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Making teeth to order: conserved genes reveal an ancient molecular pattern in paddlefish (Actinopterygii).

Smith MM, Johanson Z, Butts T, Ericsson R, Modrell M, Tulenko FJ, Davis MC, Fraser GJ - Proc. Biol. Sci. (2015)

Bottom Line: Developmental timing for each tooth field in Polyodon follows a gradient, from rostral to caudal and ventral to dorsal, repeated during subsequent loss of teeth.The transitory Polyodon dentition is modified by cessation of tooth addition and loss.As such, Polyodon represents a basal actinopterygian model for the evolution of developmental novelty: initial conservation, followed by tooth loss, accommodating the adult trophic modification to filter-feeding.

View Article: PubMed Central - PubMed

Affiliation: Craniofacial Development and Stem Cell Biology, King's College London Dental Institute, London, UK Department of Earth Sciences, Natural History Museum, London, UK moya.smith@kcl.ac.uk.

ABSTRACT
Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (+30 000 species, predominantly teleosts), with great morphological diversity, including their dentitions. How dental morphological variation evolved is best addressed by considering a range of taxa across actinopterygian phylogeny; here we examine the dentition of Polyodon spathula (American paddlefish), assigned to the basal group Acipenseriformes. Although teeth are present and functional in young individuals of Polyodon, they are completely absent in adults. Our current understanding of developmental genes operating in the dentition is primarily restricted to teleosts; we show that shh and bmp4, as highly conserved epithelial and mesenchymal genes for gnathostome tooth development, are similarly expressed at Polyodon tooth loci, thus extending this conserved developmental pattern within the Actinopterygii. These genes map spatio-temporal tooth initiation in Polyodon larvae and provide new data in both oral and pharyngeal tooth sites. Variation in cellular intensity of shh maps timing of tooth morphogenesis, revealing a second odontogenic wave as alternate sites within tooth rows, a dental pattern also present in more derived actinopterygians. Developmental timing for each tooth field in Polyodon follows a gradient, from rostral to caudal and ventral to dorsal, repeated during subsequent loss of teeth. The transitory Polyodon dentition is modified by cessation of tooth addition and loss. As such, Polyodon represents a basal actinopterygian model for the evolution of developmental novelty: initial conservation, followed by tooth loss, accommodating the adult trophic modification to filter-feeding.

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Alizarin red, Alcian blue preparations of Polyodon spathula, 7dps showing relative tooth positions. (a, c, g-k) Upper jaw and dorsal pharyngeal skeleton, (b,d–f,l) lower jaw and ventral pharyngeal skeleton. (a,b) Chondrocranium and branchial arches. (c) Upper jaw, teeth along dermopalatine bone and separate palatopterygoid tooth plate (lacking membrane bone), with two paired tooth plates caudally (black arrows indicate j, k). (d) Lower jaw, ventral pharyngeal skeleton (hyoid, 1st, 2nd gill arches). (e) Teeth on dentary bone (arrows, new teeth). (f) Eight teeth linked by bone of attachment on 1st gill arch cartilage (hypobranchial 1, lacking membrane bone). (g–i) Right upper jaw, teeth ankylosed to dermopalatine bone, separate palatopterygoid tooth plate (arrows, new teeth caudally on dermopalatine (i), rostrally on palatopterygoid (h)). (h) Palatopterygoid tooth plate, bone of attachment only (arrows new teeth). (j,k) Upper jaw tooth plates of (j) epibranchial 2, four associated teeth, (k) hyoid arch, six teeth. (l) Hypohyal and first two ventral gill arches, with paired toothplates, more teeth on hb1 than hb2, more on ventral than dorsal pharyngeal toothplates. White arrows = newest unattached teeth. Scale bars (a,b), 1 mm; (c–g,l), 500 μm; (h,i), 100 μm; abbreviations as in figure 1.
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RSPB20142700F2: Alizarin red, Alcian blue preparations of Polyodon spathula, 7dps showing relative tooth positions. (a, c, g-k) Upper jaw and dorsal pharyngeal skeleton, (b,d–f,l) lower jaw and ventral pharyngeal skeleton. (a,b) Chondrocranium and branchial arches. (c) Upper jaw, teeth along dermopalatine bone and separate palatopterygoid tooth plate (lacking membrane bone), with two paired tooth plates caudally (black arrows indicate j, k). (d) Lower jaw, ventral pharyngeal skeleton (hyoid, 1st, 2nd gill arches). (e) Teeth on dentary bone (arrows, new teeth). (f) Eight teeth linked by bone of attachment on 1st gill arch cartilage (hypobranchial 1, lacking membrane bone). (g–i) Right upper jaw, teeth ankylosed to dermopalatine bone, separate palatopterygoid tooth plate (arrows, new teeth caudally on dermopalatine (i), rostrally on palatopterygoid (h)). (h) Palatopterygoid tooth plate, bone of attachment only (arrows new teeth). (j,k) Upper jaw tooth plates of (j) epibranchial 2, four associated teeth, (k) hyoid arch, six teeth. (l) Hypohyal and first two ventral gill arches, with paired toothplates, more teeth on hb1 than hb2, more on ventral than dorsal pharyngeal toothplates. White arrows = newest unattached teeth. Scale bars (a,b), 1 mm; (c–g,l), 500 μm; (h,i), 100 μm; abbreviations as in figure 1.

