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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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Serial sagittal sections, Polyodon spathula (stage 45) after in situ hybridization for shh show sequence of tooth morphogenesis. Photomicrographs, low and high magnification (objectives 6.3×, 16×, 40×) of location and rostro-caudal timing of shh gene expression in all tooth fields relative to tooth germ morphogenesis, rostral, left and dorsal, top. (a–d) Most medial section, expression in dermopalatine (cone + collar, p3) and palatopterygoid (placode, p1). (e) More lateral section including Meckel's cartilage and pharyngeal arches. Expression loci associated with first stages of morphogenesis (placode, p1) on the 1st upper branchial arch (iph1), 1st and 2nd hypobranchials. By comparison, on 3rd and 4th pharyngeal arches tooth bud foci absent, localization is a field of expression, a stage prior to tooth morphogenesis. (f) Low magnification field of variation in expression loci on dentary and hypobranchial1, with collar epithelium downregulated on first tooth (asterisk) and adjacent second tooth germ shown as intense expression (arrowhead, weak expression in sensory papilla, arrow as (o, p4). (g) Low magnification view of variation in expression at loci on the dermopalatine (downregulated) and palatopterygoid strong expression in all dental epithelium around dentine cone (late cap stage). (h) Tooth cone (tc) developed, and 2nd tooth germ (2ndt) at cap stage (p2). (i) First hypobranchial, placode stage of shh expression (p1). (j) Tooth cone with second incipient tooth germ (itg), strong expression (p4). (k) Downregulation from cap to ‘collar’ expression (p3) in 2nd tooth. (l) Early tooth placode in oral epithelium of 2nd hypobranchial. (m) Upper jaw palatoquadrate cartilage with tooth germs on dermopalatine and palatopterygoid at different morphogenetic stages. (n) Four stages of shh expression, tooth cone with downregulated expression, incipient second tooth germ on dermoplatine, on palatopterygoid, cap stage. (o) Infrapharyngobranchial (iph1) upregulated strong expression (note evaginated tooth germ, placode-cap), alongside weak expression in sensory papilla (arrow). (p1–4) Four stages of shh expression in tooth germs, oral epithelium dorsal, contrast enhanced (translated into diagram as figure 4a–d). Scale bars (a,e), 250 μm; (b,f,g,m), 50 μm; (c,d,h–l,n–p1–4), 25 μm; abbreviations as in figure 1.
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RSPB20142700F3: Serial sagittal sections, Polyodon spathula (stage 45) after in situ hybridization for shh show sequence of tooth morphogenesis. Photomicrographs, low and high magnification (objectives 6.3×, 16×, 40×) of location and rostro-caudal timing of shh gene expression in all tooth fields relative to tooth germ morphogenesis, rostral, left and dorsal, top. (a–d) Most medial section, expression in dermopalatine (cone + collar, p3) and palatopterygoid (placode, p1). (e) More lateral section including Meckel's cartilage and pharyngeal arches. Expression loci associated with first stages of morphogenesis (placode, p1) on the 1st upper branchial arch (iph1), 1st and 2nd hypobranchials. By comparison, on 3rd and 4th pharyngeal arches tooth bud foci absent, localization is a field of expression, a stage prior to tooth morphogenesis. (f) Low magnification field of variation in expression loci on dentary and hypobranchial1, with collar epithelium downregulated on first tooth (asterisk) and adjacent second tooth germ shown as intense expression (arrowhead, weak expression in sensory papilla, arrow as (o, p4). (g) Low magnification view of variation in expression at loci on the dermopalatine (downregulated) and palatopterygoid strong expression in all dental epithelium around dentine cone (late cap stage). (h) Tooth cone (tc) developed, and 2nd tooth germ (2ndt) at cap stage (p2). (i) First hypobranchial, placode stage of shh expression (p1). (j) Tooth cone with second incipient tooth germ (itg), strong expression (p4). (k) Downregulation from cap to ‘collar’ expression (p3) in 2nd tooth. (l) Early tooth placode in oral epithelium of 2nd hypobranchial. (m) Upper jaw palatoquadrate cartilage with tooth germs on dermopalatine and palatopterygoid at different morphogenetic stages. (n) Four stages of shh expression, tooth cone with downregulated expression, incipient second tooth germ on dermoplatine, on palatopterygoid, cap stage. (o) Infrapharyngobranchial (iph1) upregulated strong expression (note evaginated tooth germ, placode-cap), alongside weak expression in sensory papilla (arrow). (p1–4) Four stages of shh expression in tooth germs, oral epithelium dorsal, contrast enhanced (translated into diagram as figure 4a–d). Scale bars (a,e), 250 μm; (b,f,g,m), 50 μm; (c,d,h–l,n–p1–4), 25 μm; abbreviations as in figure 1.

