SCPP Genes and Their Relatives in Gar: Rapid Expansion of Mineralization Genes in Osteichthyans

Kazuhiko Kawasaki, Masato Mikami, Mitsushiro Nakatomi, Ingo Braasch, Peter Batzel, John H. Postlethwait, Akie Sato, Ichiro Sasagawa, Mikio Ishiyama

Research output: Contribution to journalArticle

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Abstract

Gar is an actinopterygian that has bone, dentin, enameloid, and ganoin (enamel) in teeth and/or scales. Mineralization of these tissues involves genes encoding various secretory calcium-binding phosphoproteins (SCPPs) in osteichthyans, but no SCPP genes have been identified in chondrichthyans to date. In the gar genome, we identified 38 SCPP genes, seven of which encode “acidic-residue-rich” proteins and 31 encode “Pro/Gln (P/Q) rich” proteins. These gar SCPP genes constitute the largest known repertoire, including many newly identified P/Q-rich genes expressed in teeth and/or scales. Among gar SCPP genes, six acidic and three P/Q-rich genes were identified as orthologs of sarcopterygian genes. The sarcopterygian orthologs of most of these acidic genes are involved in bone and/or dentin formation, and sarcopterygian orthologs of all three P/Q-rich genes participate in enamel formation. The finding of these genes in gar suggests that an elaborate SCPP gene-based genetic system for tissue mineralization was already present in stem osteichthyans. While SCPP genes have been thought to originate from ancient SPARCL1, SPARCL1L1 appears to be more closely related to these genes, because it established a structure similar to acidic SCPP genes probably in stem gnathostomes, perhaps at about the same time with the origin of tissue mineralization. Assuming enamel evolved in stem osteichthyans, all P/Q-rich SCPP genes likely arose within the osteichthyan lineage. Furthermore, the absence of acidic SCPP genes in chondrichthyans might be explained by the secondary loss of earliest acidic genes. It appears that many SCPP genes expanded rapidly in stem osteichthyans and in basal actinopterygians.

Original languageEnglish (US)
Pages (from-to)645-665
Number of pages21
JournalJournal of Experimental Zoology Part B: Molecular and Developmental Evolution
Volume328
Issue number7
DOIs
StatePublished - Nov 1 2017

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Lepisosteidae
phosphoproteins
Phosphoproteins
mineralization
calcium
Calcium
gene
Genes
genes
vif Genes
teeth
stem
Dentin
stems
Tooth
tooth
bone
Bone and Bones
bones

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Medicine
  • Animal Science and Zoology
  • Genetics
  • Developmental Biology

Cite this

Kawasaki, Kazuhiko ; Mikami, Masato ; Nakatomi, Mitsushiro ; Braasch, Ingo ; Batzel, Peter ; H. Postlethwait, John ; Sato, Akie ; Sasagawa, Ichiro ; Ishiyama, Mikio. / SCPP Genes and Their Relatives in Gar : Rapid Expansion of Mineralization Genes in Osteichthyans. In: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2017 ; Vol. 328, No. 7. pp. 645-665.
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abstract = "Gar is an actinopterygian that has bone, dentin, enameloid, and ganoin (enamel) in teeth and/or scales. Mineralization of these tissues involves genes encoding various secretory calcium-binding phosphoproteins (SCPPs) in osteichthyans, but no SCPP genes have been identified in chondrichthyans to date. In the gar genome, we identified 38 SCPP genes, seven of which encode “acidic-residue-rich” proteins and 31 encode “Pro/Gln (P/Q) rich” proteins. These gar SCPP genes constitute the largest known repertoire, including many newly identified P/Q-rich genes expressed in teeth and/or scales. Among gar SCPP genes, six acidic and three P/Q-rich genes were identified as orthologs of sarcopterygian genes. The sarcopterygian orthologs of most of these acidic genes are involved in bone and/or dentin formation, and sarcopterygian orthologs of all three P/Q-rich genes participate in enamel formation. The finding of these genes in gar suggests that an elaborate SCPP gene-based genetic system for tissue mineralization was already present in stem osteichthyans. While SCPP genes have been thought to originate from ancient SPARCL1, SPARCL1L1 appears to be more closely related to these genes, because it established a structure similar to acidic SCPP genes probably in stem gnathostomes, perhaps at about the same time with the origin of tissue mineralization. Assuming enamel evolved in stem osteichthyans, all P/Q-rich SCPP genes likely arose within the osteichthyan lineage. Furthermore, the absence of acidic SCPP genes in chondrichthyans might be explained by the secondary loss of earliest acidic genes. It appears that many SCPP genes expanded rapidly in stem osteichthyans and in basal actinopterygians.",
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Kawasaki, K, Mikami, M, Nakatomi, M, Braasch, I, Batzel, P, H. Postlethwait, J, Sato, A, Sasagawa, I & Ishiyama, M 2017, 'SCPP Genes and Their Relatives in Gar: Rapid Expansion of Mineralization Genes in Osteichthyans', Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, vol. 328, no. 7, pp. 645-665. https://doi.org/10.1002/jez.b.22755

SCPP Genes and Their Relatives in Gar : Rapid Expansion of Mineralization Genes in Osteichthyans. / Kawasaki, Kazuhiko; Mikami, Masato; Nakatomi, Mitsushiro; Braasch, Ingo; Batzel, Peter; H. Postlethwait, John; Sato, Akie; Sasagawa, Ichiro; Ishiyama, Mikio.

In: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 328, No. 7, 01.11.2017, p. 645-665.

Research output: Contribution to journalArticle

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T2 - Rapid Expansion of Mineralization Genes in Osteichthyans

AU - Kawasaki, Kazuhiko

AU - Mikami, Masato

AU - Nakatomi, Mitsushiro

AU - Braasch, Ingo

AU - Batzel, Peter

AU - H. Postlethwait, John

AU - Sato, Akie

AU - Sasagawa, Ichiro

AU - Ishiyama, Mikio

PY - 2017/11/1

Y1 - 2017/11/1

N2 - Gar is an actinopterygian that has bone, dentin, enameloid, and ganoin (enamel) in teeth and/or scales. Mineralization of these tissues involves genes encoding various secretory calcium-binding phosphoproteins (SCPPs) in osteichthyans, but no SCPP genes have been identified in chondrichthyans to date. In the gar genome, we identified 38 SCPP genes, seven of which encode “acidic-residue-rich” proteins and 31 encode “Pro/Gln (P/Q) rich” proteins. These gar SCPP genes constitute the largest known repertoire, including many newly identified P/Q-rich genes expressed in teeth and/or scales. Among gar SCPP genes, six acidic and three P/Q-rich genes were identified as orthologs of sarcopterygian genes. The sarcopterygian orthologs of most of these acidic genes are involved in bone and/or dentin formation, and sarcopterygian orthologs of all three P/Q-rich genes participate in enamel formation. The finding of these genes in gar suggests that an elaborate SCPP gene-based genetic system for tissue mineralization was already present in stem osteichthyans. While SCPP genes have been thought to originate from ancient SPARCL1, SPARCL1L1 appears to be more closely related to these genes, because it established a structure similar to acidic SCPP genes probably in stem gnathostomes, perhaps at about the same time with the origin of tissue mineralization. Assuming enamel evolved in stem osteichthyans, all P/Q-rich SCPP genes likely arose within the osteichthyan lineage. Furthermore, the absence of acidic SCPP genes in chondrichthyans might be explained by the secondary loss of earliest acidic genes. It appears that many SCPP genes expanded rapidly in stem osteichthyans and in basal actinopterygians.

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