Bank vole genomics links determinate and indeterminate growth of teeth.
Dental
Development
Evolution
Genome
Glires
Molar
Rodent
Root
Selection
Tooth
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
received:
23
06
2024
accepted:
14
10
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Continuously growing teeth are an important innovation in mammalian evolution, yet genetic regulation of continuous growth by stem cells remains incompletely understood. Dental stem cells responsible for tooth crown growth are lost at the onset of tooth root formation. Genetic signaling that initiates this loss is difficult to study with the ever-growing incisor and rooted molars of mice, the most common mammalian dental model species, because signals for root formation overlap with signals that pattern tooth size and shape (i.e., cusp patterns). Bank and prairie voles (Cricetidae, Rodentia, Glires) have evolved rooted and unrooted molars while retaining similar size and shape, providing alternative models for studying roots. We assembled a de novo genome of Myodes glareolus, a vole with high-crowned, rooted molars, and performed genomic and transcriptomic analyses in a broad phylogenetic context of Glires (rodents and lagomorphs) to assess differential selection and evolution in tooth forming genes. Bulk transcriptomics comparisons of embryonic molar development between bank voles and mice demonstrated overall conservation of gene expression levels, with species-specific differences corresponding to the accelerated and more extensive patterning of the vole molar. We leverage convergent evolution of unrooted molars across the clade to examine changes that may underlie the evolution of unrooted molars. We identified 15 dental genes with changing synteny relationships and six dental genes undergoing positive selection across Glires, two of which were undergoing positive selection in species with unrooted molars, Dspp and Aqp1. Decreased expression of both genes in prairie voles with unrooted molars compared to bank voles supports the presence of positive selection and may underlie differences in root formation. Our results support ongoing evolution of dental genes across Glires and identify candidate genes for mechanistic studies of root formation. Comparative research using the bank vole as a model species can reveal the complex evolutionary background of convergent evolution for ever-growing molars.
Sections du résumé
BACKGROUND
BACKGROUND
Continuously growing teeth are an important innovation in mammalian evolution, yet genetic regulation of continuous growth by stem cells remains incompletely understood. Dental stem cells responsible for tooth crown growth are lost at the onset of tooth root formation. Genetic signaling that initiates this loss is difficult to study with the ever-growing incisor and rooted molars of mice, the most common mammalian dental model species, because signals for root formation overlap with signals that pattern tooth size and shape (i.e., cusp patterns). Bank and prairie voles (Cricetidae, Rodentia, Glires) have evolved rooted and unrooted molars while retaining similar size and shape, providing alternative models for studying roots.
RESULTS
RESULTS
We assembled a de novo genome of Myodes glareolus, a vole with high-crowned, rooted molars, and performed genomic and transcriptomic analyses in a broad phylogenetic context of Glires (rodents and lagomorphs) to assess differential selection and evolution in tooth forming genes. Bulk transcriptomics comparisons of embryonic molar development between bank voles and mice demonstrated overall conservation of gene expression levels, with species-specific differences corresponding to the accelerated and more extensive patterning of the vole molar. We leverage convergent evolution of unrooted molars across the clade to examine changes that may underlie the evolution of unrooted molars. We identified 15 dental genes with changing synteny relationships and six dental genes undergoing positive selection across Glires, two of which were undergoing positive selection in species with unrooted molars, Dspp and Aqp1. Decreased expression of both genes in prairie voles with unrooted molars compared to bank voles supports the presence of positive selection and may underlie differences in root formation.
CONCLUSIONS
CONCLUSIONS
Our results support ongoing evolution of dental genes across Glires and identify candidate genes for mechanistic studies of root formation. Comparative research using the bank vole as a model species can reveal the complex evolutionary background of convergent evolution for ever-growing molars.
