1 and 4b. All authors participated in the writing process.

Corresponding author

Correspondence to Per Erik Ahlberg.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Exon organization of P/Q-rich SCPP genes in human, anole lizard, coelacanth, spotted gar and zebrafish.

Each box represents a single exon. 5′ and 3′ untranslated regions are marked in white and protein-coding regions are marked in black. Location of the signal peptide (SP) is marked in yellow (EMPs), orange (maturation-stage proteins) and grey (zebrafish SCPP6). P/Q-labelled exons contain at least 25% of Pro and Gln residues. Exons with aromatic residues Phe, Tyr and Trp are marked with Y/F. Conserved amino acid motifs are indicated on the top or inside the exon boxes. Nearly identical exons are marked by asterisk or circle.

Extended Data Figure 2 The skull roof (IVPP V17756) of P. romeri used for making thin sections in this study.

Dorsal view (left) showing the relative positions of the thin sections and anterior view (right) showing the position of premaxilla. ‘a–h’ represent positions of the eight sections in Extended Data Fig. 3. Scale bar, 5 mm.

Extended Data Figure 3 The outlines of all the thin sections made from IVPP V17756.

Scale bar, 300 µm.

Extended Data Figure 4 Other teeth on the left premaxilla showing the absence of enamel.

a, From Extended Data Fig. 2a (IVPP V17756.1). b, Detail of a under transmission light (top) and polarized light (bottom). c, From Extended Data Fig. 2b (IVPP V17756.4), under transmission light (top) and polarized light (bottom). d, From Extended Data Fig. 2d (IVPP V17756.4). e, Detail of d under transmission light (top) and polarized light (bottom). Scale bar, 100 µm.

Extended Data Figure 5 The lower jaw (IVPP V19360) of P. romeri used for thin sections.

Scale bar, 5 mm.

Extended Data Table 1 P/Q-rich SCPP genes and SPARCL genes identified in the spotted gar and coelacanth genomes

Supplementary information

Supplementary Information

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Qu, Q., Haitina, T., Zhu, M. et al. New genomic and fossil data illuminate the origin of enamel. Nature 526, 108–111 (2015). https://doi.org/10.1038/nature15259

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