scholarly journals The unusual gene order in the Echinoderm Hox cluster is related to the embryo and larva symmetries

2015 ◽  
Author(s):  
Spyros Papageorgiou

Background: Hox gene collinearity relates the sequential location of Hox genes in the 3´ to 5´ direction on the chromosome with the linear arrangement of the body elements along the anterior-posterior (A/P) axis of bilaterian embryos. This spatial Hox gene collinearity has been almost universally respected in diverse organisms like worms, insects or vertebrates. It is therefore surprising that the above well established collinearity rule is violated in the case of Echinoderms. No explanation of this violation is apparent. Here a hypothesis is put forward which provides a cue to understand the abnormal serial gene location in the sea urchin disorganized Hox cluster. Results: Bilateral symmetry along the A/P embryo axis is established at the very early stages of ontogeny of the sea urchin. For the subsequent developmental stages, rotational symmetry emerges in the vestibula larva. In analogy to the linear A/P case, the circular topology of modules might be a reflection of the architectural restructuring of the Hox loci where the 3´ and 5´ ends of the Hox cluster approach each other so that a closed contour of the chromatin fiber is formed. At a later stage, the break and opening of the cluster contour at the level of Hox4 combined with the rotational symmetry leads to the observed Hox gene sequence that violates the standard 3´ to 5´ collinearity. Conclusion: The unusual gene series manifests the congruence of Hox gene sequence in the cluster with the circular arrangement of the sea urchin primary podia. Accordingly, the Hox sequence after the break at Hox4 is not a violation but an extension of Hox gene collinearity to animals with rotational symmetry.

2018 ◽  
Vol 62 (11-12) ◽  
pp. 673-683 ◽  
Author(s):  
Stephen J. Gaunt

The discovery of Hox gene clusters, first in Drosophila (a protostome) and then as homologues in vertebrates (deuterostomes), was a major step in our understanding of both developmental and evolutionary biology. Hox genes in both species perform the same overall function: that is, organization of the body along its head-tail axis. The conclusion is that the protostome-deuterostome ancestor, founder of 99% of all described animal species, must already have had this same basic Hox cluster, and that it probably used it in the same way to establish its body plan. A striking feature of Hox genes is the spatial collinearity rule: that order of the genes along the chromosome corresponds with the order of their expression domains along the embryo. For vertebrates, though not Drosophila, there is also the temporal collinearity rule: that order of genes along the chromosome corresponds with timing of Hox expressions in the embryo. Although Hox genes are clearly recognized in pre-bilaterians (Cnidaria), it is only in bilaterians that the characteristic clustered Hox arrangement and function is commonly found. Spatial collinearity in expression is conserved widely throughout Bilateria but temporal collinearity is so far limited to vertebrates, cephalochordates, and some arthropods and annelids. In addition to conserved use of Hox genes to pattern the head-tail axis, some animal groups, particularly lophotrochozoans, have extensively co-opted Hox genes, outside collinearity rules, to regulate development of novel structures. Satisfactory understanding of Hox cluster function requires better understanding of the bilaterian last common ancestor (Urbilateria). Xenacoelomorpha may provide useful living models of the ancestral bilaterian condition.


Development ◽  
1998 ◽  
Vol 125 (3) ◽  
pp. 393-406 ◽  
Author(s):  
V.E. Prince ◽  
C.B. Moens ◽  
C.B. Kimmel ◽  
R.K. Ho

