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.
Bibliographical noteFunding 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 ).
© 2020 The Author(s)
- enamel matrix
- SCPP genes