Coevolutionary patterning of teeth and taste buds

Ryan Fredric Bloomquist, Nicholas F. Parnell, Kristine A. Phillips, Teresa E. Fowler, Tian Y. Yu, Paul T. Sharpe, J. Todd Streelman

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Teeth and taste buds are iteratively patterned structures that line the oro-pharynx of vertebrates. Biologists do not fully understand how teeth and taste buds develop from undifferentiated epithelium or how variation in organ density is regulated. These organs are typically studied independently because of their separate anatomical location inmammals: Teeth on the jawmargin and taste buds on the tongue. However, in many aquatic animals like bony fishes, teeth and taste buds are colocalized one next to the other. Using genetic mapping in cichlid fishes, we identified shared loci controlling a positive correlation between tooth and taste bud densities. Genome intervals contained candidate genes expressed in tooth and taste bud fields. sfrp5 and bmper, notable for roles in Wingless (Wnt) and bone morphogenetic protein (BMP) signaling, were differentially expressed across cichlid species with divergent tooth and taste bud density, and were expressed in the development of both organs in mice. Synexpression analysis and chemical manipulation of Wnt, BMP, and Hedgehog (Hh) pathways suggest that a common cichlid oral lamina is competent to form teeth or taste buds. Wnt signaling couples tooth and taste bud density and BMP and Hh mediate distinct organ identity. Synthesizing data from fish and mouse, we suggest that the Wnt-BMP-Hh regulatory hierarchy that configures teeth and taste buds on mammalian jaws and tongues may be an evolutionary remnant inherited from ancestors wherein these organs were copatterned from common epithelium.

Original languageEnglish (US)
Pages (from-to)E5954-E5962
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number44
DOIs
StatePublished - Nov 3 2015

Fingerprint

Taste Buds
Tooth
Bone Morphogenetic Proteins
Cichlids
Hedgehogs
Tongue
Fishes
Epithelium
Pharynx
Jaw
Vertebrates
Genome

Keywords

  • Bipotency
  • Placode patterning
  • Plasticity
  • Quantitative trait loci
  • Tooth/taste bud development

ASJC Scopus subject areas

  • General

Cite this

Bloomquist, R. F., Parnell, N. F., Phillips, K. A., Fowler, T. E., Yu, T. Y., Sharpe, P. T., & Streelman, J. T. (2015). Coevolutionary patterning of teeth and taste buds. Proceedings of the National Academy of Sciences of the United States of America, 112(44), E5954-E5962. https://doi.org/10.1073/pnas.1514298112

Coevolutionary patterning of teeth and taste buds. / Bloomquist, Ryan Fredric; Parnell, Nicholas F.; Phillips, Kristine A.; Fowler, Teresa E.; Yu, Tian Y.; Sharpe, Paul T.; Streelman, J. Todd.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 44, 03.11.2015, p. E5954-E5962.

Research output: Contribution to journalArticle

Bloomquist, RF, Parnell, NF, Phillips, KA, Fowler, TE, Yu, TY, Sharpe, PT & Streelman, JT 2015, 'Coevolutionary patterning of teeth and taste buds', Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 44, pp. E5954-E5962. https://doi.org/10.1073/pnas.1514298112
Bloomquist, Ryan Fredric ; Parnell, Nicholas F. ; Phillips, Kristine A. ; Fowler, Teresa E. ; Yu, Tian Y. ; Sharpe, Paul T. ; Streelman, J. Todd. / Coevolutionary patterning of teeth and taste buds. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 44. pp. E5954-E5962.
@article{5141d222ce364d608fc35a2c1b555fae,
title = "Coevolutionary patterning of teeth and taste buds",
abstract = "Teeth and taste buds are iteratively patterned structures that line the oro-pharynx of vertebrates. Biologists do not fully understand how teeth and taste buds develop from undifferentiated epithelium or how variation in organ density is regulated. These organs are typically studied independently because of their separate anatomical location inmammals: Teeth on the jawmargin and taste buds on the tongue. However, in many aquatic animals like bony fishes, teeth and taste buds are colocalized one next to the other. Using genetic mapping in cichlid fishes, we identified shared loci controlling a positive correlation between tooth and taste bud densities. Genome intervals contained candidate genes expressed in tooth and taste bud fields. sfrp5 and bmper, notable for roles in Wingless (Wnt) and bone morphogenetic protein (BMP) signaling, were differentially expressed across cichlid species with divergent tooth and taste bud density, and were expressed in the development of both organs in mice. Synexpression analysis and chemical manipulation of Wnt, BMP, and Hedgehog (Hh) pathways suggest that a common cichlid oral lamina is competent to form teeth or taste buds. Wnt signaling couples tooth and taste bud density and BMP and Hh mediate distinct organ identity. Synthesizing data from fish and mouse, we suggest that the Wnt-BMP-Hh regulatory hierarchy that configures teeth and taste buds on mammalian jaws and tongues may be an evolutionary remnant inherited from ancestors wherein these organs were copatterned from common epithelium.",
keywords = "Bipotency, Placode patterning, Plasticity, Quantitative trait loci, Tooth/taste bud development",
author = "Bloomquist, {Ryan Fredric} and Parnell, {Nicholas F.} and Phillips, {Kristine A.} and Fowler, {Teresa E.} and Yu, {Tian Y.} and Sharpe, {Paul T.} and Streelman, {J. Todd}",
year = "2015",
month = "11",
day = "3",
doi = "10.1073/pnas.1514298112",
language = "English (US)",
volume = "112",
pages = "E5954--E5962",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "44",

