Abstract
BackgroundThe gene for odontogenic ameloblast-associated (ODAM) is a member of the secretory calcium-binding phosphoprotein gene family. ODAM is primarily expressed in dental tissues including the enamel organ and the junctional epithelium, and may also have pleiotropic functions that are unrelated to teeth. Here, we leverage the power of natural selection to test competing hypotheses that ODAM is tooth-specific versus pleiotropic. Specifically, we compiled and screened complete protein-coding sequences, plus sequences for flanking intronic regions, for ODAM in 165 placental mammals to determine if this gene contains inactivating mutations in lineages that either lack teeth (baleen whales, pangolins, anteaters) or lack enamel on their teeth (aardvarks, sloths, armadillos), as would be expected if the only essential functions of ODAM are related to tooth development and the adhesion of the gingival junctional epithelium to the enamel tooth surface.ResultsWe discovered inactivating mutations in all species of placental mammals that either lack teeth or lack enamel on their teeth. A surprising result is that ODAM is also inactivated in a few additional lineages including all toothed whales that were examined. We hypothesize that ODAM inactivation is related to the simplified outer enamel surface of toothed whales. An alternate hypothesis is that ODAM inactivation in toothed whales may be related to altered antimicrobial functions of the junctional epithelium in aquatic habitats. Selection analyses on ODAM sequences revealed that the composite dN/dS value for pseudogenic branches is close to 1.0 as expected for a neutrally evolving pseudogene. DN/dS values on transitional branches were used to estimate ODAM inactivation times. In the case of pangolins, ODAM was inactivated ~ 65 million years ago, which is older than the oldest pangolin fossil (Eomanis, 47 Ma) and suggests an even more ancient loss or simplification of teeth in this lineage.ConclusionOur results validate the hypothesis that the only essential functions of ODAM that are maintained by natural selection are related to tooth development and/or the maintenance of a healthy junctional epithelium that attaches to the enamel surface of teeth.
Highlights
The gene for odontogenic ameloblast-associated (ODAM) is a member of the secretory calciumbinding phosphoprotein gene family
Several features of the ODAM gene tree are in minor conflict with generally accepted species trees including the placement of Physeter as the sister group to mysticetes rather than other odontocetes [65, 66], an association of Pholidota with Chiroptera rather than Carnivora [44], a sister group relationship between Hipposideridae + Rhinolophidae and yangochiropteran bats instead of with other rhinolophoid bats [43, 67], an association of chlamyphorine armadillos (Chlamyphorus, Calyptophractus) with Chaetophractus rather than with tolypeutines (Tolypeutes, Cabassous) [45], a basal split between Condylura and other eulipotyphlans instead of between Solenodon and other eulipotyphlans [44, 68, 69], and the nonmonophyly of Elephantidae with the mammutid Mammut americanum nested inside of this clade instead of sister to this clade [70, 71]
Given the broad phylogenetic spread of mammalian lineages with inactivating mutations, these results suggest that the only essential functions of ODAM that are maintained by natural selection are related to tooth development and/ or maintenance of the adhesion of the junctional epithelium to the tooth surface, even though ODAM expression has been reported in other tissues such as salivary gland, trachea, mammary gland, and lacrimal gland [14, 15]
Summary
The gene for odontogenic ameloblast-associated (ODAM) is a member of the secretory calciumbinding phosphoprotein gene family. ODAM is expressed in the junctional epithelium, which is a specialized epithelium that attaches the soft tissue of the gingiva (gums) to the enamel surface of the tooth and protects against bacteria that promote periodontal disease [5,6,7,8,9]. In this capacity, ODAM plays a critical role in the first line of defense against bacterial invasion [10].
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