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Michael Akam - One of the best experts on this subject based on the ideXlab platform.
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odd paired controls frequency doubling in drosophila segmentation by altering the pair rule Gene regulatory network
eLife, 2016Co-Authors: Erik Clark, Michael AkamAbstract:The Drosophila embryo transiently exhibits a double-segment periodicity, defined by the expression of seven 'Pair-Rule' Genes, each in a pattern of seven stripes. At gastrulation, interactions between the Pair-Rule Genes lead to frequency doubling and the patterning of 14 parasegment boundaries. In contrast to earlier stages of Drosophila anteroposterior patterning, this transition is not well understood. By carefully analysing the spatiotemporal dynamics of Pair-Rule Gene expression, we demonstrate that frequency-doubling is precipitated by multiple coordinated changes to the network of regulatory interactions between the Pair-Rule Genes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa/Zic), as the cause of these changes, and show that the patterning of the even-numbered parasegment boundaries relies on Opa-dependent regulatory interactions. Our findings indicate that the Pair-Rule Gene regulatory network has a temporally modulated topology, permitting the Pair-Rule Genes to play stage-specific patterning roles.
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odd paired controls frequency doubling in drosophila segmentation by altering the pair rule Gene regulatory network
eLife, 2016Co-Authors: Erik Clark, Michael AkamAbstract:The basic body plan of an animal is set up in the early embryo, where key developmental Genes are expressed in specific patterns across the organism. These patterns emerge from the way in which the proteins encoded by these Genes act to regulate each other’s expression. The fruit fly Drosophila is often used as a simple model for studying how regulatory interactions between Genes lead to the formation of complex developmental patterns. One example is segmentation, the process by which the trunk (main body) region of the Drosophila embryo is subdivided into 14 segments. A group of transcription factor proteins that are encoded by the so-called “Pair-Rule” Genes play a crucial role in producing the final pattern. Early in development, the Pair-Rule Genes are expressed in patterns of seven stripes, dividing the embryo into double segment units. As the embryo develops, these patterns change to form more precise patterns of 14 stripes, corresponding to single segments. Although many of the regulatory interactions between the Pair-Rule Genes were known, how the system works as a whole to produce this change in expression patterns was not well understood. Clark and Akam have now examined how the patterns of Pair-Rule Gene expression change over time inside fly embryos. This revealed that a “rewiring” of the network of Pair-Rule Genes occurs at the end of the seven stripe stage to produce fourteen stripes. Further investigation revealed that a transcription factor encoded by the Gene odd-paired causes this rewiring, and that the timing of the expression of the Odd-paired protein determines when the rewiring happens. Further studies could now investigate whether Odd-paired’s role as a timer extends to species where segments emerge sequentially, instead of the simultaneous formation of segments seen in Drosophila. Future challenges will be to find out how Odd-paired interacts with other Pair-Rule transcription factors, and whether there are other timing factors that help to coordinate embryonic patterning.
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odd paired controls frequency doubling in drosophila segmentation by altering the pair rule Gene regulatory network
bioRxiv, 2016Co-Authors: Erik Clark, Michael AkamAbstract:Drosophila segmentation is mediated by a group of periodically expressed transcription factors known as the Pair-Rule Genes. These Genes are expressed dynamically, with many transitioning from double segment periodicity to single segment periodicity at gastrulation. The myriad cross-regulatory interactions responsible for these expression changes have been studied for over 30 years, however a systems level understanding of Pair-Rule patterning is still lacking. We carefully analysed the spatiotemporal dynamics of Pair-Rule Gene expression, and found that frequency-doubling is precipitated by multiple coordinated regulatory changes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa), as the cause of these changes, and propose a new model for the patterning of the even-numbered parasegment boundaries, which relies on Opa-dependent regulatory interactions. Our findings indicate that the Pair-Rule Gene regulatory network has temporally-modulated topology and dynamics, permitting stage-specific patterning roles.
