An ancient gene network is co-opted for teeth on old and new jaws.
An ancient gene network is co-opted for teeth on old and new jaws.
复制标题
DOI:
10.1371/journal.pbio.1000031
复制
发表时间:
2009-02-10
期刊:
影响因子:
9.8
通讯作者:
Streelman JT
中科院分区:
文献类型:
--
作者:
Fraser GJ;Hulsey CD;Bloomquist RF;Uyesugi K;Manley NR;Streelman JT
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. During evolution, teeth originated deep in the pharynx of ancient and extinct jawless fishes. Later, with the evolution of bony fish, teeth appeared in the mouth, as in most current vertebrates, although some living fishes retain teeth in the posterior pharynx. We integrate comparative morphology, paleontology, and molecular biology to infer the genetic control of the first dentition. We identify Hox genes as important components of an ancient dental gene-regulatory circuit and pinpoint subsequent modifications to this gene network that accompanied the evolution of toothed oral jaws. Furthermore, we highlight a set of genes conserved in the construction of all teeth, regardless of location and lineage. This core dental gene network is evolutionarily essential: nature appears never to have made a dentition without it. A common gene regulatory circuit controls the development of all dentitions, from the original teeth in the throats of jawless fishes half a billion years ago, to the incisors and molars of modern vertebrates.
登录
查看更多内容
影响因子:
64.8
作者:
Cohn, MJ
通讯作者:
Cohn, MJ
影响因子:
7
作者:
Drögemüller, C;Distl, O;Leeb, T
通讯作者:
Leeb, T
影响因子:
2.9
作者:
Borday-Birraux, V;Van der Heyden, C;Sire, JY
通讯作者:
Sire, JY
DOI:
10.1002/jez.b.21182
发表时间:
2008-06-15
影响因子:
2.2
作者:
Graham, Anthony
通讯作者:
Graham, Anthony
DOI:
10.1002/jez.b.21183
发表时间:
2007-12-15
影响因子:
2.2
作者:
Debiais-Thibaud, Melanie;Borday-Birraux, Veronique;Laurenti, Patrick
通讯作者:
Laurenti, Patrick