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Wim G M Damen

Publications and source records attributed to Wim G M Damen.

16 recordsLinked to original sources

The ten Hox genes of the millipede Glomeris marginata.

We have isolated the ten Hox genes from the pill millipede Glomeris marginata (Myriapoda:Diplopoda). All ten genes are expressed in characteristic Hox-gene-like expression patterns. The register of Hox gene expression borders is conserved and the expression profiles show that the anterior-most limb-bearing segment in arthropods (antennal/cheliceral segment) does not express any Hox gene, while the next segment (intercalary/second-antennal/premandibular/pedipalpal segment) does express Hox genes. The Hox expression patterns in this millipede thus support the conclusion that all arthropods possess a deuterocerebral segment. We find that there is an apparent posterior shift of Hox gene expression domains dorsally relative to their ventral patterns, indicating that the decoupling of dorsal and ventral segmentation is not restricted to the level of segment polarity genes but apparently includes the Hox genes. Although the mechanism for the decoupling of dorsal and ventral segmentation remains unsolved, the decoupling must be at a level higher in the hierarchy than that of the segment polarity and Hox genes. The expression patterns of Ultrabithorax and abdominal-A suggest a correlation between the function of these genes and the delayed outgrowth of posterior trunk appendages. This delay may be caused by an assumed repressor function of Ultrabithorax, which might partially repress the activation of the Distal-less gene. The Glomeris fushi tarazu gene is expressed in a Hox-like domain and in the developing central nervous system, but not in segmental stripes such as has been reported in another myriapod species, the centipede Lithobius. In contrast to the Lithobius fushi tarazu gene, there is no indication for a role in segment formation for the millipede fushi tarazu gene, suggesting that fushi tarazu first acquired its segmentation function in the lineage of the insects.

Amino Acid Sequence↗

A homolog of the hydrolase Notum is expressed during segmentation and appendage formation in the Central American hunting spider Cupiennius salei.

The hydrolase Notum (also known as Wingful) has been implicated in shaping the distribution gradient of the morphogen Wingless in Drosophila by modifying the Wingless-binding heparan sulfate proteoglycan (HSPG) core glypicans Dally and Dally-like. Here we report on the expression of a Notum homolog during the embryonic development of the spider Cupiennius salei. Notum is expressed in two to three stripes in the posterior region of the germband where new segments are formed. At this location no Wingless expression is present, suggesting that Notum may be involved in the regulation of another HSPG-binding morphogen, possibly Hedgehog. In older segments, however, expression of Notum and Wingless roughly coincides. In the appendages, Notum is expressed in ventral mesodermal cells, directly adjacent to the Wingless expressing ectodermal cells. This could indicate a role for the mesoderm in regulating morphogen gradient formation in the ectoderm.

Animals↗

Suppressor of Hairless and Presenilin phenotypes imply involvement of canonical Notch-signalling in segmentation of the spider Cupiennius salei.

Arthropods, vertebrates, and annelids all have a segmented body. Our recent discovery of involvement of Notch-signalling in spider segmentation revived the discussion on the origin of segmented body plans and suggests the sharing of a common genetic program in a common ancestor. Here, we analysed the spider homologues of the Suppressor of Hairless and Presenilin genes, which encode components of the canonical Notch-pathway, to further explore the role of Notch-signalling in spider segmentation. RNAi silencing of two spider Suppressor of Hairless homologues and the spider Presenilin homologue causes severe segmentation phenotypes. The most prominent defect is the consistent breakdown of segmentation after the formation of three (Suppressor of Hairless) or five (Presenilin) opisthosomal segments. These phenotypes indicate that Notch-signalling during spider segmentation likely involves the canonical pathway via Presenilin and Suppressor of Hairless. Furthermore, it implies that Notch-signalling influences both the formation and patterning of the spider segments: it is required for the specification of the posterior segments and for proper specification of the segment boundaries. We argue that alternative, partly redundant, pathways might act in the formation of the anterior segments that are not active in the posterior segments. This suggests that at least some differences exist in the specification of anterior and posterior segments of the spider, a finding that may be valid for most short germ arthropods. Our data provide additional evidence for the similarities of Notch-signalling in spider segmentation and vertebrate somitogenesis and strengthen our previous notion that the formation of the segments in arthropods and vertebrates might have shared a genetic program in a common ancestor.

Amino Acid Sequence↗

Cell death during germ band inversion, dorsal closure, and nervous system development in the spider Cupiennius salei.