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evolution of the pair rule Gene network insights from a centipede
Developmental Biology, 2013Co-Authors: Jack E Green, Michael AkamAbstract:Comparative studies have examined the expression and function of homologues of the Drosophila melanogaster pair rule and segment polarity Genes in a range of arthropods. The segment polarity Gene homologues have a conserved role in the specification of the parasegment boundary, but the degree of conservation of the upstream patterning Genes has proved more variable. Using genomic resources we identify a complete set of pair rule Gene homologues from the centipede Strigamia maritima, and document a detailed time series of expression during trunk segmentation. We find supportive evidence for a conserved hierarchical organisation of the pair rule Genes, with a division into early- and late-activated Genes which parallels the functional division into primary and secondary pair rule Genes described in insects. We confirm that the relative expression of sloppy-paired and paired with respect to wingless and engrailed at the parasegment boundary is conserved between myriapods and insects; suggesting that functional interactions between these Genes might be an ancient feature of arthropod segment patterning. However, we find that the relative expression of a number of the primary pair rule Genes is divergent between myriapods and insects. This corroborates suggestions that the evolution of upper tiers in the segmentation Gene network is more flexible. Finally, we find that the expression of the Strigamia pair rule Genes in periodic patterns is restricted to the ectoderm. This suggests that any direct role of these Genes in segmentation is restricted to this germ layer, and that mesoderm segmentation is either dependent on the ectoderm, or occurs through an independent mechanism.
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the segmentation cascade in the centipede strigamia maritima involvement of the notch pathway and pair rule Gene homologues
Developmental Biology, 2008Co-Authors: Ariel D Chipman, Michael AkamAbstract:The centipede Strigamia maritima forms all of its segments during embryoGenesis. Trunk segments form sequentially from an apparently undifferentiated disk of cells at the posterior of the germ band. We have previously described periodic patterns of Gene expression in this posterior disc that precede overt differentiation of segments, and suggested that a segmentation oscillator may be operating in the posterior disc. We now show that Genes of the Notch signalling pathway, including the ligand Delta, and homologues of the Drosophila Pair-Rule Genes even-skipped and hairy, show periodic expression in the posterior disc, consistent with their involvement in, or regulation by, such an oscillator. These Genes are expressed in a pattern of apparently expanding concentric rings around the proctodeum, which become stripes at the base of the germ band where segments are emerging. In this transition zone, these primary stripes define a double segment periodicity: segmental stripes of engrailed expression, which mark the posterior of each segment, arise at two different phases of the primary pattern. Delta and even-skipped are also activated in secondary stripes that intercalate between primary stripes in this region, further defining the single segment repeat. These data, together with observations that Notch mediated signalling is required for segment pattern formation in other arthropods, suggest that the ancestral arthropod segmentation cascade may have involved a segmentation oscillator that utilised Notch signalling.
Graham E Budd - One of the best experts on this subject based on the ideXlab platform.
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Gene expression analysis reveals that delta notch signalling is not involved in onychophoran segmentation
Development Genes and Evolution, 2016Co-Authors: Ralf Janssen, Graham E BuddAbstract:Delta/Notch (Dl/N) signalling is involved in the Gene regulatory network underlying the segmentation process in vertebrates and possibly also in annelids and arthropods, leading to the hypothesis that segmentation may have evolved in the last common ancestor of bilaterian animals. Because of seemingly contradicting results within the well-studied arthropods, however, the role and origin of Dl/N signalling in segmentation Generally is still unclear. In this study, we investigate core components of Dl/N signalling by means of Gene expression analysis in the onychophoran Euperipatoides kanangrensis, a close relative to the arthropods. We find that neither Delta or Notch nor any other investigated components of its signalling pathway are likely to be involved in segment addition in onychophorans. We instead suggest that Dl/N signalling may be involved in posterior elongation, another conserved function of these Genes. We suggest further that the posterior elongation network, rather than classic Dl/N signalling, may be in the control of the highly conserved segment polarity Gene network and the lower-level Pair-Rule Gene network in onychophorans. Consequently, we believe that the Pair-Rule Gene network and its interaction with Dl/N signalling may have evolved within the arthropod lineage and that Dl/N signalling has thus likely been recruited independently for segment addition in different phyla.
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Gene expression analysis reveals that Delta/Notch signalling is not involved in onychophoran segmentation
Development Genes and Evolution, 2016Co-Authors: Ralf Janssen, Graham E BuddAbstract:Delta/Notch (Dl/N) signalling is involved in the Gene regulatory network underlying the segmentation process in vertebrates and possibly also in annelids and arthropods, leading to the hypothesis that segmentation may have evolved in the last common ancestor of bilaterian animals. Because of seemingly contradicting results within the well-studied arthropods, however, the role and origin of Dl/N signalling in segmentation Generally is still unclear. In this study, we investigate core components of Dl/N signalling by means of Gene expression analysis in the onychophoran Euperipatoides kanangrensis , a close relative to the arthropods. We find that neither Delta or Notch nor any other investigated components of its signalling pathway are likely to be involved in segment addition in onychophorans. We instead suggest that Dl/N signalling may be involved in posterior elongation, another conserved function of these Genes. We suggest further that the posterior elongation network, rather than classic Dl/N signalling, may be in the control of the highly conserved segment polarity Gene network and the lower-level Pair-Rule Gene network in onychophorans. Consequently, we believe that the Pair-Rule Gene network and its interaction with Dl/N signalling may have evolved within the arthropod lineage and that Dl/N signalling has thus likely been recruited independently for segment addition in different phyla.
