Evolution of Hox Gene Clusters

Ferrier, David E. K.

doi:10.1007/978-0-387-68990-6_4

Cited by 73 publications

(135 citation statements)

References 84 publications

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“…Conversely, C. teleta, which apparently has a split cluster, does exhibit these features (43). In general, these observations suggest that the presence of collinearity-in particular, temporal collinearity-may be associated with the retention of a more or less intact spiralian Hox cluster, as seems to be the case for the vertebrate cluster (14,23,55,56). Nonetheless, more studies combining genomic and expression information, and including the vast spiralian morphological diversity, are essential to draw robust conclusions about Hox gene evolution and regulation in Spiralia and Metazoa (57).…”

Section: Significancementioning

confidence: 79%

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Schiemann

Martín-Durán

Børve

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Temporal collinearity is often considered the main force preserving Hox gene clusters in animal genomes. Studies that combine genomic and gene expression data are scarce, however, particularly in invertebrates like the Lophotrochozoa. As a result, the temporal collinearity hypothesis is currently built on poorly supported foundations. Here we characterize the complement, cluster, and expression of Hox genes in two brachiopod species, Terebratalia transversa and Novocrania anomala. T. transversa has a split cluster with 10 genes (lab, pb, Hox3, Dfd, Scr, Lox5, Antp, Lox4, Post2, and Post1), whereas N. anomala has 9 genes (apparently missing Post1). Our in situ hybridization, real-time quantitative PCR, and stage-specific transcriptomic analyses show that brachiopod Hox genes are neither strictly temporally nor spatially collinear; only pb (in T. transversa), Hox3 (in both brachiopods), and Dfd (in both brachiopods) show staggered mesodermal expression. Thus, our findings support the idea that temporal collinearity might contribute to keeping Hox genes clustered. Remarkably, expression of the Hox genes in both brachiopod species demonstrates cooption of Hox genes in the chaetae and shell fields, two major lophotrochozoan morphological novelties. The shared and specific expression of Hox genes, together with Arx, Zic, and Notch pathway components in chaetae and shell fields in brachiopods, mollusks, and annelids provide molecular evidence supporting the conservation of the molecular basis for these lophotrochozoan hallmarks.chaetae | shell fields | Lophotrochozoa | Wiwaxia | Hox cluster

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Section: Significancementioning

confidence: 79%

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Schiemann

Martín-Durán

Børve

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Hence, the model predicts a ProtoHox complex with four genes (Figure 2a): An Anterior ProtoHox gene, ancestor of an Anterior Hox gene (PG1/2) and an Anterior ParaHox (Gsh) gene, a Group 3 ProtoHox gene (ancestor of Hox PG3 and Xlox), a Central ProtoHox gene, (ancestor of a Central Hox gene (PG4/8), a central ParaHox was lost soon after ProtoHox cluster duplication), and a Posterior ProtoHox gene (ancestor of a Posterior Hox gene PG9/13 and Cdx). New discoveries on the ParaHox cluster (eg Finnerty and Martindale, 1999;Yanze et al, 2001;Ferrier and Holland, 2003;Cook et al, 2004) and reviews on Hox/ParaHox evolution (eg Ferrier and Holland, 2001;Martínez and Amemiya, 2002;Ferrier and Minguilló n, 2003) always present an evolutionary framework with a ProtoHox cluster with four genes. Here, I propose an alternative scenario for the structure of the ProtoHox cluster and the primordial Hox and ParaHox clusters, which takes into account a reconsideration of the available data and recent discoveries on lower metazoans.…”

Section: Introductionmentioning

confidence: 99%

Hox, ParaHox, ProtoHox: facts and guesses

Garcia‐Fernàndez

2004

Heredity

122

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The Hox gene cluster has captivated the imagination of evolutionary and developmental biologists worldwide. In this review, the origin of the Hox and ParaHox gene clusters by duplication of a ProtoHox gene cluster, and the changes in their gene numbers in major Metazoan Transitions are reviewed critically. Re-evaluation of existing data and recent findings in Cnidarians, Acoels, and critical stages of vertebrate evolution suggest alternative scenarios for the origin, structure, and changes in Hox gene numbers in relevant events of Metazoan evolution. I discuss opposing views and propose that (i) the ProtoHox cluster had only two genes, and not four as commonly believed: a corollary is that the origin of Bilaterians was coincident with the invention of new Hox and ParaHox gene classes, which may have facilitated such a transition; (ii) the ProtoHox cluster duplication was a cis duplication event, rather than a trans duplication event, as previously suggested, and (iii) the ancestral vertebrate cluster possessed 14 Hox genes, and not the 13 generally assumed. These hypotheses could be verified or refuted in the near future, but they may help critical discussion of the evolution of the Hox/ParaHox family in the metazoan kingdom. Heredity (2005) 94, 145-152.

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“…Within the ANTP class Hox genes have attracted particular attention because they show a remarkable similarity across Bilateria not only in sequence identity but also in genomic organization and function (Ferrier and Minguillon, 2003;Garcia-Fernandez, 2005a,b). Bilaterian Hox genes pattern the anterior-posterior axis during development and their defining characteristic is that they are organized in clusters in which genomic organization reflects directly domains of expression along the anterior-posterior body axis: genes at one end of the cluster pattern the anterior end of the embryo, genes at the opposite end pattern the posterior end.…”

mentioning

confidence: 99%

Ancient linkage of a POU class 6 and an anterior hox‐like gene in cnidaria: implications for the evolution of homeobox genes

Kamm¹,

Schierwater²

2007

J Exp Zool Pt B

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Linkage analyses in metazoan genomes suggest two ancestral arrays for the majority of homeobox genes. The related homeobox genes and chromosomal regions that are dispersed in extant species derived possibly from only two single common ancestor regions. One proposed ancestral array, designated as ANTP mega-array, contains most of the ANTP class homeobox genes; the second, named the contraHox super-paralogon, would consist of the classes PRD, POU, LIM, CUT, prospero, TALE and SIX. Here, we report the tight linkage of a POU class 6 gene to an anterior Hoxlike gene in the hydrozoan Eleutheria dichotoma and discuss its possible significance for the evolution of homeobox genes. POU class 6 genes also seem to be ancestrally linked to the HoxC and A clusters in vertebrates, despite POU homeobox genes belonging to the contraHox paralogon. Hence, the much tighter linkage of a POU class 6 gene to an anterior Hox-like gene in a cnidarian is possibly the evolutionary echo of an ancestral genomic region from which most metazoan homeobox classes emerged.

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Evolution of Hox Gene Clusters

Cited by 73 publications

References 84 publications

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Hox, ParaHox, ProtoHox: facts and guesses

Ancient linkage of a POU class 6 and an anterior hox‐like gene in cnidaria: implications for the evolution of homeobox genes

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