Identifiants
pubmed: 39472825
doi: 10.1186/s12864-024-10901-2
pii: 10.1186/s12864-024-10901-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1000Subventions
Organisme : National Science Foundation
ID : CNS-0958379
Organisme : Helsingin Yliopisto
ID : Doctoral Programme in Biomedicine
Organisme : NIDCR NIH HHS
ID : R01-DE027620
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
R Soc Open Sci. 2018 Jan 3;5(1):170761
pubmed: 29410800
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Nature. 2015 Jun 4;522(7554):81-4
pubmed: 25799987
Nat Commun. 2014 Jun 03;5:3966
pubmed: 24892994
Development. 2002 Jul;129(13):3021-32
pubmed: 12070079
Curr Opin Plant Biol. 2017 Apr;36:129-134
pubmed: 28327435
Trends Genet. 2020 May;36(5):383-384
pubmed: 32029288
Proc Natl Acad Sci U S A. 2019 Feb 5;116(6):2165-2174
pubmed: 30674676
Eur J Hum Genet. 2015 Apr;23(4):445-51
pubmed: 25118030
J Exp Zool B Mol Dev Evol. 2021 Jan;336(1):7-17
pubmed: 33128445
BMC Genomics. 2014 Nov 28;15:1036
pubmed: 25429894
Development. 2006 Apr;133(7):1359-66
pubmed: 16510502
Nucleic Acids Res. 2016 Jan 4;44(D1):D81-9
pubmed: 26612867
Genome Res. 2019 Apr;29(4):635-645
pubmed: 30894395
Nucleic Acids Res. 2012 Apr;40(7):e49
pubmed: 22217600
Plant Physiol. 2014 Feb;164(2):513-24
pubmed: 24306534
Dev Dyn. 2006 May;235(5):1167-80
pubmed: 16450392
Nucleic Acids Res. 2014 Jul;42(12):e99
pubmed: 24803667
Nat Rev Genet. 2012 Jun 18;13(7):505-16
pubmed: 22705669
Bioinformatics. 2017 Jul 15;33(14):2202-2204
pubmed: 28369201
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
Genome Res. 2017 May;27(5):757-767
pubmed: 28381613
J Dent Res. 2003 Mar;82(3):172-6
pubmed: 12598544
J Biol Chem. 2003 Jul 4;278(27):24874-80
pubmed: 12721295
Bioinformatics. 2012 Dec 15;28(24):3211-7
pubmed: 23071270
Nat Rev Genet. 2007 Mar;8(3):206-16
pubmed: 17304246
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
FEBS J. 2020 Apr;287(7):1262-1283
pubmed: 32250558
J Mol Biol. 1999 Sep 17;292(2):195-202
pubmed: 10493868
J Bone Miner Res. 2012 Jun;27(6):1309-21
pubmed: 22392858
Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14444-8
pubmed: 11121045
Environ Pollut. 2004 Sep;131(1):71-9
pubmed: 15210277
G3 (Bethesda). 2018 Jul 2;8(7):2145-2152
pubmed: 29794166
Mol Biol Evol. 2015 Oct;32(10):2798-800
pubmed: 26130081
Genetics. 2004 Oct;168(2):1041-51
pubmed: 15514074
Evol Dev. 2016 Jan-Feb;18(1):31-40
pubmed: 26086993
Chem Rev. 2022 Aug 24;122(16):13401-13446
pubmed: 35839101
Genome Biol. 2014;15(12):550
pubmed: 25516281
Mech Dev. 2000 Mar 15;92(1):19-29
pubmed: 10704885
Front Physiol. 2014 Aug 28;5:324
pubmed: 25221518
Heredity (Edinb). 2017 Apr;118(4):348-357
pubmed: 27782121
Science. 2015 May 22;348(6237):880-6
pubmed: 25999502
J Dent Res. 2016 Mar;95(3):302-10
pubmed: 26503913
Proc Biol Sci. 2018 Nov 7;285(1890):
pubmed: 30404877
Nat Biotechnol. 2020 Mar;38(3):276-278
pubmed: 32055031
Hum Mol Genet. 2003 Apr 1;12 Spec No 1:R69-73
pubmed: 12668599
Annu Rev Plant Biol. 2007;58:377-406
pubmed: 17280525
Sci Rep. 2018 Feb 12;8(1):2797
pubmed: 29434310
Development. 2003 Sep;130(18):4451-60
pubmed: 12900460
Genome Res. 2018 Nov;28(11):1720-1732
pubmed: 30341161
Genome Biol. 2002;3(5):reviews1012
pubmed: 12049669
Stem Cell Reports. 2023 May 9;18(5):1166-1181
pubmed: 37084723
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Cells Tissues Organs. 2011;194(2-4):113-8
pubmed: 21555860
PeerJ. 2020 Mar 31;8:e8813
pubmed: 32266119
Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14338-43
pubmed: 16176987
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12
pubmed: 16845082
Genome Res. 2008 Jan;18(1):188-96
pubmed: 18025269
J Clin Invest. 1994 Sep;94(3):1043-9
pubmed: 7521882
Epigenetics Chromatin. 2022 Jan 29;15(1):4
pubmed: 35090532