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deciphering the onychophoran segmentation Gene cascade Gene expression reveals limited involvement of pair rule Gene orthologs in segmentation but a highly conserved segment polarity Gene network
Developmental Biology, 2013Co-Authors: Ralf Janssen, Graham E BuddAbstract:The hallmark of the arthropods is their segmented body, although origin of segmentation, however, is unresolved. In order to shed light on the origin of segmentation we investigated orthologs of pair rule Genes (PRGs) and segment polarity Genes (SPGs) in a member of the closest related sister-group to the arthropods, the onychophorans. Our Gene expression data analysis suggests that most of the onychophoran PRGs do not play a role in segmentation. One possible exception is the even-skipped (eve) Gene that is expressed in the posterior end of the onychophoran where new segments are likely patterned, and is also expressed in segmentation-Gene typical transverse stripes in at least a number of newly formed segments. Other onychophoran PRGs such as runt (run), hairy/Hes (h/Hes) and odd-skipped (odd) do not appear to have a function in segmentation at all. Onychophoran PRGs that act low in the segmentation Gene cascade in insects, however, are potentially involved in segment-patterning. Most obvious is that from the expression of the pairberry (pby) Gene ortholog that is expressed in a typical SPG-pattern. Since this result suggested possible conservation of the SPG-network we further investigated SPGs (and associated factors) such as Notum in the onychophoran. We find that the expression patterns of SPGs in arthropods and the onychophoran are highly conserved, suggesting a conserved SPG-network in these two clades, and indeed also in an annelid. This may suggest that the common ancestor of lophotrochozoans and ecdysozoans was already segmented utilising the same SPG-network, or that the SPG-network was recruited independently in annelids and onychophorans/arthropods.
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expression of pair rule Gene orthologs in the blastoderm of a myriapod evidence for pair rule like mechanisms
BMC Developmental Biology, 2012Co-Authors: Ralf Janssen, Wim G.m. Damen, Graham E BuddAbstract:Background A hallmark of Drosophila segmentation is the stepwise subdivision of the body into smaller and smaller units, and finally into the segments. This is achieved by the function of the well-understood segmentation Gene cascade. The first molecular sign of a segmented body appears with the action of the pair rule Genes, which are expressed as transversal stripes in alternating segments. Drosophila development, however, is derived, and in most other arthropods only the anterior body is patterned (almost) simultaneously from a pre-existing field of cells; posterior segments are added sequentially from a posterior segment addition zone. A long-standing question is to what extent segmentation mechanisms known from Drosophila may be conserved in short-germ arthropods. Despite the derived developmental modes, it appears more likely that conserved mechanisms can be found in anterior patterning.
Susan J. Brown - One of the best experts on this subject based on the ideXlab platform.
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A segmentation clock operating in blastoderm and germband stages of Tribolium development
Development (Cambridge England), 2012Co-Authors: Ezzat El-sherif, Michalis Averof, Susan J. BrownAbstract:In Drosophila, all segments form in the blastoderm where morphogen gradients spanning the entire anterior-posterior axis of the embryo provide positional information. However, in the beetle Tribolium castaneum and most other arthropods, a number of anterior segments form in the blastoderm, and the remaining segments form sequentially from a posterior growth zone during germband elongation. Recently, the cyclic nature of the Pair-Rule Gene Tc-odd-skipped was demonstrated in the growth zone of Tribolium, indicating that a vertebrate-like segmentation clock is employed in the germband stage of its development. This suggests that two mechanisms might function in the same organism: a Drosophila-like mechanism in the blastoderm, and a vertebrate-like mechanism in the germband. Here, we show that segmentation at both blastoderm and germband stages of Tribolium is based on a segmentation clock. Specifically, we show that the Tribolium primary Pair-Rule Gene, Tc-even-skipped (Tc-eve), is expressed in waves propagating from the posterior pole and progressively slowing until they freeze into stripes; such dynamics are a hallmark of clock-based segmentation. Phase shifts between Tc-eve transcripts and protein confirm that these waves are due to expression dynamics. Moreover, by tracking cells in live embryos and by analyzing mitotic profiles, we found that neither cell movement nor oriented cell division could explain the observed wave dynamics of Tc-eve. These results pose intriguing evolutionary questions, as Drosophila and Tribolium segment their blastoderms using the same Genes but different mechanisms.