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)

Serial sagittal sections, Polyodon spathula (stage 45) after in situ hybridization for shh show sequence of tooth morphogenesis. Photomicrographs, low and high magnification (objectives 6.3×, 16×, 40×) of location and rostro-caudal timing of shh gene expression in all tooth fields relative to tooth germ morphogenesis, rostral, left and dorsal, top. (a–d) Most medial section, expression in dermopalatine (cone + collar, p3) and palatopterygoid (placode, p1). (e) More lateral section including Meckel's cartilage and pharyngeal arches. Expression loci associated with first stages of morphogenesis (placode, p1) on the 1st upper branchial arch (iph1), 1st and 2nd hypobranchials. By comparison, on 3rd and 4th pharyngeal arches tooth bud foci absent, localization is a field of expression, a stage prior to tooth morphogenesis. (f) Low magnification field of variation in expression loci on dentary and hypobranchial1, with collar epithelium downregulated on first tooth (asterisk) and adjacent second tooth germ shown as intense expression (arrowhead, weak expression in sensory papilla, arrow as (o, p4). (g) Low magnification view of variation in expression at loci on the dermopalatine (downregulated) and palatopterygoid strong expression in all dental epithelium around dentine cone (late cap stage). (h) Tooth cone (tc) developed, and 2nd tooth germ (2ndt) at cap stage (p2). (i) First hypobranchial, placode stage of shh expression (p1). (j) Tooth cone with second incipient tooth germ (itg), strong expression (p4). (k) Downregulation from cap to ‘collar’ expression (p3) in 2nd tooth. (l) Early tooth placode in oral epithelium of 2nd hypobranchial. (m) Upper jaw palatoquadrate cartilage with tooth germs on dermopalatine and palatopterygoid at different morphogenetic stages. (n) Four stages of shh expression, tooth cone with downregulated expression, incipient second tooth germ on dermoplatine, on palatopterygoid, cap stage. (o) Infrapharyngobranchial (iph1) upregulated strong expression (note evaginated tooth germ, placode-cap), alongside weak expression in sensory papilla (arrow). (p1–4) Four stages of shh expression in tooth germs, oral epithelium dorsal, contrast enhanced (translated into diagram as figure 4a–d). Scale bars (a,e), 250 μm; (b,f,g,m), 50 μm; (c,d,h–l,n–p1–4), 25 μm; abbreviations as in figure 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSPB20142700F3: Serial sagittal sections, Polyodon spathula (stage 45) after in situ hybridization for shh show sequence of tooth morphogenesis. Photomicrographs, low and high magnification (objectives 6.3×, 16×, 40×) of location and rostro-caudal timing of shh gene expression in all tooth fields relative to tooth germ morphogenesis, rostral, left and dorsal, top. (a–d) Most medial section, expression in dermopalatine (cone + collar, p3) and palatopterygoid (placode, p1). (e) More lateral section including Meckel's cartilage and pharyngeal arches. Expression loci associated with first stages of morphogenesis (placode, p1) on the 1st upper branchial arch (iph1), 1st and 2nd hypobranchials. By comparison, on 3rd and 4th pharyngeal arches tooth bud foci absent, localization is a field of expression, a stage prior to tooth morphogenesis. (f) Low magnification field of variation in expression loci on dentary and hypobranchial1, with collar epithelium downregulated on first tooth (asterisk) and adjacent second tooth germ shown as intense expression (arrowhead, weak expression in sensory papilla, arrow as (o, p4). (g) Low magnification view of variation in expression at loci on the dermopalatine (downregulated) and palatopterygoid strong expression in all dental epithelium around dentine cone (late cap stage). (h) Tooth cone (tc) developed, and 2nd tooth germ (2ndt) at cap stage (p2). (i) First hypobranchial, placode stage of shh expression (p1). (j) Tooth cone with second incipient tooth germ (itg), strong expression (p4). (k) Downregulation from cap to ‘collar’ expression (p3) in 2nd tooth. (l) Early tooth placode in oral epithelium of 2nd hypobranchial. (m) Upper jaw palatoquadrate cartilage with tooth germs on dermopalatine and palatopterygoid at different morphogenetic stages. (n) Four stages of shh expression, tooth cone with downregulated expression, incipient second tooth germ on dermoplatine, on palatopterygoid, cap stage. (o) Infrapharyngobranchial (iph1) upregulated strong expression (note evaginated tooth germ, placode-cap), alongside weak expression in sensory papilla (arrow). (p1–4) Four stages of shh expression in tooth germs, oral epithelium dorsal, contrast enhanced (translated into diagram as figure 4a–d). Scale bars (a,e), 250 μm; (b,f,g,m), 50 μm; (c,d,h–l,n–p1–4), 25 μm; abbreviations as in figure 1.
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