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

doi:10.1016/j.isci.2020.102023

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

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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 language	English
Article number	102023
Number of pages	61
Journal	iScience
Volume	24
Issue number	1
DOIs	https://doi.org/10.1016/j.isci.2020.102023
Publication status	Published - 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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title = "Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans",

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. ",

keywords = "enamel, ganoin, enameloid, acrodin, enamel matrix, SCPP genes",

author = "Kazuhiko Kawasaki and Keating, {Joseph N} and Mitsushiro Nakatomi and Welten, {Monique C M} and Masato Mikami and Ichiro Sasagawa and Puttick, {Mark N} and Donoghue, {Philip C J} and Mikio Ishiyama",

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: {\textcopyright} 2020 The Author(s)",

year = "2021",

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doi = "10.1016/j.isci.2020.102023",

language = "English",

volume = "24",

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issn = "2589-0042",

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T1 - Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans

AU - Kawasaki, Kazuhiko

AU - Keating, Joseph N

AU - Nakatomi, Mitsushiro

AU - Welten, Monique C M

AU - Mikami, Masato

AU - Sasagawa, Ichiro

AU - Puttick, Mark N

AU - Donoghue , Philip C J

AU - Ishiyama, Mikio

N1 - 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)

PY - 2021/1/22

Y1 - 2021/1/22

N2 - 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.

AB - 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.

KW - enamel

KW - ganoin

KW - enameloid

KW - acrodin

KW - enamel matrix

KW - SCPP genes

U2 - 10.1016/j.isci.2020.102023

DO - 10.1016/j.isci.2020.102023

M3 - Article (Academic Journal)

C2 - 33506188

SN - 2589-0042

VL - 24

JO - iScience

JF - iScience

IS - 1

M1 - 102023

ER -

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

Abstract

Bibliographical note

Keywords

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