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loss of tc arrow and canonical wnt signaling alters posterior morphology and pair rule Gene expression in the short germ insect tribolium castaneum
Development Genes and Evolution, 2009Co-Authors: Renata Bolognesi, Tamara D Fischer, Susan J. BrownAbstract:Wnt signaling has been implicated in posterior patterning in short-germ insects, including the red flour beetle Tribolium castaneum (Bolognesi et al. Curr Biol 18:1624–1629, 2008b; Angelini and Kaufman Dev Biol 283:409–423, 2005; Miyawaki et al. Mech Dev 121:119–130, 2004). Specifically, depletion of Wnt ligands Tc-Wnt1 and Tc-WntD/8 produces Tribolium embryos lacking abdominal segments. Similar phenotypes are produced by depletion of Tc-porcupine (Tc-porc) or Tc-pangolin (Tc-pan), indicating that the signal is transmitted through the canonical Wnt pathway (Bolognesi et al. Curr Biol 18:1624–1629, 2008b). Here we show that RNAi for the receptor Tc-arrow produced similar truncated phenotypes, providing additional evidence supporting canonical signal transduction. Furthermore, since in Tribolium segments are defined sequentially by a Pair-Rule Gene circuit that, when interrupted, produces truncated phenotypes (Choe et al. Proc Natl Acad Sci U S A 103:6560–6564, 2006), we investigated the relationship between loss of Wnt signaling and this Pair-Rule Gene circuit. After depletion of the receptor Tc-arrow, expression of Tc-Wnt1 was noticeably absent from the growth zone, while Tc-WntD/8 was restricted to a single spot of expression in what remained of the posterior growth zone. The primary Pair-Rule Genes Tc-runt (Tc-run) and Tc-even-skipped (Tc-eve) were expressed normally in the anterior segments, but were reduced to a single spot in the remnants of the posterior growth zone. Thus, expression of Pair-Rule Genes and Tc-WntD/8 are similarly affected by depletion of Wnt signal and disruption of the posterior growth zone.
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Genetic regulation of engrailed and wingless in tribolium segmentation and the evolution of pair rule segmentation
Developmental Biology, 2009Co-Authors: Chong Pyo Choe, Susan J. BrownAbstract:In Drosophila, primary Pair-Rule Genes establish the parasegmental boundaries and indirectly control the periodic expression of the segment polarity Genes engrailed (en) and wingless (wg) via regulation of secondary Pair-Rule Genes. Although orthologs of some Drosophila Pair-Rule Genes are not required for proper segmentation in Tribolium, segmental expression of Tc-en and Tc-wg is conserved. To understand how these segment polarity Genes are regulated, we examined the results of expressing one or two Pair-Rule Genes in the absence of the other known Pair-Rule Genes. Expression of one or both of the secondary Pair-Rule Genes, Tc-sloppy-paired (Tc-slp) and Tc-paired (Tc-prd), activated Tc-wg in the absence of the primary Pair-Rule Genes, Tc-even-skipped (Tc-eve), Tc-runt (Tc-run) and Tc-odd-skipped (Tc-odd). Tc-eve alone failed to activate Tc-wg or Tc-en, but in combination with Tc-run or Tc-prd activated Tc-en. These results, interpreted within the Pair-Rule Gene expression patterns, suggest separate models for the Genetic regulation of the juxtaposed expression of Tc-wg and Tc-en at odd- and even-numbered parasegmental boundaries, respectively. Conserved interactions between eve and prd at the anterior boundary of odd-numbered parasegments may reflect an ancestral segmentation mechanism that functioned in every segment prior to the evolution of Pair-Rule segmentation.