The developing hindbrain is organized into a series of segments termed rhombomeres which represent lineage restricted compartments correlating with domains of gene expression and neuronal differentiation. In this study, we investigate the processes of hindbrain segmentation and the acquisition of segmental identity by analyzing the expression of zebrafish hox genes in the hindbrains of normal fish and fish with a loss-of-function mutation in the segmentation gene valentino (val, the homologue of mouse kreisler; Moens, C. B., Cordes, S. P. Giorgianni, M. W., Barsh, G. S. and Kimmel, C. B. (1998). Development 125, 381–391). We find that zebrafish hox genes generally have similar expression profiles to their murine and avian counterparts, although there are several differences in timing and spatial extent of expression which may underlie some of the functional changes that have occurred along the separate evolutionary lineages of teleosts and tetrapods. Our analysis of hox gene expression in val- embryos confirms that the val gene product is important for subdivision of the presumptive rhombomere 5 and 6 territory into definitive rhombomeres, suggests that the val gene product plays a critical role in regulating hox gene transcription, and indicates that some neural crest cells are inappropriately specified in val- embryos. Our analysis of gene expression at several developmental stages has allowed us to infer differences between primary and secondary defects in the val mutant: we find that extended domains of expression for some hox genes are secondary, late phenomena potentially resulting from inappropriate cell mixing or lack of normal inter-rhombomeric interactions in the caudal hindbrain.


Development ◽  
1991 ◽  
Vol 113 (Supplement_1) ◽  
pp. 187-196 ◽  
Author(s):  
Paul Hunt ◽  
Jenny Whiting ◽  
Ian Muchamore ◽  
Heather Marshall ◽  
Robb Krumlauf

Antennapedia class homeobox genes, which in insects are involved in regional specification of the segmented central regions of the body, have been implicated in a similar role in the vertebrate hindbrain. The development of the hindbrain involves the establishment of compartments which are subsequently made distinct from each other by Hox gene expression, implying that the lineage of neural cells may be an important factor in their development. The hindbrain produces the neural crest that gives rise to the cartilages of the branchial skeleton. Lineage also seems to be important in the neural crest, as experiments have shown that the crest will form cartilages appropriate to its level of origin when grafted to a heterotopic location. We show how the Hox genes could also be involved in patterning the mesenchymal structures of the branchial skeleton. Recently it has been proposed that the rhombomererestricted expression pattern of Hox 2 genes is the result of a tight spatially localised induction from underlying head mesoderm, in which a prepattern of Hox expression is visible. We find no evidence for this model, our data being consistent with the idea that the spatially localised expression pattern is a result of segmentation processes whose final stages are intrinsic to the neural plate. We suggest the following model for patterning in the branchial region. At first a segment-restricted code of Hox gene expression becomes established in the neuroepithelium and adjacent presumptive neural crest. This expression is then maintained in the neural crest during migration, resulting in a Hox code in the cranial ganglia and branchial mesenchyme that reflects the crest's rhombomere of origin. The final stage is the establishment of Hox 2 expression in the surface ectoderm which is brought into contact with neural crest-derived branchial mesenchyme. The Hox code of the branchial ectoderm is established later in development than that of the neural plate and crest, and involves the same combination of genes as the underlying crest. Experimental observations suggest the idea of an instructive interaction between branchial crest and its overlying ectoderm, which would be consistent with our observations. The distribution of clusters of Antennapedia class genes within the animal kingdom suggests that the primitive chordates ancestral to vertebrates had at least one Hox cluster. The origin of the vertebrates is thought to have been intimately linked to the appearance of the neural crest, initially in the branchial region. Our data are consistent with the idea that the branchial region of the head arose in evolution before the more anterior parts, the development of the branchial region employing the Hox genes in a more determinate patterning system. In this scenario, the anterior parts of the head arose subsequently, which may explain the greater importance of interactions in their development, and the fact that Antennapedia class Hox genes are not expressed there.


1995 ◽  
Vol 349 (1329) ◽  
pp. 313-319 ◽  

Homeobox genes encode transcription factors that carry out diverse roles during development. They are widely distributed among eukaryotes, but appear to have undergone an extensive radiation in the earliest metazoa, to generate a range of homeobox subclasses now shared between diverse metazoan phyla. The Hox genes comprise one of these subfamilies, defined as much by conserved chromosomal organization and expression as by sequence characteristics. These Hox genes act as markers of position along the antero—posterior axis of the body in nematodes, arthropods, chordates, and by implication, most other triploblastic phyla. In the arthropods this role is visualized most clearly in the control of segment identity. Exactly how Hox genes control the structure of segments is not yet understood, but their differential deployment between segments provides a model for the basis of segment diversity. Within the arthropods, distantly related taxonomic groups with very different body plans (insects, crustaceans) may share the same set of Hox genes. The expression of these Hox genes provides a new character to define the homology of different body regions. Comparisons of Hox gene deployment between insects and a branchiopod crustacean suggest a novel model for the derivation of the insect body plan.


