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BMC Evol Biol
2018 Aug 30;181:127. doi: 10.1186/s12862-018-1241-y.
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Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families.
Enault S
,
Muñoz D
,
Simion P
,
Ventéo S
,
Sire JY
,
Marcellini S
,
Debiais-Thibaud M
.
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BACKGROUND: The molecular bases explaining the diversity of dental tissue mineralization across gnathostomes are still poorly understood. Odontodes, such as teeth and body denticles, are serial structures that develop through deployment of a gene regulatory network shared between all gnathostomes. Dentin, the inner odontode mineralized tissue, is produced by odontoblasts and appears well-conserved through evolution. In contrast, the odontode hypermineralized external layer (enamel or enameloid) produced by ameloblasts of epithelial origin, shows extensive structural variations. As EMP (Enamel Matrix Protein) genes are as yet only found in osteichthyans where they play a major role in the mineralization of teeth and others skeletal organs, our understanding of the molecular mechanisms leading to the mineralized odontode matrices in chondrichthyans remains virtually unknown.
RESULTS: We undertook a phylogenetic analysis of the SPARC/SPARC-L gene family, from which the EMPs are supposed to have arisen, and examined the expression patterns of its members and of major fibrillar collagens in the spotted catshark Scyliorhinus canicula, the thornback ray Raja clavata, and the clawed frog Xenopus tropicalis. Our phylogenetic analyses reveal that the single chondrichthyan SPARC-L gene is co-orthologous to the osteichthyan SPARC-L1 and SPARC-L2 paralogues. In all three species, odontoblasts co-express SPARC and collagens. In contrast, ameloblasts do not strongly express collagen genes but exhibit strikingly similar SPARC-L and EMP expression patterns at their maturation stage, in the examined chondrichthyan and osteichthyan species, respectively.
CONCLUSIONS: A well-conserved odontoblastic collagen/SPARC module across gnathostomes further confirms dentin homology. Members of the SPARC-L clade evolved faster than their SPARC paralogues, both in terms of protein sequence and gene duplication. We uncover an osteichthyan-specific duplication that produced SPARC-L1 (subsequently lost in pipidae frogs) and SPARC-L2 (independently lost in teleosts and tetrapods).Our results suggest the ameloblastic expression of the single chondrichthyan SPARC-L gene at the maturation stage reflects the ancestral gnathostome situation, and provide new evidence in favor of the homology of enamel and enameloids in all gnathostomes.
Fig. 1
Phylogenetic relationships of the vertebrate SPARC and SPARC-L gene families. Bayesian inference was run with Phylobayes and the site-heterogeneous CAT+Î4 model of sequence evolution. The tree was rooted with the lamprey SPARC-A and SPARC-B sequences. Posterior probabilities are indicated on the branches
Fig. 2
Histology and gene expression in the developing odontodes of Scyliorhinus canicula and Raja clavata. Lower jaw longitudinal sections (anterior, left; dorsal, up) of a 20 cm long S.c. juvenile (a), a 9 cm long S.c. embryo (b-f), and a 9 cm long R.c embryos (m-r), revealing the presence of tooth series at the maturation stage as well as less developed secretory stage tooth bud harboring columnar ameloblasts (black arrowhead). Thoracic transverse sections are shown for of 6 cm (g-l) and 7 cm (g’-l’) long S.c. embryos, focusing on developing primary dorsal dermal denticles at late morphogenesis and late maturation stage, respectively (dorsal to the top). Sections were stained with HES (a, g, g’, m) or in situ hybridized against SPARC (b, h, h’, n), SPARC-L (c, i, i’, o), Col1a1 (d, j, j’, p), Col1a2 (e, k, k’, q) and Col2a1-L (f, l, l’, r). The asterisks locate the mineralized matrix in teeth and denticles at the late mineralization stage, separating the ameloblasts (Am, located by the dashed lines) from the odontoblasts (Od, delineated by the orange line). MC: Meckel. The scale bar in (a) represents 100 μm in (a-f, m-r), and the scale bar in (g) represents 50 μm in (g-l’)
Fig. 3
Histology and gene expression in developing teeth of Xenopus tropicalis. Longitudinal sections of the X.t. upper jaw at the NF57 developmental stages were stained with HES (a, g) or processed by in situ hybridization for the indicated genes (b-f and h-l). Ameloblasts and odontoblasts are delineated by black dotted lines or by an orange line, respectively. The asterisks locate the mineralized matrix. The scale bars in (a) and (g) respectively represent 20 μm in (a-f) and (g-l)
Fig. 4
Favored model for the evolution of gene content and ameloblastic expression in gnathostomes. A cladogram shows the classically accepted phylogenetic relationships of Scyliorhinus canicula (S.c.), Raja clavata (R.c.), Lepisosteus oculatus (L.o.), Danio rerio (D.r.), Takifugu rubripes (T.r.), Latimeria chalumnae (L.c.), Xenopus tropicalis (X.t.) and Mus musculus (M.m.), as well as putative ancestral situations and polarized evolutionary changes. Pentagons summarize the gene content identified in each species and inferred to have existed in their last common ancestor. Ameloblastic gene expression status is summarized as transcribed (blue), undetected (white) or unknown (grey). Dotted arrows represent unresolved ambiguities with respect to the origin of the SCPP members. See text for details and references
enam (enamelin) in a section of NF stage 59 xenopus Tropicalis upper jaw
sparc (secreted protein, acidic, cysteine-rich (osteonectin)) in a section of NF stage 59 xenopus Tropicalis tooth
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