Low divergence in <i>Dlx</i> gene expression between dentitions of the medaka (<i>Oryzias latipes</i>) versus high level of expression shuffling in osteichtyans

Debiais-Thibaud, Mélanie; Germon, Isabelle; Laurenti, Patrick; Casañe, Didier; Borday-Birraux, Véronique

doi:10.1111/j.1525-142x.2008.00257.x

Cited by 17 publications

(35 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We show that odontoblasts co-express SPARC , Col1a1 , Col1a2 and Col2a1 in catshark teeth and dermal denticles, and in thornback ray teeth, thereby supporting the consistency of this co-expression in selachians and the serial nature of chondrichthyan odontodes [9–11]. SPARC , Col1a1 and Col1a2 are also co-expressed in X.t.…”

Section: Discussionsupporting

confidence: 56%

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

et al. 2018

View full text Add to dashboard Cite

BackgroundThe molecular bases explaining the diversity of dental tissue mineralization across gnathostomes are still poorly understood. Odontodes, such as teeth and body denticles, are serial structures that develop through deployment of a gene regulatory network shared between all gnathostomes. Dentin, the inner odontode mineralized tissue, is produced by odontoblasts and appears well-conserved through evolution. In contrast, the odontode hypermineralized external layer (enamel or enameloid) produced by ameloblasts of epithelial origin, shows extensive structural variations. As EMP (Enamel Matrix Protein) genes are as yet only found in osteichthyans where they play a major role in the mineralization of teeth and others skeletal organs, our understanding of the molecular mechanisms leading to the mineralized odontode matrices in chondrichthyans remains virtually unknown.ResultsWe undertook a phylogenetic analysis of the SPARC/SPARC-L gene family, from which the EMPs are supposed to have arisen, and examined the expression patterns of its members and of major fibrillar collagens in the spotted catshark Scyliorhinus canicula, the thornback ray Raja clavata, and the clawed frog Xenopus tropicalis. Our phylogenetic analyses reveal that the single chondrichthyan SPARC-L gene is co-orthologous to the osteichthyan SPARC-L1 and SPARC-L2 paralogues. In all three species, odontoblasts co-express SPARC and collagens. In contrast, ameloblasts do not strongly express collagen genes but exhibit strikingly similar SPARC-L and EMP expression patterns at their maturation stage, in the examined chondrichthyan and osteichthyan species, respectively.ConclusionsA well-conserved odontoblastic collagen/SPARC module across gnathostomes further confirms dentin homology. Members of the SPARC-L clade evolved faster than their SPARC paralogues, both in terms of protein sequence and gene duplication. We uncover an osteichthyan-specific duplication that produced SPARC-L1 (subsequently lost in pipidae frogs) and SPARC-L2 (independently lost in teleosts and tetrapods).Our results suggest the ameloblastic expression of the single chondrichthyan SPARC-L gene at the maturation stage reflects the ancestral gnathostome situation, and provide new evidence in favor of the homology of enamel and enameloids in all gnathostomes.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1241-y) contains supplementary material, which is available to authorized users.

show abstract

Section: Discussionsupporting

confidence: 56%

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

et al. 2018

View full text Add to dashboard Cite

show abstract

“…In tetrapods, the Dlx family consist of six genes organized into the Dlx1/2 , Dlx3/4 and Dlx5/6 bigene clusters. In zebrafish, eight dlx genes have been reported among which six ( dlx1a/2a, dlx3b/dlx4b, dlx5a/6a ) are arranged on chromosomes similarly to their tetrapod counterparts [24]–[27]. Expression and functional analyses of Dlx5/6 have demonstrated their key roles in the development of the nervous system, of craniofacial structures, of endochondral bones and of appendages [13], [14], [28]–[38].…”

Section: Introductionmentioning

confidence: 99%

The dlx5a/dlx6a Genes Play Essential Roles in the Early Development of Zebrafish Median Fin and Pectoral Structures

2014

View full text Add to dashboard Cite

The Dlx5 and Dlx6 genes encode homeodomain transcription factors essential for the proper development of limbs in mammalian species. However, the role of their teleost counterparts in fin development has received little attention. Here, we show that dlx5a is an early marker of apical ectodermal cells of the pectoral fin buds and of the median fin fold, but also of cleithrum precursor cells during pectoral girdle development. We propose that early median fin fold establishment results from the medial convergence of dlx5a-expressing cells at the lateral edges of the neural keel. Expression analysis also shows involvement of dlx5a during appendage skeletogenesis. Using morpholino-mediated knock down, we demonstrate that disrupted dlx5a/6a function results in pectoral fin agenesis associated with misexpression of bmp4, fgf8a, and1 and msx genes. In contrast, the median fin fold presents defects in mesenchymal cell migration and actinotrichia formation, whereas the initial specification seems to occur normally. Our results demonstrate that the dlx5a/6a genes are essential for the induction of pectoral fin outgrowth, but are not required during median fin fold specification. The dlx5a/6a knock down also causes a failure of cleithrum formation associated with a drastic loss of runx2b and col10a1 expression. The data indicate distinct requirements for dlx5a/6a during median and pectoral fin development suggesting that initiation of unpaired and paired fin formation are not directed through the same molecular mechanisms. Our results refocus arguments on the mechanistic basis of paired appendage genesis during vertebrate evolution.

show abstract

“…Within the gnathostomes, Dlx genes are found as three tandem bigene clusters in the genome (six coding sequences, Dlx1 to Dlx6 , reviewed in [30]) with additional genes (single or tandem clusters) in teleost genomes due to an ancestral whole genome duplication ( dlx1a and dlx1b to dlx6a and dlx6b [31], [32]). Within the gnathostome sister group (cyclostomes), Dlx genes from the lamprey and hagfish have been identified but could not be strictly designated as members of the gnathostome Dlx1 to Dlx6 orthology groups ( Petromyzon marinus 4 genes [1]; Lampetra japonica , 6 genes [33], Eptatretus burgeri , 6 genes [34]).…”

Section: Introductionmentioning

confidence: 99%

Heterogeneous Conservation of Dlx Paralog Co-Expression in Jawed Vertebrates

et al. 2013

View full text Add to dashboard Cite

BackgroundThe Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark Scyliorhinus canicula to fill in the gap and provide an overview of the evolution of the Dlx family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model.ResultsThe genomic organisation of the catshark Dlx genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark Dlx clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family.Conclusion Dlx gene expression patterns in the catshark show that there has been little neo-functionalization in Dlx genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six Dlx coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.

show abstract

Low divergence in Dlx gene expression between dentitions of the medaka (Oryzias latipes) versus high level of expression shuffling in osteichtyans

Cited by 17 publications

References 41 publications

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

The dlx5a/dlx6a Genes Play Essential Roles in the Early Development of Zebrafish Median Fin and Pectoral Structures

Heterogeneous Conservation of Dlx Paralog Co-Expression in Jawed Vertebrates

Contact Info

Product

Resources

About