Cell death is an important feature in the development of animals, because it is one possibility for the embryo to control cell number in developing tissues and thereby determine the form of a growing organ. In Drosophila, cell death has been shown to be involved in the shaping of many different organs of the embryo. We have used terminal deoxynucleotidyl transferase-mediated dUTP-digoxygenin nick end labeling (TUNEL) and an antibody against the activated form of caspase-3 to visualize cell death in the spider Cupiennius salei. We find that similar to Drosophila, massive cell death occurs during the development of the nervous system, suggesting that this is an ancestral feature in the arthropods. We also detect cell death during leg development, most probably related to the formation of tarsal sensory organs. No cell death seems to be required for germ band segmentation. Most importantly, we find that cell death has a role in germ band inversion, a morphogenetic event unique to spiders that involves epithelial fission ventrally and tissue fusion dorsally. Our data show that germ band inversion involves cell death to facilitate the ventral splitting of the germ band, as well as the epithelial fusion during dorsal closure.

Animals↗

Arthropod segmentation: why centipedes are odd.

Recent work has revealed a double segmental periodicity of gene expression in the centipede, a potential molecular explanation for the observation that this arthropod always has an odd number of trunk segments. Is this an oddity of centipedes, or might it mean that double segmental pair-rule patterning dates back to the Ur-arthropod?

Animals↗

Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda).

Diplopods (millipedes) are known for their irregular body segmentation. Most importantly, the number of dorsal segmental cuticular plates (tergites) does not match the number of ventral structures (e.g., sternites). Controversial theories exist to explain the origin of this so-called diplosegmentation. We have studied the embryology of a representative diplopod, Glomeris marginata, and have analyzed the segmentation genes engrailed (en), hedgehog (hh), cubitus-interruptus (ci), and wingless (wg). We show that dorsal segments can be distinguished from ventral segments. They differ not only in number and developmental history, but also in gene expression patterns. engrailed, hedgehog, and cubitus-interruptus are expressed in both ventral and dorsal segments, but at different intrasegmental locations, whereas wingless is expressed only in the ventral segments, but not in the dorsal segments. Ventrally, the patterns are similar to what has been described from Drosophila and other arthropods, consistent with a conserved role of these genes in establishing parasegment boundaries. On the dorsal side, however, the gene expression patterns are different and inconsistent with a role in boundary formation between segments, but they suggest that these genes might function to establish the tergite borders. Our data suggest a profound and rather complete decoupling of dorsal and ventral segmentation leading to the dorsoventral discrepancies in the number of segmental elements. Based on gene expression, we propose a model that may resolve the hitherto controversial issue of the correlation between dorsal tergites and ventral leg pairs in basal diplopods (e.g., Glomeris) and is suggestive also for derived, ring-forming diplopods (e.g., Juliformia).

Amino Acid Sequence↗

Expression patterns of leg genes in the mouthparts of the spider Cupiennius salei (Chelicerata: Arachnida).

The leg genes extradenticle, homothorax, dachshund, and Distal-less define three antagonistic developmental domains in the legs, but not in the antenna, of Drosophila. Here we report the expression patterns of these leg genes in the prosomal appendages of the spider Cupiennius salei. The prosoma of the spider bears six pairs of appendages: a pair of cheliceres, a pair of pedipalps, and four pairs of walking legs. Three types of appendages thus can be distinguished in the spider. We show here that in the pedipalp, the leg-like second prosomal appendage, the patterns are very similar to those in the legs themselves, indicating the presence of three antagonistic developmental domains in both appendage types. In contrast, in the chelicera, the fang-like first prosomal appendage, the patterns are different and there is no evidence for antagonistic domains. Together with data from Drosophila this suggests that leg-shaped morphology of arthropod appendages requires an underlying set of antagonistic developmental domains, whereas other morphologies (e.g. antenna, chelicera) may result from the loss of such antagonistic domains.

Animals↗

Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signaling.

Leg development in Drosophila has been studied in much detail. However, Drosophila limbs form in the larva as imaginal discs and not during embryogenesis as in most other arthropods. Here, we analyze appendage genes in the spider Cupiennius salei and the beetle Tribolium castaneum. Differences in decapentaplegic (dpp) expression suggest a different mode of distal morphogen signaling suitable for the specific geometry of growing limb buds. Also, expression of the proximal genes homothorax (hth) and extradenticle (exd) is significantly altered: in the spider, exd is restricted to the proximal leg and hth expression extends distally, while in insects, exd is expressed in the entire leg and hth is restricted to proximal parts. This reversal of spatial specificity demonstrates an evolutionary shift, which is nevertheless compatible with a conserved role of this gene pair as instructor of proximal fate. Different expression dynamics of dachshund and Distal-less point to modifications in the regulation of the leg gap gene system. We comment on the significance of this finding for attempts to homologize leg segments in different arthropod classes. Comparison of the expression profiles of H15 and optomotor-blind to the Drosophila patterns suggests modifications also in the dorsal-ventral patterning system of the legs. Together, our results suggest alterations in many components of the leg developmental system, namely proximal-distal and dorsal-ventral patterning, and leg segmentation. Thus, the leg developmental system exhibits a propensity to evolutionary change, which probably forms the basis for the impressive diversity of arthropod leg morphologies.

