Journal Article

Odontogenic ameloblast-associated (ODAM) is inactivated in toothless/enamelless placental mammals and toothed whales

Randall, Jason, Emerling, Christopher A., Gatesy, John, Hecker, Nikolai, Hiller, Michael, Springer, Mark S., Collin, Matthew A., Delsuc, Frédéric

2019

Overview

Background The 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. Results We 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. Conclusion Our 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.

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: Ameloblasts - metabolism / Analysis / Animal biology / Animal Systematics/Taxonomy/Biogeography / Animals / Aquatic habitats / Aquatic mammals / Archives & records / Base Sequence / Bayes Theorem / Biochemistry, Molecular Biology / Biodiversity / Biodiversity and Ecology / Biomedical and Life Sciences / Calcium / Codon - genetics / Deactivation / Dental enamel / Dental Enamel - metabolism / Dental restorative materials / Edentulism / Enamel / Entomology / Environmental Sciences / Epithelium / Eutheria - genetics / Evolution / Evolution (Biology) / Evolutionary Biology / Exocrine glands / Female / Fossils / Gene expression / Gene Silencing / Genes / Genetic aspects / Genetics and Population Dynamics / Genomes / Genomics / Hypotheses / Inactivation / Junctional epithelium / Life Sciences / Likelihood Functions / Mammals / Marine mammals / Mutation / Mutation - genetics / Natural selection / ODAM / Odontoceti / Odontogenesis / Phosphoproteins / Phylogeny / Physiological aspects / Populations and Evolution / Pregnancy / Proteins / Proteins - genetics / Proteins - metabolism / Pseudogene / Research Article / Software / Speciation and evolutionary genetics / Teeth / Vertebrate Zoology / Vertebrates / Whales / Whales - genetics