An ancient gene network is co-opted for teeth on old and new jaws

Gareth J. Fraser, C. Darrin Hulsey, Ryan Fredric Bloomquist, Kristine Uyesugi, Nancy R. Manley, J. Todd Streelman

Research output: Contribution to journalArticle

121 Citations (Scopus)

Abstract

Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.

Original languageEnglish (US)
Pages (from-to)233-247
Number of pages15
JournalPLoS Biology
Volume7
Issue number2
DOIs
StatePublished - Feb 1 2009
Externally publishedYes

Fingerprint

Gene Regulatory Networks
Jaw
jaws
Tooth
teeth
Genes
Ectodysplasins
mouth
Fish
Vertebrates
Dentition
Gene expression
vertebrates
Cichlids
Arches
gene regulatory networks
Homeobox Genes
Pharynx
Lakes
pharynx

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Fraser, G. J., Hulsey, C. D., Bloomquist, R. F., Uyesugi, K., Manley, N. R., & Streelman, J. T. (2009). An ancient gene network is co-opted for teeth on old and new jaws. PLoS Biology, 7(2), 233-247. https://doi.org/10.1371/journal.pbio.1000031

An ancient gene network is co-opted for teeth on old and new jaws. / Fraser, Gareth J.; Hulsey, C. Darrin; Bloomquist, Ryan Fredric; Uyesugi, Kristine; Manley, Nancy R.; Streelman, J. Todd.

In: PLoS Biology, Vol. 7, No. 2, 01.02.2009, p. 233-247.

Research output: Contribution to journalArticle

Fraser, GJ, Hulsey, CD, Bloomquist, RF, Uyesugi, K, Manley, NR & Streelman, JT 2009, 'An ancient gene network is co-opted for teeth on old and new jaws', PLoS Biology, vol. 7, no. 2, pp. 233-247. https://doi.org/10.1371/journal.pbio.1000031
Fraser, Gareth J. ; Hulsey, C. Darrin ; Bloomquist, Ryan Fredric ; Uyesugi, Kristine ; Manley, Nancy R. ; Streelman, J. Todd. / An ancient gene network is co-opted for teeth on old and new jaws. In: PLoS Biology. 2009 ; Vol. 7, No. 2. pp. 233-247.
@article{0e13f3a490ee4df49ccb51e60c30752d,
title = "An ancient gene network is co-opted for teeth on old and new jaws",
abstract = "Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.",
author = "Fraser, {Gareth J.} and Hulsey, {C. Darrin} and Bloomquist, {Ryan Fredric} and Kristine Uyesugi and Manley, {Nancy R.} and Streelman, {J. Todd}",
year = "2009",
month = "2",
day = "1",
doi = "10.1371/journal.pbio.1000031",
language = "English (US)",
volume = "7",
pages = "233--247",
journal = "PLoS Biology",
issn = "1545-7885",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - An ancient gene network is co-opted for teeth on old and new jaws

AU - Fraser, Gareth J.

AU - Hulsey, C. Darrin

AU - Bloomquist, Ryan Fredric

AU - Uyesugi, Kristine

AU - Manley, Nancy R.

AU - Streelman, J. Todd

PY - 2009/2/1

Y1 - 2009/2/1

N2 - Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.

AB - Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.

UR - http://www.scopus.com/inward/record.url?scp=61349091159&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=61349091159&partnerID=8YFLogxK

U2 - 10.1371/journal.pbio.1000031

DO - 10.1371/journal.pbio.1000031

M3 - Article

VL - 7

SP - 233

EP - 247

JO - PLoS Biology

JF - PLoS Biology

SN - 1545-7885

IS - 2

ER -