Developmental mechanisms driving complex tooth shape in reptiles

Abstract

Background In mammals, odontogenesis is regulated by transient signaling centers known as enamel knots (EKs), which drive the dental epithelium shaping. However, the developmental mechanisms contributing to formation of complex tooth shape in reptiles are not fully understood. Here, we aim to elucidate whether signaling organizers similar to EKs appear during reptilian odontogenesis and how enamel ridges are formed. Results Morphological structures resembling the mammalian EK were found during reptile odontogenesis. Similar to mammalian primary EKs, they exhibit the presence of apoptotic cells and no proliferating cells. Moreover, expression of mammalian EK‐specific molecules (SHH, FGF4, and ST14) and GLI2‐negative cells were found in reptilian EK‐like areas. 3D analysis of the nucleus shape revealed distinct rearrangement of the cells associated with enamel groove formation. This process was associated with ultrastructural changes and lipid droplet accumulation in the cells directly above the forming ridge, accompanied by alteration of membranous molecule expression (Na/K‐ATPase) and cytoskeletal rearrangement (F‐actin). Conclusions The final complex shape of reptilian teeth is orchestrated by a combination of changes in cell signaling, cell shape, and cell rearrangement. All these factors contribute to asymmetry in the inner enamel epithelium development, enamel deposition, ultimately leading to the formation of characteristic enamel ridges.

Multiple evolutionary origins and losses of tooth complexity in squamates

“…Squamata is recognized for including species bearing complex multicuspid teeth within heterodont dentitions 20 , and squamate ecology spans a broad range of past and present niches. Squamates express dental marker genes broadly conserved across vertebrates 18 , with varying patterns of localization and expression compared to mammals, and structures at least partially homologous to mammalian enamel knots (non-proliferative signalling centres of ectodermal cells) determine tooth shape in some squamate clades 19,21,22 . In mammals – the most commonly studied dental system – novel morphologies arise from developmental changes in tooth morphogenesis 23 .…”

“…Several dental developmental differences to mammals can be suggested to explain why squamates didn’t fall into a developmental complexity trap 40 , but instead evolved complex teeth highly liable to developmental instability and simplification 41 . These include simpler, less compartmentalised expression of dental development genes during tooth formation 19,22 , a less complex morphological starting point than mammal teeth 7 , and potentially simpler and/or looser gene regulatory networks 18 . We propose these characteristics of squamates explain both the evolutionary lability of their dental complexity and diet, and the near-complete absence of mammal-like teeth in over 250 million years of squamate history 42 .…”

Coordinated labio-lingual asymmetries in dental and bone development create a symmetrical acrodont dentition

“…Previously, we revealed that matriptase (also known as ST14, TADG15, or epithin) is expressed in the enamel knot at the cap stage but also exhibits distinct expression in the tooth germ of chameleons 17 . Here, we asked if the expression in the tooth germ is restricted to specific part of the dental loop and how the expression pattern appears in the interdental areas.…”

“…To further determine labio-lingual differences, we analyzed the expression of ST14 (matriptase) during chameleon odontogenesis. Matriptase is a serine protease, which plays critical role in the maintenance of epithelial integrity in numerous tissues [23][24][25] , and is also expressed in the enamel knot during murine tooth development 17 . At early stages of development (bud to cap), ST14 was expressed on the lingual side of the cervical loop (Fig.…”

“…Ultra-thin sections were placed on formvar-coated nickel grids and contrasted with lead citrate and uranyl acetate. More details were published previously elsewhere 17 .…”