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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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Related in: MedlinePlus

Diagram summarizing stages of tooth germ morphogenesis relative to shh expression (from figure 3p1–4). Intensity of cellular expression is partitioned characteristically within the dental epithelium, with negative differentiated, interactive cells of dental epithelium shown (proactive d.e.), and also in sensory papilla of taste buds on right of tooth germ. (a) Cellular partitioning of shh expression as ‘placode’ (localized within epithelium, can be evaginated). (b) ‘Cap’, expression in the cap-shaped epithelium of tooth germ, surrounding dental papilla. (c) ‘Cone + collar’, cones of dentine with expression associated with the tooth base, or collar epithelium below the cap. (d) ‘Cone + bud’, expression in a new site within the outer dental epithelia (incipient bud for new tooth germ).
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RSPB20142700F4: Diagram summarizing stages of tooth germ morphogenesis relative to shh expression (from figure 3p1–4). Intensity of cellular expression is partitioned characteristically within the dental epithelium, with negative differentiated, interactive cells of dental epithelium shown (proactive d.e.), and also in sensory papilla of taste buds on right of tooth germ. (a) Cellular partitioning of shh expression as ‘placode’ (localized within epithelium, can be evaginated). (b) ‘Cap’, expression in the cap-shaped epithelium of tooth germ, surrounding dental papilla. (c) ‘Cone + collar’, cones of dentine with expression associated with the tooth base, or collar epithelium below the cap. (d) ‘Cone + bud’, expression in a new site within the outer dental epithelia (incipient bud for new tooth germ).

Mentions: Rostro-caudal and ventro-dorsal graded trends from oral to pharyngeal sites in tooth addition during development and transition of the embryo to juvenile dentition, Polyodon spathula. Differences in total tooth number at each stage of development are shown and reflect a directed pattern in time and space throughout the oropharyngeal cavity. Abbreviations: de, dentary; d.pal, dermopalatine; epb, epibranchial; hb1, 2, hypobranchial 1, 2; iph, infrapharyngobranchial; ppt, pterygopalatine; UBS, LBS, upper, lower branchial skeleton; UJ, LJ, upper, lower jaw. Numbers are per left or right half.


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)

Diagram summarizing stages of tooth germ morphogenesis relative to shh expression (from figure 3p1–4). Intensity of cellular expression is partitioned characteristically within the dental epithelium, with negative differentiated, interactive cells of dental epithelium shown (proactive d.e.), and also in sensory papilla of taste buds on right of tooth germ. (a) Cellular partitioning of shh expression as ‘placode’ (localized within epithelium, can be evaginated). (b) ‘Cap’, expression in the cap-shaped epithelium of tooth germ, surrounding dental papilla. (c) ‘Cone + collar’, cones of dentine with expression associated with the tooth base, or collar epithelium below the cap. (d) ‘Cone + bud’, expression in a new site within the outer dental epithelia (incipient bud for new tooth germ).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSPB20142700F4: Diagram summarizing stages of tooth germ morphogenesis relative to shh expression (from figure 3p1–4). Intensity of cellular expression is partitioned characteristically within the dental epithelium, with negative differentiated, interactive cells of dental epithelium shown (proactive d.e.), and also in sensory papilla of taste buds on right of tooth germ. (a) Cellular partitioning of shh expression as ‘placode’ (localized within epithelium, can be evaginated). (b) ‘Cap’, expression in the cap-shaped epithelium of tooth germ, surrounding dental papilla. (c) ‘Cone + collar’, cones of dentine with expression associated with the tooth base, or collar epithelium below the cap. (d) ‘Cone + bud’, expression in a new site within the outer dental epithelia (incipient bud for new tooth germ).
Mentions: Rostro-caudal and ventro-dorsal graded trends from oral to pharyngeal sites in tooth addition during development and transition of the embryo to juvenile dentition, Polyodon spathula. Differences in total tooth number at each stage of development are shown and reflect a directed pattern in time and space throughout the oropharyngeal cavity. Abbreviations: de, dentary; d.pal, dermopalatine; epb, epibranchial; hb1, 2, hypobranchial 1, 2; iph, infrapharyngobranchial; ppt, pterygopalatine; UBS, LBS, upper, lower branchial skeleton; UJ, LJ, upper, lower jaw. Numbers are per left or right half.

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