Amino Acid Sequence↗

Involvement of Notch and Delta genes in spider segmentation.

It is currently debated whether segmentation in different animal phyla has a common origin and shares a common genetic mechanism. The apparent use of different genetic networks in arthropods and vertebrates has become a strong argument against a common origin of segmentation. Our knowledge of arthropod segmentation is based mainly on the insect Drosophila, in which a hierarchical cascade of transcription factors controls segmentation. The function of some of these genes seems to be conserved among arthropods, including spiders, but not vertebrates. The Notch pathway has a key role in vertebrate segmentation (somitogenesis) but is not involved in Drosophila body segmentation. Here we show that Notch and Delta genes are involved in segmentation of another arthropod, the spider Cupiennius salei. Expression patterns of Notch and Delta, coupled with RNA interference experiments, identify many similarities between spider segmentation and vertebrate somitogenesis. Our data indicate that formation of the segments in arthropods and vertebrates may have shared a genetic programme in a common ancestor and that parts of this programme have been lost in particular descendant lineages.

Animals↗

Diverse adaptations of an ancestral gill: a common evolutionary origin for wings, breathing organs, and spinnerets.

Changing conditions of life impose new requirements on the morphology and physiology of an organism. One of these changes is the evolutionary transition from aquatic to terrestrial life, leading to adaptations in locomotion, breathing, reproduction, and mechanisms for food capture. We have shown previously that insects' wings most likely originated from one of the gills of ancestral aquatic arthropods during their transition to life on land. Here we investigate the fate of these ancestral gills during the evolution of another major arthropod group, the chelicerates. We examine the expression of two developmental genes, pdm/nubbin and apterous, that participate in the specification of insects' wings and are expressed in particular crustacean epipods/gills. In the horseshoe crab, a primitively aquatic chelicerate, pdm/nubbin is specifically expressed in opisthosomal appendages that give rise to respiratory organs called book gills. In spiders (terrestrial chelicerates), pdm/nubbin and apterous are expressed in successive segmental primordia that give rise to book lungs, lateral tubular tracheae, and spinnerets, novel structures that are used by spiders to breathe on land and to spin their webs. Combined with morphological and palaeontological evidence, these observations suggest that fundamentally different new organs (wings, air-breathing organs, and spinnerets) evolved from the same ancestral structure (gills) in parallel instances of terrestrialization.

Adaptation, Physiological↗

fushi tarazu: a Hox gene changes its role.

The Hox genes play a role in anteroposterior axis specification of bilaterian animals that has been conserved for more than 600 million years. However, some of these genes have occasionally changed their roles in evolution. For example, the insect gene fushi tarazu (ftz), although localised in the Hox cluster, no longer acts as a Hox gene, but is involved in segmentation and nervous system development. Recent data of Mouchel-Vielh et al., and Hughes and Kaufman on ftz homologues in a crustacean and a myriapod, respectively, shed new light onto the evolution of this gene.

Animals↗

Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis.

Spiders belong to the chelicerates, which is a basal arthropod group. To shed more light on the evolution of the segmentation process, orthologs of the Drosophila segment polarity genes engrailed, wingless/Wnt and cubitus interruptus have been recovered from the spider Cupiennius salei. The spider has two engrailed genes. The expression of Cs-engrailed-1 is reminiscent of engrailed expression in insects and crustaceans, suggesting that this gene is regulated in a similar way. This is different for the second spider engrailed gene, Cs-engrailed-2, which is expressed at the posterior cap of the embryo from which stripes split off, suggesting a different mode of regulation. Nevertheless, the Cs-engrailed-2 stripes eventually define the same border as the Cs-engrailed-1 stripes. The spider wingless/Wnt genes are expressed in different patterns from their orthologs in insects and crustaceans. The Cs-wingless gene is expressed in iterated stripes just anterior to the engrailed stripes, but is not expressed in the most ventral region of the germ band. However, Cs-Wnt5-1 appears to act in this ventral region. Cs-wingless and Cs-Wnt5-1 together seem to perform the role of insect wingless. Although there are differences, the wingless/Wnt-expressing cells and en-expressing cells seem to define an important boundary that is conserved among arthropods. This boundary may match the parasegmental compartment boundary and is even visible morphologically in the spider embryo. An additional piece of evidence for a parasegmental organization comes from the expression domains of the Hox genes that are confined to the boundaries, as molecularly defined by the engrailed and wingless/Wnt genes. Parasegments, therefore, are presumably important functional units and conserved entities in arthropod development and form an ancestral character of arthropods. The lack of by engrailed and wingless/Wnt-defined boundaries in other segmented phyla does not support a common origin of segmentation.

