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Expression of 20 SCPP genes during tooth and bone mineralization in Senegal bichir

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Abstract

The African bichir (Polypterus senegalus) is a living representative of Polypteriformes. P. senegalus possesses teeth composed of dentin covered by an enameloid cap and a layer of collar enamel on the tooth shaft, as in lepisosteids. A thin layer of enamel matrix can also be found covering the cap enameloid after its maturation and during the collar enamel formation. Teleosts fish do not possess enamel; teeth are protected by cap and collar enameloid, and inversely in sarcopterygians, where teeth are only covered by enamel, with the exception of the cap enameloid in teeth of larval urodeles. The presence of enameloid and enamel in the teeth of the same organism is an opportunity to solve the evolutionary history of the presence of enamel/enameloid in basal actinopterygians. In silico analyses of the jaw transcriptome of a juvenile bichir provided twenty SCPP transcripts. They included enamel, dentin, and bone-specific SCPPs known in sarcopterygians and several actinopterygian-specific SCPPs. The expression of these 20 genes was investigated by in situ hybridizations on jaw sections during tooth and dentary bone formation. A spatiotemporal expression patterns were established and compared with previous studies of SCPP gene expression during enamel/enameloid and bone formation. Similarities and differences were highlighted, and several SCPP transcripts were found specifically expressed during tooth or bone formation suggesting either conserved or new functions of these SCPPs.

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Data availability

DNA Sequences are accessible in genbank; Genbank accession numbers: (names given in 2016 in Genbank by Sire et al.)

AMBN: KX833883

ENAM: KX923546

AMTN: KX833904

ODAM: KX833888

ODAM-like: KX833889

SCPP-PQ1: KX833901

DSPP: KX833884

IBSP: KX833886

MEPE: KX833887

SPP1: KX833902

SCPP1: KX833890; L.o: KU189281

SCPP3: KX833891 (=SCPP3A); P.s C: KX833892 (=SCPP3C); KX833903 (=SCPP3B

SCPP5: KX833893

SCPP7: KX833896

SCPP7-Like: KX833897

SCPP9: KX833898; L.o: KU189286

SCPP5-like: KX833895

SCPP-LPQ15: KX833900

Abbreviations

AMBN :

ameloblastin

AMEL :

amelogenin

AMTN :

amelotin

bp :

base pairs

DMP1 :

dentin matrix acidic phosphoprotein 1

DSPP :

dentin sialophosphoprotein

DSPPL1 :

dentin sialophosphoprotein-like 1

EMP :

enamel matrix protein

ENAM :

enamelin

FPKM :

fragments per kilobase of exon per million fragments mapped

IBSP :

Integrin binding sialophosphoprotein

KLK :

kallikrein

MABT :

maleic acid buffer tween

MA :

million years

MEPE :

matrix extracellular phosphoglycoprotein

MMP20 :

matrix metalloproteinase 20

NBT/BCIP :

nitro blue tetrazolium chloride/5-bromo-4-chloro-3-indolylphosphate

NGSP :

nested gene specific primer

No :

number

NTM :

NaCL, TrisHCl, MgCl2

ODAM :

odontogenic ameloblast-associated protein

PBS :

phosphate buffered saline

PCR :

polymerase chain reaction

RACE :

rapid amplification of cDNA end

RGD :

arg gly-asp domain

RT-PCR :

reverse transcription polymerase chain reaction

SCPP :

secretory calcium-binding phosphoprotein

SCPP-LPQ :

secretory calcium-binding phosphoprotein-like, proline and glutamine rich

SCPPPQ1 :

secretory calcium-binding phosphoprotein, proline and glutamine rich 1

SPP1 :

secreted phosphoprotein 1

SSC :

saline sodium citrate

UTR :

untranslated region

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Acknowledgements

We thank Marie-Claire Lajarille for paraffin section cutting. We are grateful to the Roscoff Bioinformatics platform ABiMS (http://abims.sb-roscoff.fr), part of the Institut Français de Bioinformatique (ANR-11-INBS-0013) and BioGenouest network, for providing computing and storage resources….

Funding

This project was financially supported by Sorbonne Université, CNRS, and ANR-12-BSV7-020, project “Jaws”.