Mentions: In P. spathula larvae, shh and bmp4 expression reveal both the early events of oral and pharyngeal dental patterning and sequential addition of tooth loci as development proceeds. There are notable differences in the addition of new tooth germs in individual dentate fields, normally caudal, but exceptionally rostrally on the palatopterygoid tooth plate. Concerning timing along the body axis, tooth initiation begins in association with Meckel's cartilage, establishing a spatio-temporal gradient that extends from the oral, through to tooth sites in the pharyngeal cavities (figures 1 and 2; electronic supplementary material, figure S4). Skeletal preparations provide additional data on pattern order; after tooth rows form on the dentary and dermopalatine, they develop on the more caudal palatopterygoids and first hypobranchials (figures 1a,c and 2a,b, respectively). Teeth are later organized into toothed plates, connected by basal bone of attachment, representing functional surfaces of the oropharyngeal dentition (table 1, electronic supplementary material, figure S2c) [1–3].Table 1.


Making teeth to order: conserved genes reveal an ancient molecular pattern in paddlefish (Actinopterygii).

Smith MM, Johanson Z, Butts T, Ericsson R, Modrell M, Tulenko FJ, Davis MC, Fraser GJ - Proc. Biol. Sci. (2015)

Alizarin red, Alcian blue preparations of Polyodon spathula, 7dps showing relative tooth positions. (a, c, g-k) Upper jaw and dorsal pharyngeal skeleton, (b,d–f,l) lower jaw and ventral pharyngeal skeleton. (a,b) Chondrocranium and branchial arches. (c) Upper jaw, teeth along dermopalatine bone and separate palatopterygoid tooth plate (lacking membrane bone), with two paired tooth plates caudally (black arrows indicate j, k). (d) Lower jaw, ventral pharyngeal skeleton (hyoid, 1st, 2nd gill arches). (e) Teeth on dentary bone (arrows, new teeth). (f) Eight teeth linked by bone of attachment on 1st gill arch cartilage (hypobranchial 1, lacking membrane bone). (g–i) Right upper jaw, teeth ankylosed to dermopalatine bone, separate palatopterygoid tooth plate (arrows, new teeth caudally on dermopalatine (i), rostrally on palatopterygoid (h)). (h) Palatopterygoid tooth plate, bone of attachment only (arrows new teeth). (j,k) Upper jaw tooth plates of (j) epibranchial 2, four associated teeth, (k) hyoid arch, six teeth. (l) Hypohyal and first two ventral gill arches, with paired toothplates, more teeth on hb1 than hb2, more on ventral than dorsal pharyngeal toothplates. White arrows = newest unattached teeth. Scale bars (a,b), 1 mm; (c–g,l), 500 μm; (h,i), 100 μm; abbreviations as in figure 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4389609&req=5

