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

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

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

5 Citations (Scopus)
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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, while AMEL and SCPP5 are found only in sarcopterygians and actinopterygians, respectively. Actinopterygian AMBN, ENAM, and SCPP5 are expressed during 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 emergence of an ancestral enamel in stem-osteichthyans, while 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, while 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.
Original languageEnglish
Article number102023
Number of pages61
JournaliScience
Volume24
Issue number1
DOIs
Publication statusPublished - 22 Jan 2021

Bibliographical note

Funding Information:
K.K. is grateful to Prof. Joan T. Richtsmeier at Penn State University for critical reading of the manuscript. We acknowledge funding from the National Science Foundation ( BCS0725227 ) and the Penn State Evan Pugh Professors Research Fund to Prof. Kenneth M. Weiss, from the European Commission Marie Curie scheme to M.W. ( 626424 ), from the Royal Commission for the Exhibition of 1851 (1851 Research Fellowship) to M.N.P., from a Royal Society Wolfson Merit Award to P.C.J.D., from the Natural Environment Research Council ( NE/N002067/1 ; NE/P013678/1 ) to P.C.J.D., from the Biotechnology and Biological Sciences Research Council ( BB/N000919/1 ) to P.C.J.D., from the Ministry of Education, Science, and Culture of Japan (Grant-in-Aid 18592013 ) to M.I., and from the Nippon Dental University to I.S. ( NDUF-13-10 , NDUF-14-12 , and NDU Grants N-15015 ) and to M.I. ( NDUF-10-04 , NDUF-11-03 , NDUF-14-07 , NDUF-15-04 , and NDU Grants N-17006 ).

Publisher Copyright:
© 2020 The Author(s)

Keywords

  • enamel
  • ganoin
  • enameloid
  • acrodin
  • enamel matrix
  • SCPP genes

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