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Authors and Affiliations

  1. Sorbonne Université, MNHN, CNRS, EPHE, Institut Systématique Évolution Biodiversité, ISYEB, Equipe Homologies, 75005, Paris, France

    S Delgado

  2. Sorbonne Université, CNRS, Institut de Biologie Paris-Seine, UMR 7138, Equipe Evolution et Développement du Squelette, 75005, Paris, France

    MA Fernandez-Trujillo, J Silvent & JY Sire

  3. Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS, CR2P (Centre de Recherche en Paléontologie – Paris), UMR 7207, Equipe Formes, Structures et Fonctions, 43 rue Buffon, 75005, Paris, France

    G Houée

  4. Sorbonne Université - CNRS, FR2424, Station Biologique de Roscoff, Plateforme ABiMS (Analysis and Bioinformatics for Marine Science), 29680, Roscoff, France

    X Liu & E Corre

Authors
  1. S Delgado
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  2. MA Fernandez-Trujillo
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  3. G Houée
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  4. J Silvent
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  5. X Liu
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  6. E Corre
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  7. JY Sire
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Contributions

Fernandez-Trujillo MA and Silvent J carried out the molecular biology experiments. Liu X, Corre E and Sire JY performed in silico data recovery. Fernandez-Trujillo MA, Silvent J, Sire JY conceived and designed the experiments, and wrote the manuscript. Houée G and Delgado S wrote the manuscript and critically revised the manuscript. All authors read and approved the final manuscript. Houée G and Delgado S corrected, submitted the manuscript. Thanks to François Meunier for his corrections and proofreading of the manuscript.

Corresponding author

Correspondence to S Delgado.

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All animal experiments conformed to the directives of the European parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes (Directive 2010/63/EU) and the French Rural Code (Article R214-87 to R214-137, Decree no. 2013-118 of 1st February 2013). Certificate of authorization for vertebrate animal experiment was obtained under the no. 75-600.

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Communicated by Matthias Hammerschmidt

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Supplementary file 1

Supplementary material S1. Forward and reverse primer sequences used for normal PCR in order to build probes for in situ hybridization (ISH) and to check the 20 cDNA sequences identified in the jaw transcriptome of Polypterus senegalus. RACE PCR was used to complete the ENAM and DSPP sequences at the 3' and 5' extremities. The expected length (base pairs) of the probe is indicated between brackets. Two values represent the length of variants 1 and 2, respectively. GenBank accession numbers are indicated. (DOCX 15 kb)

Supplementary file 2

Supplementary material S2. The 20 SCPPs identified in the jaw transcriptome of Polypterus senegalus (P.s). The amino acid sequences of 18 of them are aligned with the homologous sequence (the larger sequence when two variants have been revealed, i.e. in ENAM, SCPP5 and SCPP9) of the spotted gar Lepisosteus oculatus (L.o). The two other bichir SCPPs, SCPP5-like (not found in the submitted spotted gar sequences) and SCPP-LPQ15 (only a short, partial sequence in spotted gar) are presented alone. Signal peptides are underlined and SxE and RGD motifs are highlighted in grey. (.): identical residue to P.s amino acid; (-) gap inserted for alignment purpose; (?): unknown residue. GenBank accession numbers for each sequence is indicated. (DOCX 26 kb)

Supplementary file 3

Supplementary material S3. A) In situ hybridization showing no expression of SCPPs during tooth development. B) Expression of SCPP5 variant 1 and SCPP9 variant 2 transcripts. (PNG 818 kb). Scale bars = 50 μm.

High resolution image (TIF 10767 kb)

Supplementary file 4

Supplementary material S4. Adapted from Mikami et al. (2022). SCPP genes identified in the Senegal bichir genome from Mikami et al. (2022). The 20 genes identified in jaw transcriptome are Surrounded in grey. Scpps coding for P/Q rich proteins are in red, Scpps coding for acidic proteins are in blue. (DOCX 22 kb)

Supplementary file 5

Supplementary material S5 (DOCX 14 kb)

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Delgado, S., Fernandez-Trujillo, M., Houée, G. et al. Expression of 20 SCPP genes during tooth and bone mineralization in Senegal bichir. Dev Genes Evol 233, 91–106 (2023). https://doi.org/10.1007/s00427-023-00706-w

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