2018 ◽  
Vol 285 (1888) ◽  
pp. 20181513 ◽  
Author(s):  
Tim Wollesen ◽  
Sonia Victoria Rodríguez Monje ◽  
André Luiz de Oliveira ◽  
Andreas Wanninger

Hox genes are expressed along the anterior–posterior body axis in a colinear fashion in the majority of bilaterians. Contrary to polyplacophorans, a group of aculiferan molluscs with conserved ancestral molluscan features, gastropods and cephalopods deviate from this pattern by expressing Hox genes in distinct morphological structures and not in a staggered fashion. Among conchiferans, scaphopods exhibit many similarities with gastropods, cephalopods and bivalves, however, the molecular developmental underpinnings of these similar traits remain unknown. We investigated Hox gene expression in developmental stages of the scaphopod Antalis entalis to elucidate whether these genes are involved in patterning morphological traits shared by their kin conchiferans. Scaphopod Hox genes are predominantly expressed in the foot and mantle but also in the central nervous system. Surprisingly, the scaphopod mid-stage trochophore exhibits a near-to staggered expression of all nine Hox genes identified. Temporal colinearity was not found and early-stage and late-stage trochophores, as well as postmetamorphic individuals, do not show any apparent traces of staggered expression. In these stages, Hox genes are expressed in distinct morphological structures such as the cerebral and pedal ganglia and in the shell field of early-stage trochophores. Interestingly, a re-evaluation of previously published data on early-stage cephalopod embryos and of the gastropod pre-torsional veliger shows that these developmental stages exhibit traces of staggered Hox expression. Considering our results and all gene expression and genomic data available for molluscs as well as other bilaterians, we suggest a last common molluscan ancestor with colinear Hox expression in predominantly ectodermal tissues along the anterior–posterior axis. Subsequently, certain Hox genes have been co-opted into the patterning process of distinct structures (apical organ or prototroch) in conchiferans.


Development ◽  
2000 ◽  
Vol 127 (21) ◽  
pp. 4631-4643 ◽  
Author(s):  
C. Arenas-Mena ◽  
A.R. Cameron ◽  
E.H. Davidson

The Hox cluster of the sea urchin Strongylocentrous purpuratus contains ten genes in a 500 kb span of the genome. Only two of these genes are expressed during embryogenesis, while all of eight genes tested are expressed during development of the adult body plan in the larval stage. We report the spatial expression during larval development of the five ‘posterior’ genes of the cluster: SpHox7, SpHox8, SpHox9/10, SpHox11/13a and SpHox11/13b. The five genes exhibit a dynamic, largely mesodermal program of expression. Only SpHox7 displays extensive expression within the pentameral rudiment itself. A spatially sequential and colinear arrangement of expression domains is found in the somatocoels, the paired posterior mesodermal structures that will become the adult perivisceral coeloms. No such sequential expression pattern is observed in endodermal, epidermal or neural tissues of either the larva or the presumptive juvenile sea urchin. The spatial expression patterns of the Hox genes illuminate the evolutionary process by which the pentameral echinoderm body plan emerged from a bilateral ancestor.


