The rise and fall of Hox gene clusters

Duboule, Denis

doi:10.1242/dev.001065

Cited by 471 publications

(553 citation statements)

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“…Mammals and birds have 39 and 36 Hox genes, respectively, which are arranged in four clusters in the genome from the 3 0 to the 5 0 end (Duboule, 2007;Richardson et al, 2007). The spatio-temporal expression of the genes is determined by gene position within the cluster, properties known as spatial and temporal colinearity.…”

Section: Introductionmentioning

confidence: 99%

Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation

Barak

Noon

Reshef

2012

Developmental Dynamics

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Background: Hox genes are key players in AP patterning of the vertebrate body plan and are necessary for organogenesis. Several studies provide evidence for the role Hox genes play during kidney development and especially regarding metanephros initiation and formation. However, the role Hox genes play during early stages of kidney development is largely unknown. A recent study in our lab revealed the role Hoxb4 plays in conferring the competence of intermediate mesodermal cells to respond to kidney inductive signals and express early kidney regulators. Results: As a first step in understanding the role Hox genes play in setting the formation of the pronephros morphogenetic field and the expression of early regulators of kidney development, we studied in detail the expression pattern of 10 Hox genes in relation to the 6th somite axial level, the anterior sharp border of the kidney field. Despite the idea of spatial co-linearity as exemplified in the Hox gene expression pattern in late developmental stages, a very dynamic spatio-temporal expression of these genes was found in early stages. Conclusions: Since mesodermal patterning occurs at gastrula stages, the relevance of a ''Hox code'' at early stages is questioned in this study.

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Section: Introductionmentioning

confidence: 99%

Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation

Barak

Noon

Reshef

2012

Developmental Dynamics

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“…Although this genetic system has been used as a paradigm in the study of the evolution of body plans 6 , recent studies have highlighted an unexpected diversity in Hox gene number, genomic organization and expression patterns 7,8 . In tetrapods, these genes are classified into 13 groups of paralogy and are tightly clustered at four loci: HoxA to HoxD.…”

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confidence: 99%

Changes in Hox genes’ structure and function during the evolution of the squamate body plan

Di‐Poï

Montoya‐Burgos

Miller

et al. 2010

Nature

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Hox genes are central to the specification of structures along the anterior-posterior body axis 1,2 , and modifications in their expression have paralleled the emergence of diversity in vertebrate body plans 3,4 . Here we describe the genomic organization of Hox clusters in different reptiles and show that squamates have accumulated unusually large numbers of transposable elements at these loci 5 , reflecting extensive genomic rearrangements of coding and non-coding regulatory regions. Comparative expression analyses between two species showing different axial skeletons, the corn snake and the whiptail lizard, revealed major alterations in Hox13 and Hox10 expression features during snake somitogenesis, in line with the expansion of both caudal and thoracic regions. Variations in both protein sequences and regulatory modalities of posterior Hox genes suggest how this genetic system has dealt with its intrinsic collinear constraint to accompany the substantial morphological radiation observed in this group.In many animal species, Hox genes are clustered, and their expression domains, in both time and space, reflect their respective genomic order 1 . Although this genetic system has been used as a paradigm in the study of the evolution of body plans 6 , recent studies have highlighted an unexpected diversity in Hox gene number, genomic organization and expression patterns 7,8 . In tetrapods, these genes are classified into 13 groups of paralogy and are tightly clustered at four loci: HoxA to HoxD. A clear correspondence between particular Hox groups and defined morphological boundaries along the anteroposterior axis has been documented, either by comparing expression profiles between various vertebrates or by genetic experiments in the mouse 1,3,4,9 .Vertebrate species have highly variable number of vertebrae, ranging from fewer than ten to several hundreds 10-12 , a parameter that is probably dependent on the speed of the segmentation clock relative to axial growth, as proposed for snakes 13 . Within reptiles, squamates (that is, lizards and snakes) have a large realm of morphologies, suggesting that Hox genes were modified, either in their structure or in their regulation. Previous expression analyses in snakes showed an expansion of anterior Hox gene expression along the body axis, in parallel with body plan elongation 9 , and revealed that collinearity was fully respected 14 . However, these studies involved selected genes, in the absence of genomic information. Here we describe how structural and regulatory adaptations in this gene family may have accompanied the transition towards such a body plan and suggest that the unexpected invasion of all Squamata Hox clusters by transposons might have facilitated such adaptations.We characterized the genomic organization of posterior Hox loci in the corn snake (Pantherophis guttatus) and other reptiles, including the turtle, tuatara and several lizards, with a particular focus on repeated elements that are generally excluded from these loci in tetrapods but are abundan...

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“…Paralogues within these clusters are functionally related, playing pivotal roles for the organism, such as oxygen transport (globin genes 2,3 ) and development (Hox genes 4 ). To date, analysis of the varying degree of Hox gene clustering across taxa has been instrumental for understanding the interface between the evolution, function and organization of paralogous gene clusters in animal genomes 5 . Thus, the evolutionary conservation of the ancient clustering of Hox genes in vertebrate lineages is thought to reflect a constraint imposed by the sequential expression of these genes during development, which parallels how they are ordered in the cluster 5,6 .…”

mentioning

confidence: 99%

“…To date, analysis of the varying degree of Hox gene clustering across taxa has been instrumental for understanding the interface between the evolution, function and organization of paralogous gene clusters in animal genomes 5 . Thus, the evolutionary conservation of the ancient clustering of Hox genes in vertebrate lineages is thought to reflect a constraint imposed by the sequential expression of these genes during development, which parallels how they are ordered in the cluster 5,6 . The mechanistic bases underlying this temporal collinearity are not fully understood, but are consistent with a delicate, coordinated regulation of the constituent genes 7,8 .…”

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confidence: 99%

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Remodelling of a homeobox gene cluster by multiple independent gene reunions in Drosophila

et al. 2015

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Genome clustering of homeobox genes is often thought to reflect arrangements of tandem gene duplicates maintained by advantageous coordinated gene regulation. Here we analyse the chromosomal organization of the NK homeobox genes, presumed to be part of a single cluster in the Bilaterian ancestor, across 20 arthropods. We find that the ProtoNK cluster was extensively fragmented in some lineages, showing that NK clustering in Drosophila species does not reflect selectively maintained gene arrangements. More importantly, the arrangement of NK and neighbouring genes across the phylogeny supports that, in two instances within the Drosophila genus, some cluster remnants became reunited via large-scale chromosomal rearrangements. Simulated scenarios of chromosome evolution indicate that these reunion events are unlikely unless the genome neighbourhoods harbouring the participating genes tend to colocalize in the nucleus. Our results underscore how mechanisms other than tandem gene duplication can result in paralogous gene clustering during genome evolution.

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The rise and fall of Hox gene clusters

Cited by 471 publications

References 71 publications

Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation

Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation

Changes in Hox genes’ structure and function during the evolution of the squamate body plan

Remodelling of a homeobox gene cluster by multiple independent gene reunions in Drosophila

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