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Moya M Smith

Publications and source records attributed to Moya M Smith.

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Developmental and evolutionary origins of the vertebrate dentition: molecular controls for spatio-temporal organisation of tooth sites in osteichthyans.

The rainbow trout (Oncorhynchus mykiss) as a developmental model surpasses both zebrafish and mouse for a more widespread distribution of teeth in the oro-pharynx as the basis for general vertebrate odontogenesis, one in which replacement is an essential requirement. Studies on the rainbow trout have led to the identification of the initial sequential appearance of teeth, through differential gene expression as a changing spatio-temporal pattern, to set in place the primary teeth of the first generation, and also to regulate the continuous production of replacement tooth families. Here we reveal gene expression data that address both the field and clone theories for patterning a polyphyodont osteichthyan dentition. These data inform how the initial pattern may be established through up-regulation at tooth loci from a broad odontogenic band. It appears that control and regulation of replacement pattern resides in the already primed dental epithelium at the sides of the predecessor tooth. A case is presented for the developmental changes that might have occurred during vertebrate evolution, for the origin of a separate successional dental lamina, by comparison with an osteichthyan tetrapod dentition (Ambystoma mexicanum). The evolutionary origins of such a permanent dental lamina are proposed to have occurred from the transient one demonstrated here in the trout. This has implications for phylogenies based on the homology of teeth as only those developed from a dental lamina. Utilising the data generated from the rainbow trout model, we propose this as a standard for comparative development and evolutionary theories of the vertebrate dentition.

Ambystoma↗

How do genes make teeth to order through development?

This introduction to new patterning theories for the vertebrate dentition outlines the historical concepts to explain graded sequences in tooth shape in mammals (incisors, canines, premolars, molars) which change in evolution in a linked manner, constant for each region. The classic developmental models for shape regulation, known as the 'regional field' and 'dental clone' models, were inspired by the human dentition, where it is known that the last tooth in each series is the one commonly absent. The mouse, as a valuable experimental model, has provided data to test these models and more recently, based on spatial-temporal gene expression data, the 'dental homeobox code' was proposed to specify regions and regulate tooth shape. We have attempted to combine these hypotheses in a new model of the combinatorial homeobox gene expression pattern with the clone and field theories in one of 'co-operative genetic interaction'. This also explains the genetic absence of teeth in humans ascribed to point mutations in mesenchymally expressed genes, which affect tooth number in each series.

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Origin and evolution of gnathostome dentitions: a question of teeth and pharyngeal denticles in placoderms.

The fossil group Placodermi is the most phylogenetically basal of the clade of jawed vertebrates but lacks a marginal dentition comparable to that of the dentate Chondrichthyes, Acanthodii and Osteichthyes (crown-group Gnathostomata). The teeth of crown-group gnathostomes are part of an ordered dentition replaced from, and patterned by, a dental lamina, exemplified by the elasmobranch model. A dentition recognised by these criteria has been previously judged absent in placoderms, based on structural evidence such as absence of tooth whorls and typical vertebrate dentine. However, evidence for regulated tooth addition in a precise spatiotemporal order can be observed in placoderms, but significantly, only within the group Arthrodira. In these fossils, as in other jawed vertebrates with statodont, non-replacing dentitions, new teeth are added at the ends of rows below the bite, but in line with biting edges of the dentition. The pattern is different on each gnathal bone and probably arises from single odontogenic primordia on each, but tooth rows are arranged in a distinctive placoderm pattern. New teeth are made of regular dentine comparable to that of crown-gnathostomes, formed from a pulp cavity. This differs from semidentine previously described for placoderm gnathalia, a type present in the external dermal tubercles. The Arthrodira is a derived taxon within the Placodermi, hence origin of teeth in placoderms occurs late in the phylogeny and teeth are convergently derived, relative to those of other jawed vertebrates. More basal placoderm taxa adopted other strategies for providing biting surfaces and these vary substantially, but include addition of denticles to the growing gnathal plates, at the margins of pre-existing denticle patches. These alternative strategies and apparent absence of regular dentine have led to previous interpretations that teeth were entirely absent from the placoderm dentition. A consensus view emerged that a dentition, as developed within a dental lamina, is a synapomorphy characterising the clade of crown-group gnathostomes. Recent comparisons between sets of denticle whorls in the pharyngeal region of the jawless fish Loganellia scotica (Thelodonti) and those in sharks suggest homology of these denticle sets on gill arches. Although the placoderm pharyngeal region appears to lack denticles (placoderm gill arches are poorly known), the posterior wall of the pharyngeal cavity, formed by a bony flange termed the postbranchial lamina, is covered in rows of patterned denticle arrays. These arrays differ significantly, both in morphology and arrangement, from those of the denticles located externally on the head and trunkshield plates. Denticles in these arrays are homologous to denticles associated with the gill arches in other crown-gnathostomes, with pattern similarities for order and position of pharyngeal denticles. From their location in the pharynx these are inferred to be under the influence of a cell lineage from endoderm, rather than ectoderm. Tooth sets and tooth whorls in crown-group gnathostomes are suggested to derive from the pharyngeal denticle whorls, at least in sharks, with the patterning mechanisms co-opted to the oral cavity. A comparable co-option is suggested for the Placodermi.

Animals↗

Conserved deployment of genes during odontogenesis across osteichthyans.