Development ◽  
2000 ◽  
Vol 127 (11) ◽  
pp. 2239-2249 ◽  
Author(s):  
A. Abzhanov ◽  
T.C. Kaufman

Representatives of the Insecta and the Malacostraca (higher crustaceans) have highly derived body plans subdivided into several tagma, groups of segments united by a common function and/or morphology. The tagmatization of segments in the trunk, the part of the body between head and telson, in both lineages is thought to have evolved independently from ancestors with a distinct head but a homonomous, undifferentiated trunk. In the branchiopod crustacean, Artemia franciscana, the trunk Hox genes are expressed in broad overlapping domains suggesting a conserved ancestral state (Averof, M. and Akam, M. (1995) Nature 376, 420–423). In comparison, in insects, the Antennapedia-class genes of the homeotic clusters are more regionally deployed into distinct domains where they serve to control the morphology of the different trunk segments. Thus an originally Artemia-like pattern of homeotic gene expression has apparently been modified in the insect lineage associated with and perhaps facilitating the observed pattern of tagmatization. Since insects are the only arthropods with a derived trunk tagmosis tested to date, we examined the expression patterns of the Hox genes Antp, Ubx and abd-A in the malacostracan crustacean Porcellio scaber (Oniscidae, Isopoda). We found that, unlike the pattern seen in Artemia, these genes are expressed in well-defined discrete domains coinciding with tagmatic boundaries which are distinct from those of the insects. Our observations suggest that, during the independent tagmatization in insects and malacostracan crustaceans, the homologous ‘trunk’ genes evolved to perform different developmental functions. We also propose that, in each lineage, the changes in Hox gene expression pattern may have been important in trunk tagmatization.


Development ◽  
1996 ◽  
Vol 122 (5) ◽  
pp. 1651-1661 ◽  
Author(s):  
S.J. Salser ◽  
C. Kenyon

Hox genes establish body pattern throughout the animal kingdom, but the role these genes play at the cellular level to modify and shape parts of the body remains a mystery. We find that the C. elegans Antennapedia homolog, mab-5, sequentially programs many independent events within individual cell lineages. In one body region, mab-5 first switches ON in a lineage to stimulate proliferation, then OFF to specify epidermal structures, then ON in just one branch of the lineage to promote neuroblast formation, and finally OFF to permit proper sense organ morphology. In a neighboring lineage, continuous mab-5 expression leads to a different pattern of development. Thus, this Hox gene achieves much of its power to diversify the anteroposterior axis through fine spatiotemporal differences in expression coupled with a changing pattern of cellular response.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Masahiro Oka ◽  
Sonoko Mura ◽  
Mayumi Otani ◽  
Yoichi Miyamoto ◽  
Jumpei Nogami ◽  
...  

We previously demonstrated that CRM1, a major nuclear export factor, accumulates at Hox cluster regions to recruit nucleoporin-fusion protein Nup98HoxA9, resulting in robust activation of Hox genes (Oka et al., 2016). However, whether this phenomenon is general to other leukemogenic proteins remains unknown. Here, we show that two other leukemogenic proteins, nucleoporin-fusion SET-Nup214 and the NPM1 mutant, NPM1c, which contains a nuclear export signal (NES) at its C-terminus and is one of the most frequent mutations in acute myeloid leukemia, are recruited to the HOX cluster region via chromatin-bound CRM1, leading to HOX gene activation in human leukemia cells. Furthermore, we demonstrate that this mechanism is highly sensitive to a CRM1 inhibitor in leukemia cell line. Together, these findings indicate that CRM1 acts as a key molecule that connects leukemogenic proteins to aberrant HOX gene regulation either via nucleoporin-CRM1 interaction (for SET-Nup214) or NES-CRM1 interaction (for NPM1c).


Author(s):  
James C.-G. Hombría ◽  
Mar García-Ferrés ◽  
Carlos Sánchez-Higueras

During evolution, bilateral animals have experienced a progressive process of cephalization with the anterior concentration of nervous tissue, sensory organs and the appearance of dedicated feeding structures surrounding the mouth. Cephalization has been achieved by the specialization of the unsegmented anterior end of the body (the acron) and the sequential recruitment to the head of adjacent anterior segments. Here we review the key developmental contribution of Hox1–5 genes to the formation of cephalic structures in vertebrates and arthropods and discuss how this evolved. The appearance of Hox cephalic genes preceded the evolution of a highly specialized head in both groups, indicating that Hox gene involvement in the control of cephalic structures was acquired independently during the evolution of vertebrates and invertebrates to regulate the genes required for head innovation.


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