Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizard

Denis Duboule
2009
Article

Hox genes control many aspects of embryonic development in metazoans. Previous analyses of this gene family revealed a surprising diversity in terms of gene number and organization between various animal species. In vertebrates, Hox genes are grouped into tightly organized clusters, claimed to be devoid of repetitive sequences. Here, we report the genomic organization of the four Hox loci present in the green anole lizard and show that they have massively accumulated retrotransposons, leading to gene clusters larger in size when compared to other vertebrates. In addition, similar repeats are present in many other development-related gene-containing regions, also thought to be refractory to such repetitive elements. Transposable elements are major sources of genetic variations, including alterations of gene expression, and hence this situation, so far unique among vertebrates, may have been associated with the evolution of the spectacular realm of morphological variations in the body plans of Squamata. Finally, sequence alignments highlight some divergent evolution in highly conserved DNA regions between vertebrate Hox clusters, which may coincide with the emergence of mammalian-specific features.

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Denis Duboule
2009
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https://infoscience.epfl.ch/record/134602?ln=fr

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A typical relaxation of structural constraints in Hox gene clusters of squamates

Denis Duboule

Hox genes control many aspects of embryonic development in metazoans. Previous analyses of this gene family has revealed a surprising diversity in terms of gene number and organization between various animal species. In vertebrates, Hox genes are grouped into tightly organized clusters, originally claimed to be devoid of repetitive sequences. Here, we report the genomic organization of the posterior Hox loci (from Hox13 to Hox10) present in reptiles including the green anole lizard (Anolis carolinensis) and the corn snake (Pantherophis guttatus), and show that squamates have massively accumulated transposable elements, leading to gene clusters larger in size when compared to other vertebrates. In addition, we show the disappearance of highly conserved regulatory sequences within both the HoxA and HoxD clusters, as well as the rapid evolution of Hox coding regions within the squamata lineages. Finally, in parallel with these modifications in the genomic organization of squamata Hox clusters, we observe specific alterations in the expression patterns of posterior Hox genes during corn snake somitogenesis. Because transposable elements are major sources of genetic variations, we speculate that their insertion into Hox gene clusters, not reported so far for other vertebrates, may have associated with the evolution of the spectacular realm of morphological variations in the body plans of squamates.

Elsevier Science BV2009

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The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes

Denis Duboule

This paper reports the cloning of the fourth major murine homeogene complex, HOX-5. The partial characterization of this gene cluster revealed the presence of two novel genes (Hox-5.2, Hox-5.3) located at the 5' extremity of this complex. In situ hybridization experiments showed that these two genes are transcribed in very posterior domains during embryonic and foetal development. We also show that Hox-1.6, the gene located at the 3' most position in the HOX-1 complex, has a very anterior expression boundary during early development. These results clearly support the recently proposed hypothesis that the expression of murine Antp-like homeobox-containing genes along the antero-posterior developing body axis follows a positional hierarchy which reflects their respective physical positions within the HOX clusters, similar to that which is found for the Drosophila homeotic genes. Such a structural and functional organization is likely conserved in most vertebrates. Moreover, on the basis of sequence comparisons, we propose that the ordering of homeobox-containing genes within clusters has been conserved between Drosophila and the house mouse. Thus, very different body plans might be achieved, both in insects and vertebrates, by evolutionarily conserved gene networks possibly displaying similar regulatory interactions.

1989

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Teleost HoxD and HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex

Denis Duboule

In tetrapods, Hox genes are essential for the proper organization and development of axial structures. Experiments involving Hox gene inactivations have revealed their particularly important functions in the establishment of morphological transitions within metameric series such as the vertebral column. Teleost fish show a much simpler range of axial (trunk or appendicular) morphologies, which prompted us to investigate the nature of the Hox system in these lower vertebrates. Here, we show that fish have a family of Hox genes, very similar in both number and general organization, to that of tetrapods. Expression studies, carried out with HoxD and HoxA genes, showed that all vertebrates use the same general scheme, involving the colinear activation of gene expression in both space and time. Comparisons between tetrapods and fish allowed us to propose a model which accounts for the primary function of this gene family. In this model, a few ancestral Hox genes were involved in the determination of polarity in the digestive tract and were further recruited in more elaborate axial structures.

1996

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Expression génétique

L'expression des gènes, encore appelée expression génique ou expression génétique, désigne l'ensemble des processus biochimiques par lesquels l'information héréditaire stockée dans un gène est lue po

Gène Hox

Les gènes Hox sont une catégorie particulière de gènes homéotiques ; ils sont parmi les gènes les plus longuement étudiés de la biologie évolutive. Les gènes homéotiques possèdent une séquence ADN qua

Gène

Un gène, du grec ancien (« génération, naissance, origine »), est, en biologie, une séquence discrète et héritable de nucléotides dont l'expression affecte les caractères d'un organisme. L'ensemble