Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans

Kazuhiko Kawasaki; Joseph N Keating; Mitsushiro Nakatomi; Monique Welten; Masato Mikami; Ichiro Sasagawa; Mark N Puttick; Philip C J Donoghue; Mikio Ishiyama

doi:10.1016/j.isci.2020.102023

Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans

iScience. 2021 Jan 1;24(1):102023. doi: 10.1016/j.isci.2020.102023. eCollection 2021 Jan 22.

Authors

Kazuhiko Kawasaki¹, Joseph N Keating², Mitsushiro Nakatomi³, Monique Welten², Masato Mikami⁴, Ichiro Sasagawa⁵, Mark N Puttick^{2

6}, Philip C J Donoghue², Mikio Ishiyama⁷

Affiliations

¹ Department of Anthropology, Pennsylvania State University, University Park, PA 16802, USA.
² School of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UK.
³ Division of Anatomy, Kyushu Dental University, Kitakyushu, Fukuoka 803-8580, Japan.
⁴ Department of Microbiology, School of Life Dentistry at Niigata, the Nippon Dental University, Niigata, Niigata 951-8580, Japan.
⁵ Advanced Research Center, School of Life Dentistry at Niigata, the Nippon Dental University, Niigata, Niigata 951-8580, Japan.
⁶ Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK.
⁷ Department of Histology, School of Life Dentistry at Niigata, the Nippon Dental University, Niigata, Niigata 951-8580, Japan.

Abstract

We resolve debate over the evolution of vertebrate hypermineralized tissues through analyses of matrix protein-encoding secretory calcium-binding phosphoprotein (SCPP) genes and phylogenetic inference of hypermineralized tissues. Among these genes, AMBN and ENAM are found in both sarcopterygians and actinopterygians, whereas AMEL and SCPP5 are found only in sarcopterygians and actinopterygians, respectively. Actinopterygian AMBN, ENAM, and SCPP5 are expressed during the formation of hypermineralized tissues on scales and teeth: ganoin, acrodin, and collar enamel in gar, and acrodin and collar enameloid in zebrafish. Our phylogenetic analyses indicate the emergence of an ancestral enamel in stem-osteichthyans, whereas ganoin emerged in stem-actinopterygians and true enamel in stem-sarcopterygians. Thus, AMBN and ENAM originated in concert with ancestral enamel, SCPP5 evolved in association with ganoin, and AMEL evolved with true enamel. Shifts in gene expression domain and timing explain the evolution of different hypermineralized tissues. We propose that hypermineralized tissues in osteichthyans coevolved with matrix SCPP genes.

Keywords: Evolutionary Biology; Evolutionary Processes; Paleobiology; Phylogenetics.