Amino Acid Sequence↗

Evolution of dorsal-ventral axis formation in arthropod appendages: H15 and optomotor-blind/bifid-type T-box genes in the millipede Glomeris marginata (Myriapoda: Diplopoda).

In Drosophila, the T-box genes optomotor-blind (omb) and H15 have been implicated in specifying the development of the dorso-ventral (DV) axis of the appendages. Results from the spider Cupiennius salei have suggested that this DV patterning system may be at least partially conserved. Here we extend the study of the DV patterning genes omb and H15 to a representative of the Myriapoda in order to add to the existing comparative data set and to gain further insight into the evolution of the DV patterning system in arthropod appendages. The omb gene of the millipede Glomeris marginata is expressed on the dorsal side of all appendages including trunk legs, maxillae, mandibles, and antennae. This is similar to what is known from Drosophila and Cupiennius and suggests that the role of omb in instructing dorsal fates is conserved in arthropods. Interestingly, the lobe-shaped portions of the mouthparts do not express omb, indicating that these are ventral components and thus may be homologous to the endites present in the corresponding appendages in insects. Concerning the H15 gene we were able to identify two paralogous genes in Glomeris. Both genes are expressed in the sensory organs of the maxilla and antenna, but only Gm-H15-1 is expressed along the ventral side of the trunk legs. The expression is more extensive than in Cupiennius, but less so than in Drosophila. In addition, no ventral expression domain is present in the maxilla, mandible, and antenna. Because of this, the role of H15 in the determination of ventral fate remains unclear.

Animals↗

Expression of Pax group III genes suggests a single-segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei.

Pair-rule patterning forms a key step for segmentation in insects. The expression patterns of pair-rule gene orthologs in representatives of other arthropod groups imply that these genes were segmentation genes in the last common ancestor of the various arthropod groups, but almost nothing is known about the underlying mechanism in noninsect arthropods. Here, we cloned and analyzed members of the Pax group III genes from the spider Cupiennius salei. Pax group III genes comprise genes like the Drosophila genes paired, gooseberry, and gooseberry-neuro, as well as the vertebrate Pax 3 and Pax 7 genes. We recovered three Pax group III genes from the spider C. salei, Cs-pairberry-1, Cs-pairberry-2, and Cs-pairberry-3, and show that the combined expression of the three spider genes mimics the patterns in insects, suggesting an ancestral role for Pax group III genes in segmentation, neurogenesis, and appendage formation in arthropods. One of the genes, pairberry-3, is expressed in a segmental periodicity before overt morphological segmentation is visible, suggesting a single segmental periodicity for opisthosomal segment pattering in the spider. Comparisons among arthropods suggest that the underlying mechanisms for pair-rule gene orthologs are more diverged than the ones for the segment-polarity genes. We argue that there may be a correlation between the lower variation in patterns of segment-polarity genes and the phylotypic stage. The segment-polarity genes are required to define the segment borders of the embryo at the germ-band stage, the arthropod phylotypic stage. Pair-rule gene orthologs act more upstream and may display more variation in their action.

Animals↗

Pair rule gene orthologs in spider segmentation.

The activation of pair rule genes is the first indication of the metameric organization of the Drosophila embryo and thus forms a key step in the segmentation process. There are two classes of pair rule genes in Drosophila: the primary pair rule genes that are directly activated by the maternal and gap genes and the secondary pair rule genes that rely on input from the primary pair rule genes. Here we analyze orthologs of Drosophila primary and secondary pair rule orthologs in the spider Cupiennius salei. The expression patterns of the spider pair rule gene orthologs can be subdivided in three groups: even-skipped and runt-1 expression is in stripes that start at the posterior end of the growth zone and their expression ends before the stripes reach the anterior end of the growth zone, while hairy and pairberry-3 stripes also start at the posterior end, but do not cease in the anterior growth zone. Stripes of odd-paired, odd-skipped-related-1, and sloppy paired are only found in the anterior portion of the growth zone. The various genes thus seem to be active during different phases of segment specification. It is notable that the spider orthologs of the Drosophila primary pair rule genes are active more posterior in the growth zone and thus during earlier phases of segment specification than most orthologs of Drosophila secondary pair rule genes, indicating that parts of the hierarchy might be conserved between flies and spiders. The spider ortholog of the Drosophila pair rule gene fushi tarazu is not expressed in the growth zone, but is expressed in a Hox-like fashion. The segmentation function of fushi tarazu thus appears to be a newly acquired role of the gene in the lineage of the mandibulate arthropods.

Amino Acid Sequence↗