Coevolutionary patterning of teeth and taste buds.
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 in mammals: teeth on the jaw margin 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.
School of Biology and Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA 30332; College of Dental Medicine, Georgia Regents University, Augusta, GA 30912; rbloomquist@gru.edu todd.streelman@biology.gatech.edu.
Ryan F
RF
Bloomquist
School of Biology and Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA 30332;
Nicholas F
NF
Parnell
School of Biology and Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA 30332;
Kristine A
KA
Phillips
School of Biology and Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA 30332;
Teresa E
TE
Fowler
Department of Craniofacial Development and Stem Cell Biology, Dental Institute, King's College London, London WC2R 2LS, United Kingdom.
Tian Y
TY
Yu
Department of Craniofacial Development and Stem Cell Biology, Dental Institute, King's College London, London WC2R 2LS, United Kingdom.
Paul T
PT
Sharpe
School of Biology and Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA 30332; rbloomquist@gru.edu todd.streelman@biology.gatech.edu.
J Todd
JT
Streelman
D000818:Animals; D005075:Biological Evolution; D019521:Body Patterning; D023681:Cichlids / Q000196:embryology; D051379:Mice; D008969:Molecular Sequence Data; D040641:Quantitative Trait Loci; D015398:Signal Transduction; D013650:Taste Buds / Q000196:embryology*; D014070:Tooth / Q000196:embryology*
bipotency; placode patterning; plasticity; quantitative trait loci; tooth/taste bud development