Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans
Summary: 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 sarcoptery...
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Elsevier
2021-01-01
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| Series: | iScience |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004220312207 |
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| author | Kazuhiko Kawasaki Joseph N. Keating Mitsushiro Nakatomi Monique Welten Masato Mikami Ichiro Sasagawa Mark N. Puttick Philip C.J. Donoghue Mikio Ishiyama |
| author_facet | Kazuhiko Kawasaki Joseph N. Keating Mitsushiro Nakatomi Monique Welten Masato Mikami Ichiro Sasagawa Mark N. Puttick Philip C.J. Donoghue Mikio Ishiyama |
| author_sort | Kazuhiko Kawasaki |
| collection | DOAJ |
| description | Summary: 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. |
| first_indexed | 2024-12-21T14:14:02Z |
| format | Article |
| id | doaj.art-fec7547577f348df947909551a582f49 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-12-21T14:14:02Z |
| publishDate | 2021-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-fec7547577f348df947909551a582f492022-12-21T19:00:58ZengElsevieriScience2589-00422021-01-01241102023Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyansKazuhiko Kawasaki0Joseph N. Keating1Mitsushiro Nakatomi2Monique Welten3Masato Mikami4Ichiro Sasagawa5Mark N. Puttick6Philip C.J. Donoghue7Mikio Ishiyama8Department of Anthropology, Pennsylvania State University, University Park, PA 16802, USA; Corresponding authorSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UKDivision of Anatomy, Kyushu Dental University, Kitakyushu, Fukuoka 803-8580, JapanSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UKDepartment of Microbiology, School of Life Dentistry at Niigata, the Nippon Dental University, Niigata, Niigata 951-8580, JapanAdvanced Research Center, School of Life Dentistry at Niigata, the Nippon Dental University, Niigata, Niigata 951-8580, JapanSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UK; Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UKSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UKDepartment of Histology, School of Life Dentistry at Niigata, the Nippon Dental University, Niigata, Niigata 951-8580, JapanSummary: 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.http://www.sciencedirect.com/science/article/pii/S2589004220312207Evolutionary BiologyEvolutionary ProcessesPhylogeneticsPaleobiology |
| spellingShingle | Kazuhiko Kawasaki Joseph N. Keating Mitsushiro Nakatomi Monique Welten Masato Mikami Ichiro Sasagawa Mark N. Puttick Philip C.J. Donoghue Mikio Ishiyama Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans iScience Evolutionary Biology Evolutionary Processes Phylogenetics Paleobiology |
| title | Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans |
| title_full | Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans |
| title_fullStr | Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans |
| title_full_unstemmed | Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans |
| title_short | Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans |
| title_sort | coevolution of enamel ganoin enameloid and their matrix scpp genes in osteichthyans |
| topic | Evolutionary Biology Evolutionary Processes Phylogenetics Paleobiology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004220312207 |
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