}

TY - JOUR

T1 - Coevolutionary patterning of teeth and taste buds

AU - Bloomquist, Ryan Fredric

AU - Parnell, Nicholas F.

AU - Phillips, Kristine A.

AU - Fowler, Teresa E.

AU - Yu, Tian Y.

AU - Sharpe, Paul T.

AU - Streelman, J. Todd

PY - 2015/11/3

Y1 - 2015/11/3

N2 - Teeth and taste buds are iteratively patterned structures that line the oro-pharynx of vertebrates. Biologists do not fully understand how teeth and taste buds develop from undifferentiated epithelium or how variation in organ density is regulated. These organs are typically studied independently because of their separate anatomical location inmammals: Teeth on the jawmargin and taste buds on the tongue. However, in many aquatic animals like bony fishes, teeth and taste buds are colocalized one next to the other. Using genetic mapping in cichlid fishes, we identified shared loci controlling a positive correlation between tooth and taste bud densities. Genome intervals contained candidate genes expressed in tooth and taste bud fields. sfrp5 and bmper, notable for roles in Wingless (Wnt) and bone morphogenetic protein (BMP) signaling, were differentially expressed across cichlid species with divergent tooth and taste bud density, and were expressed in the development of both organs in mice. Synexpression analysis and chemical manipulation of Wnt, BMP, and Hedgehog (Hh) pathways suggest that a common cichlid oral lamina is competent to form teeth or taste buds. Wnt signaling couples tooth and taste bud density and BMP and Hh mediate distinct organ identity. Synthesizing data from fish and mouse, we suggest that the Wnt-BMP-Hh regulatory hierarchy that configures teeth and taste buds on mammalian jaws and tongues may be an evolutionary remnant inherited from ancestors wherein these organs were copatterned from common epithelium.

AB - Teeth and taste buds are iteratively patterned structures that line the oro-pharynx of vertebrates. Biologists do not fully understand how teeth and taste buds develop from undifferentiated epithelium or how variation in organ density is regulated. These organs are typically studied independently because of their separate anatomical location inmammals: Teeth on the jawmargin and taste buds on the tongue. However, in many aquatic animals like bony fishes, teeth and taste buds are colocalized one next to the other. Using genetic mapping in cichlid fishes, we identified shared loci controlling a positive correlation between tooth and taste bud densities. Genome intervals contained candidate genes expressed in tooth and taste bud fields. sfrp5 and bmper, notable for roles in Wingless (Wnt) and bone morphogenetic protein (BMP) signaling, were differentially expressed across cichlid species with divergent tooth and taste bud density, and were expressed in the development of both organs in mice. Synexpression analysis and chemical manipulation of Wnt, BMP, and Hedgehog (Hh) pathways suggest that a common cichlid oral lamina is competent to form teeth or taste buds. Wnt signaling couples tooth and taste bud density and BMP and Hh mediate distinct organ identity. Synthesizing data from fish and mouse, we suggest that the Wnt-BMP-Hh regulatory hierarchy that configures teeth and taste buds on mammalian jaws and tongues may be an evolutionary remnant inherited from ancestors wherein these organs were copatterned from common epithelium.

KW - Bipotency

KW - Placode patterning

KW - Plasticity

KW - Quantitative trait loci

KW - Tooth/taste bud development

UR - http://www.scopus.com/inward/record.url?scp=84946616218&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84946616218&partnerID=8YFLogxK

U2 - 10.1073/pnas.1514298112

DO - 10.1073/pnas.1514298112

M3 - Article

C2 - 26483492

AN - SCOPUS:84946616218

VL - 112

SP - E5954-E5962

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 44

ER -