Nature. 2011 Oct 12;478(7370):476-82
pubmed: 21993624
Environ Pollut. 2000 Dec;110(3):441-9
pubmed: 15092823
Bone. 2008 Dec;43(6):983-90
pubmed: 18789408
PLoS Comput Biol. 2021 Sep 10;17(9):e1008947
pubmed: 34506480
J Bone Miner Res. 2020 Nov;35(11):2252-2264
pubmed: 32569388
BMC Bioinformatics. 2017 Nov 21;18(1):507
pubmed: 29162056
Genome Res. 2017 May;27(5):722-736
pubmed: 28298431
Bioinformatics. 2011 Mar 15;27(6):757-63
pubmed: 21216780
Mol Biol Evol. 2015 Mar;32(3):820-32
pubmed: 25540451
Nucleic Acids Res. 2019 Jul 2;47(W1):W402-W407
pubmed: 31251384
Biomed Res. 2012;33(4):225-33
pubmed: 22975633
Nucleic Acids Res. 2013 Jan;41(Database issue):D70-82
pubmed: 23203985
Genome Res. 2017 May;27(5):849-864
pubmed: 28396521
Nat Commun. 2011;2:248
pubmed: 21427719
Development. 2002 Mar;129(6):1533-41
pubmed: 11880361
Bioinformatics. 2014 Dec 15;30(24):3558-60
pubmed: 25172923
Mol Biol Evol. 2005 Apr;22(4):1107-18
pubmed: 15689528
Arch Oral Biol. 1973 Apr;18(4):543-53
pubmed: 4516067
J Dent Res. 2023 Jun;102(6):589-598
pubmed: 36919873
Science. 2007 Feb 9;315(5813):848-53
pubmed: 17289997
Trends Genet. 2005 Dec;21(12):673-82
pubmed: 16242204
Curr Protoc Bioinformatics. 2014 Dec 12;48:4.11.1-4.11.39
pubmed: 25501943
Nat Biotechnol. 2016 Mar;34(3):303-11
pubmed: 26829319
BMC Bioinformatics. 2009 Feb 23;10:67
pubmed: 19236712
Anat Rec (Hoboken). 2009 Feb;292(2):299-308
pubmed: 19051250
Development. 2003 Mar;130(6):1049-57
pubmed: 12571097
Development. 2012 Oct;139(19):3487-97
pubmed: 22949612
Sci Adv. 2019 Apr 10;5(4):eaaw1668
pubmed: 30989119
Nat Commun. 2017 Sep 5;8(1):441
pubmed: 28874668
Gene. 2005 Jan 17;345(1):119-26
pubmed: 15716085
Plant Cell. 2017 Jun;29(6):1278-1292
pubmed: 28584165
Bioinformatics. 2013 Apr 15;29(8):1072-5
pubmed: 23422339
PLoS Genet. 2008 Aug 01;4(8):e1000144
pubmed: 18670650
Curr Protoc Bioinformatics. 2014 Dec 12;48:3.13.1-3.13.16
pubmed: 25501942
Nat Genet. 2018 Nov;50(11):1574-1583
pubmed: 30275530
Genome Biol Evol. 2013;5(7):1324-35
pubmed: 23781097
IEEE/ACM Trans Comput Biol Bioinform. 2013 May-Jun;10(3):645-56
pubmed: 24091398
Mol Biol Evol. 2005 Dec;22(12):2472-9
pubmed: 16107592
Dev Genes Evol. 1998 Nov;208(9):477-86
pubmed: 9799429
Bioinformatics. 2019 Jul 15;35(14):i117-i126
pubmed: 31510664
Exp Cell Res. 2014 Jul 15;325(2):78-82
pubmed: 24560742
Nature. 2004 Apr 1;428(6982):493-521
pubmed: 15057822
Mol Ecol. 2010 Mar;19 Suppl 1:255-65
pubmed: 20331784
Proc Natl Acad Sci U S A. 2015 Jan 20;112(3):905-10
pubmed: 25548158
Wiley Interdiscip Rev Dev Biol. 2017 May;6(3):
pubmed: 28251841
J Anat. 2009 Apr;214(4):477-501
pubmed: 19422426
BMC Bioinformatics. 2018 Jan 30;19(1):26
pubmed: 29382321
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Int J Biochem Cell Biol. 2009 Feb;41(2):298-306
pubmed: 18929678
Proc Natl Acad Sci U S A. 2023 Jun 20;120(25):e2300374120
pubmed: 37307487
Matrix Biol. 2016 May-Jul;52-54:60-77
pubmed: 26763578
J Cell Biol. 1999 Oct 4;147(1):105-20
pubmed: 10508859
Proc Biol Sci. 1994 May 23;256(1346):119-24
pubmed: 8029240
Bioinformatics. 2012 Jul 1;28(13):1684-91
pubmed: 22531217
Bioessays. 2013 Feb;35(2):123-30
pubmed: 23281172
Cell Rep. 2015 May 5;11(5):673-80
pubmed: 25921530
Nat Genet. 2001 Feb;27(2):151-2
pubmed: 11175779
Syst Biol. 2006 Apr;55(2):301-13
pubmed: 16611601
Arch Oral Biol. 2004 Apr;49(4):247-57
pubmed: 15003543
Nature. 2019 Jul;571(7766):505-509
pubmed: 31243369
Genome Biol. 2015 Aug 06;16:157
pubmed: 26243257
J Cell Physiol. 2021 Jul;236(7):5387-5398
pubmed: 33377198
Biol Rev Camb Philos Soc. 2011 Aug;86(3):733-58
pubmed: 21418504
BMC Bioinformatics. 2004 May 14;5:59
pubmed: 15144565
Nature. 2002 Dec 5;420(6915):520-62
pubmed: 12466850
Periodontol 2000. 1997 Feb;13:76-90
pubmed: 9567924