Odontogenesis has only been closely scrutinized at the molecular level in the mouse, an animal with an extremely restricted dentition of only two types and one set. However, within osteichthyans many species display complex and extensive dentitions, which questions the extent to which information from the mouse is applicable to all osteichthyans. We present novel comparative molecular and morphological data in the rainbow trout (Oncorhynchus mykiss) that show that three genes, essential for murine odontogenesis, follow identical spatial-temporal expression. Thus, at all tooth bud sites, epithelial genes Pitx-2 and Shh initiate the odontogenic cascade, resulting in dental mesenchymal Bmp-4 expression, importantly, including the previously unknown formation of replacement teeth. Significantly, this spatial-temporal sequence is the same for marginal and lingual dentitions, but we find notable differences regarding the deployment of Pitx-2 in the developing pharyngeal dentition. This difference may be highly significant in relation to the theory that dentitions may have evolved from pharyngeal tooth sets in jawless fishes. We have provided the first data on operational genes in tooth development to show that the same signalling genes choreograph this evolutionary stable event in fishes since the osteichthyan divergence 420 Myr ago, with the identical spatial-temporal expression as in mammals.

Animals↗

Placoderm fishes, pharyngeal denticles, and the vertebrate dentition.

The correlation of the origin of teeth with jaws in vertebrate history has recently been challenged with an alternative to the canonical view of teeth deriving from separate skin denticles. This alternative proposes that organized denticle whorls on the pharyngeal (gill) arches in the fossil jawless fish Loganellia are precursors to tooth families developing from a dental lamina along the jaw, such as those occurring in sharks, acanthodians, and bony fishes. This not only indicates that homologs of tooth families were present, but also illustrates that they possessed the relevant developmental controls, prior to the evolution of jaws. However, in the Placodermi, a phylogenetically basal group of jawed fishes, the state of pharyngeal denticles is poorly known, tooth whorls are absent, and the presence of teeth homologous to those in extant jawed fishes (Chondrichthyes + Osteichthyes) is controversial. Thus, placoderms would seem to provide little evidence for the early evolution of dentitions, or of denticle whorls, or tooth families, at the base of the clade of jawed fishes. However, organized denticles do occur at the rear of the placoderm gill chamber, but are associated with the postbranchial lamina of the anterior trunkshield, assumed to be part of the dermal cover. Significantly, these denticles have a different organization and morphology relative to the external dermal trunkshield tubercles. We propose that they represent a denticulate part of the visceral skeleton, under the influence of pharyngeal patterning controls comparable to those for pharyngeal denticles in other jawed vertebrates and Loganellia.

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Developmental plasticity and disparity in early dipnoan (lungfish) dentitions.

Although the lungfish (Dipnoi) belong within the Osteichthyes, their dentitions are radically different from other osteichthyans. Lungfish dentitions also show a uniquely high structural disparity during the early evolution of the group, partly owing to the independent variation of odontogenic and odontoclastic processes that are tightly and stereotypically coordinated in other osteichthyans. We present a phylogenetic analysis of early lungfishes incorporating a novel approach to coding these process characters in preference to the resultant adult dental morphology. The results only partially resolve the interrelationships of Devonian dipnoans, but show that the widely discussed hypothesis of separate tooth-plated, dentine-plated, and denticulated lineages is unlikely to be true. The dipnoan status of Diabolepis is corroborated. Lungfish dentitions seem to have undergone extensive and nonparsimonious evolution during the early history of the group, but much of the resulting disparity can be explained by a modest number of evolutionary steps in the underlying developmental processes, those for dental formation (odontogenic) and those for the remodeling of dentine tissue (odontoclastic). Later in lungfish evolution, this disparity was lost as the group settled to a pattern of dental development that is just as stereotypic as, but completely different from, that of other osteichthyans.

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Gene deployment for tooth replacement in the rainbow trout (Oncorhynchus mykiss): a developmental model for evolution of the osteichthyan dentition.

Repeated tooth initiation occurs often in nonmammalian vertebrates (polyphyodontism), recurrently linked with tooth shedding and in a definite order of succession. Regulation of this process has not been genetically defined and it is unclear if the mechanisms for constant generation of replacement teeth (secondary dentition) are similar to those used to generate the primary dentition. We have therefore examined the expression pattern of a sub-set of genes, implicated in tooth initiation in mouse, in relation to replacement tooth production in an osteichthyan fish (Oncorhynchus mykiss). Two epithelial genes pitx2, shh and one mesenchymal bmp4 were analyzed at selected stages of development for O. mykiss. pitx2 expression is upregulated in the basal outer dental epithelium (ODE) of the predecessor tooth and before cell enlargement, on the postero-lingual side only. This coincides with the site for replacement tooth production identifying a region responsible for further tooth generation. This corresponds with the expression of pitx2 at focal spots in the basal oral epithelium during initial (first generation) tooth formation but is now sub-epithelial in position and associated with the dental epithelium of each predecessor tooth. Co-incidental expression of bmp4 and aggregation of the mesenchymal cells identifies the epithelial-mesenchymal interactions and marks initiation of the dental papilla. These together suggest a role in tooth site regulation by pitx2 together with bmp4. Conversely, the expression of shh is confined to the inner dental epithelium during the initiation of the first teeth and is lacking from the ODE in the predecessor teeth, at sites identified as those for replacement tooth initiation. Importantly, these genes expressed during replacement tooth initiation can be used as markers for the sites of "set-aside cells," the committed odontogenic cells both epithelial and mesenchymal, which together can give rise to further generations of teeth. This information may show how initial pattern formation is translated into secondary tooth replacement patterns, as a general mechanism for patterning the vertebrate dentition. Replacement of the marginal sets of teeth serves as a basis for discussion of the evolutionary significance, as these dentate bones (dentary, premaxilla, maxilla) form the restricted arcades of oral teeth in many crown-group gnathostomes, including members of the tetrapod stem group.

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