RSPB20142700F2: Alizarin red, Alcian blue preparations of Polyodon spathula, 7dps showing relative tooth positions. (a, c, g-k) Upper jaw and dorsal pharyngeal skeleton, (b,d–f,l) lower jaw and ventral pharyngeal skeleton. (a,b) Chondrocranium and branchial arches. (c) Upper jaw, teeth along dermopalatine bone and separate palatopterygoid tooth plate (lacking membrane bone), with two paired tooth plates caudally (black arrows indicate j, k). (d) Lower jaw, ventral pharyngeal skeleton (hyoid, 1st, 2nd gill arches). (e) Teeth on dentary bone (arrows, new teeth). (f) Eight teeth linked by bone of attachment on 1st gill arch cartilage (hypobranchial 1, lacking membrane bone). (g–i) Right upper jaw, teeth ankylosed to dermopalatine bone, separate palatopterygoid tooth plate (arrows, new teeth caudally on dermopalatine (i), rostrally on palatopterygoid (h)). (h) Palatopterygoid tooth plate, bone of attachment only (arrows new teeth). (j,k) Upper jaw tooth plates of (j) epibranchial 2, four associated teeth, (k) hyoid arch, six teeth. (l) Hypohyal and first two ventral gill arches, with paired toothplates, more teeth on hb1 than hb2, more on ventral than dorsal pharyngeal toothplates. White arrows = newest unattached teeth. Scale bars (a,b), 1 mm; (c–g,l), 500 μm; (h,i), 100 μm; abbreviations as in figure 1.
Mentions: In P. spathula larvae, shh and bmp4 expression reveal both the early events of oral and pharyngeal dental patterning and sequential addition of tooth loci as development proceeds. There are notable differences in the addition of new tooth germs in individual dentate fields, normally caudal, but exceptionally rostrally on the palatopterygoid tooth plate. Concerning timing along the body axis, tooth initiation begins in association with Meckel's cartilage, establishing a spatio-temporal gradient that extends from the oral, through to tooth sites in the pharyngeal cavities (figures 1 and 2; electronic supplementary material, figure S4). Skeletal preparations provide additional data on pattern order; after tooth rows form on the dentary and dermopalatine, they develop on the more caudal palatopterygoids and first hypobranchials (figures 1a,c and 2a,b, respectively). Teeth are later organized into toothed plates, connected by basal bone of attachment, representing functional surfaces of the oropharyngeal dentition (table 1, electronic supplementary material, figure S2c) [1–3].Table 1.

Bottom Line: Developmental timing for each tooth field in Polyodon follows a gradient, from rostral to caudal and ventral to dorsal, repeated during subsequent loss of teeth.The transitory Polyodon dentition is modified by cessation of tooth addition and loss.As such, Polyodon represents a basal actinopterygian model for the evolution of developmental novelty: initial conservation, followed by tooth loss, accommodating the adult trophic modification to filter-feeding.

View Article: PubMed Central - PubMed

Affiliation: Craniofacial Development and Stem Cell Biology, King's College London Dental Institute, London, UK Department of Earth Sciences, Natural History Museum, London, UK moya.smith@kcl.ac.uk.

ABSTRACT
Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (+30 000 species, predominantly teleosts), with great morphological diversity, including their dentitions. How dental morphological variation evolved is best addressed by considering a range of taxa across actinopterygian phylogeny; here we examine the dentition of Polyodon spathula (American paddlefish), assigned to the basal group Acipenseriformes. Although teeth are present and functional in young individuals of Polyodon, they are completely absent in adults. Our current understanding of developmental genes operating in the dentition is primarily restricted to teleosts; we show that shh and bmp4, as highly conserved epithelial and mesenchymal genes for gnathostome tooth development, are similarly expressed at Polyodon tooth loci, thus extending this conserved developmental pattern within the Actinopterygii. These genes map spatio-temporal tooth initiation in Polyodon larvae and provide new data in both oral and pharyngeal tooth sites. Variation in cellular intensity of shh maps timing of tooth morphogenesis, revealing a second odontogenic wave as alternate sites within tooth rows, a dental pattern also present in more derived actinopterygians. Developmental timing for each tooth field in Polyodon follows a gradient, from rostral to caudal and ventral to dorsal, repeated during subsequent loss of teeth. The transitory Polyodon dentition is modified by cessation of tooth addition and loss. As such, Polyodon represents a basal actinopterygian model for the evolution of developmental novelty: initial conservation, followed by tooth loss, accommodating the adult trophic modification to filter-feeding.

Show MeSH
Related in: MedlinePlus