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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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Expression of shh, bmp4 in Polyodon spathula oral and pharyngeal initial dentitions, stage 41. (a–c,e) shh expression in tooth buds of cleared whole mount jaws compared with (d) stage 37 upper jaw, expression restricted to oral surfaces and on first infrapharygobranchial arches. (a,c) Multiple loci on tooth fields of dentary and dermopalatine, only two loci on hypobranchial and palatopterygoid. Arrows indicate alternate timing of strongest expression. (b,e) Strong expression in hypobranchial 1 and palatopterygoid (arrowheads); cone expression in dentary, hypobranchial, dermopalatine, compared to early placode expression on palatopterygoid. (f–i) bmp4 expression for comparison to shh expression. (f,g) Lower jaw, (h,i) upper jaw bmp4 in the dental papillary mesenchyme marks all oral jaw tooth positions. Dental mesenchyme underlies the dental epithelium and expression appears diffuse, however, more intense expression is seen at alternate tooth loci (arrows, f,g,i) with weaker expression indicating earlier (older) loci (asterisk), equivalent to shh expression pattern. Abbreviations: b1, 2, basibranchials; ba, bone of attachment, cb1–5, ceratobranchials; ch, ceratohyal; de, dentary; d.pal, dermopalatine; hb1, 2, 1st, 2nd hypobranchial; hb1tp, hb2tp, hypobranchial toothplates; hh, hypohyal; hym, hyomandibular; itg, incipient tooth germ; iph, infrapharyngobranchial; iphtp, infrapharyngobranchial toothplate; Mc, Meckels's cartilage; ppt, palatopterygoid; tc, tooth cone; 2ndt, second tooth.
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RSPB20142700F1: Expression of shh, bmp4 in Polyodon spathula oral and pharyngeal initial dentitions, stage 41. (a–c,e) shh expression in tooth buds of cleared whole mount jaws compared with (d) stage 37 upper jaw, expression restricted to oral surfaces and on first infrapharygobranchial arches. (a,c) Multiple loci on tooth fields of dentary and dermopalatine, only two loci on hypobranchial and palatopterygoid. Arrows indicate alternate timing of strongest expression. (b,e) Strong expression in hypobranchial 1 and palatopterygoid (arrowheads); cone expression in dentary, hypobranchial, dermopalatine, compared to early placode expression on palatopterygoid. (f–i) bmp4 expression for comparison to shh expression. (f,g) Lower jaw, (h,i) upper jaw bmp4 in the dental papillary mesenchyme marks all oral jaw tooth positions. Dental mesenchyme underlies the dental epithelium and expression appears diffuse, however, more intense expression is seen at alternate tooth loci (arrows, f,g,i) with weaker expression indicating earlier (older) loci (asterisk), equivalent to shh expression pattern. Abbreviations: b1, 2, basibranchials; ba, bone of attachment, cb1–5, ceratobranchials; ch, ceratohyal; de, dentary; d.pal, dermopalatine; hb1, 2, 1st, 2nd hypobranchial; hb1tp, hb2tp, hypobranchial toothplates; hh, hypohyal; hym, hyomandibular; itg, incipient tooth germ; iph, infrapharyngobranchial; iphtp, infrapharyngobranchial toothplate; Mc, Meckels's cartilage; ppt, palatopterygoid; tc, tooth cone; 2ndt, second tooth.

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)

Expression of shh, bmp4 in Polyodon spathula oral and pharyngeal initial dentitions, stage 41. (a–c,e) shh expression in tooth buds of cleared whole mount jaws compared with (d) stage 37 upper jaw, expression restricted to oral surfaces and on first infrapharygobranchial arches. (a,c) Multiple loci on tooth fields of dentary and dermopalatine, only two loci on hypobranchial and palatopterygoid. Arrows indicate alternate timing of strongest expression. (b,e) Strong expression in hypobranchial 1 and palatopterygoid (arrowheads); cone expression in dentary, hypobranchial, dermopalatine, compared to early placode expression on palatopterygoid. (f–i) bmp4 expression for comparison to shh expression. (f,g) Lower jaw, (h,i) upper jaw bmp4 in the dental papillary mesenchyme marks all oral jaw tooth positions. Dental mesenchyme underlies the dental epithelium and expression appears diffuse, however, more intense expression is seen at alternate tooth loci (arrows, f,g,i) with weaker expression indicating earlier (older) loci (asterisk), equivalent to shh expression pattern. Abbreviations: b1, 2, basibranchials; ba, bone of attachment, cb1–5, ceratobranchials; ch, ceratohyal; de, dentary; d.pal, dermopalatine; hb1, 2, 1st, 2nd hypobranchial; hb1tp, hb2tp, hypobranchial toothplates; hh, hypohyal; hym, hyomandibular; itg, incipient tooth germ; iph, infrapharyngobranchial; iphtp, infrapharyngobranchial toothplate; Mc, Meckels's cartilage; ppt, palatopterygoid; tc, tooth cone; 2ndt, second tooth.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSPB20142700F1: Expression of shh, bmp4 in Polyodon spathula oral and pharyngeal initial dentitions, stage 41. (a–c,e) shh expression in tooth buds of cleared whole mount jaws compared with (d) stage 37 upper jaw, expression restricted to oral surfaces and on first infrapharygobranchial arches. (a,c) Multiple loci on tooth fields of dentary and dermopalatine, only two loci on hypobranchial and palatopterygoid. Arrows indicate alternate timing of strongest expression. (b,e) Strong expression in hypobranchial 1 and palatopterygoid (arrowheads); cone expression in dentary, hypobranchial, dermopalatine, compared to early placode expression on palatopterygoid. (f–i) bmp4 expression for comparison to shh expression. (f,g) Lower jaw, (h,i) upper jaw bmp4 in the dental papillary mesenchyme marks all oral jaw tooth positions. Dental mesenchyme underlies the dental epithelium and expression appears diffuse, however, more intense expression is seen at alternate tooth loci (arrows, f,g,i) with weaker expression indicating earlier (older) loci (asterisk), equivalent to shh expression pattern. Abbreviations: b1, 2, basibranchials; ba, bone of attachment, cb1–5, ceratobranchials; ch, ceratohyal; de, dentary; d.pal, dermopalatine; hb1, 2, 1st, 2nd hypobranchial; hb1tp, hb2tp, hypobranchial toothplates; hh, hypohyal; hym, hyomandibular; itg, incipient tooth germ; iph, infrapharyngobranchial; iphtp, infrapharyngobranchial toothplate; Mc, Meckels's cartilage; ppt, palatopterygoid; tc, tooth cone; 2ndt, second tooth.
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