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a pair rule Gene circuit defines segments sequentially in the short germ insect tribolium castaneum
Proceedings of the National Academy of Sciences of the United States of America, 2006Co-Authors: Chong Pyo Choe, Sherry Miller, Susan J. BrownAbstract:In Drosophila, a hierarchy of maternal, gap, Pair-Rule, and segment polarity Gene interactions regulates virtually simultaneous blastoderm segmentation. For the last decade, studies have focused on revealing the extent to which Drosophila segmentation mechanisms are conserved in other arthropods where segments are added sequentially from anterior to posterior in a cellular environment. Despite our increased knowledge of individual segmentation Genes, details of their interactions in non-Drosophilid insects are not well understood. We analyzed the Tribolium orthologs of Drosophila Pair-Rule Genes, which display Pair-Rule expression patterns. Tribolium castaneum paired (Tc-prd) and sloppy-paired (Tc-slp) Genes produced Pair-Rule phenotypes when their transcripts were severely reduced by RNA interference. In contrast, similar analysis of T. castaneum even-skipped (Tc-eve), runt (Tc-run), or odd-skipped (Tc-odd) Genes produced severely truncated, almost completely asegmental phenotypes. Analysis of interactions between Pair-Rule components revealed that Tc-eve, Tc-run, and Tc-odd form a three-Gene circuit to regulate one another as well as their downstream targets, Tc-prd and Tc-slp. The complement of primary Pair-Rule Genes in Tribolium differs from Drosophila in that it includes Tc-odd but not Tc-hairy. This Gene circuit defines segments sequentially in double segment periodicity. Furthermore, this single mechanism functions in the early blastoderm stage and subsequently during germ-band elongation. The periodicity of the Tribolium Pair-Rule Gene interactions reveals components of the Genetic hierarchy that are regulated in a repetitive circuit or clock-like mechanism. This Pair-Rule Gene circuit provides insight into short-germ segmentation in Tribolium that may be more Generally applicable to segmentation in other arthropods.
Wim G.m. Damen - One of the best experts on this subject based on the ideXlab platform.
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the wnt and delta notch signalling pathways interact to direct pair rule Gene expression via caudal during segment addition in the spider parasteatoda tepidariorum
Development, 2016Co-Authors: Anna Schonauer, Wim G.m. Damen, Christian L B Paese, Maarten Hilbrant, Daniel J Leite, Evelyn E Schwager, Natalia Martins Feitosa, Cornelius Eibner, Alistair P McgregorAbstract:In short-germ arthropods, posterior segments are added sequentially from a segment addition zone (SAZ) during embryoGenesis. Studies in spiders such as Parasteatoda tepidariorum have provided insights into the Gene regulatory network (GRN) underlying segment addition, and revealed that Wnt8 is required for dynamic Delta (Dl) expression associated with the formation of new segments. However, it remains unclear how these pathways interact during SAZ formation and segment addition. Here, we show that Delta-Notch signalling is required for Wnt8 expression in posterior SAZ cells, but represses the expression of this Wnt Gene in anterior SAZ cells. We also found that these two signalling pathways are required for the expression of the spider orthologues of even-skipped (eve) and runt-1 (run-1), at least in part via caudal (cad). Moreover, it appears that dynamic expression of eve in this spider does not require a feedback loop with run-1, as is found in the Pair-Rule circuit of the beetle Tribolium Taken together, our results suggest that the development of posterior segments in Parasteatoda is directed by dynamic interactions between Wnt8 and Delta-Notch signalling that are read out by cad, which is necessary but probably not sufficient to regulate the expression of eve and run-1 Our study therefore provides new insights towards better understanding the evolution and developmental regulation of segmentation in other arthropods, including insects.
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expression of pair rule Gene orthologs in the blastoderm of a myriapod evidence for pair rule like mechanisms
BMC Developmental Biology, 2012Co-Authors: Ralf Janssen, Wim G.m. Damen, Graham E BuddAbstract:Background A hallmark of Drosophila segmentation is the stepwise subdivision of the body into smaller and smaller units, and finally into the segments. This is achieved by the function of the well-understood segmentation Gene cascade. The first molecular sign of a segmented body appears with the action of the pair rule Genes, which are expressed as transversal stripes in alternating segments. Drosophila development, however, is derived, and in most other arthropods only the anterior body is patterned (almost) simultaneously from a pre-existing field of cells; posterior segments are added sequentially from a posterior segment addition zone. A long-standing question is to what extent segmentation mechanisms known from Drosophila may be conserved in short-germ arthropods. Despite the derived developmental modes, it appears more likely that conserved mechanisms can be found in anterior patterning.
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Evolutionary conservation and divergence of the segmentation process in arthropods
Developmental dynamics : an official publication of the American Association of Anatomists, 2007Co-Authors: Wim G.m. DamenAbstract:A fundamental characteristic of the arthropod body plan is its organization in metameric units along the anterior-posterior axis. The segmental organization is laid down during early embryoGenesis. Our view on arthropod segmentation is still strongly influenced by the huge amount of data available from the fruit fly Drosophila melanogaster (the Drosophila paradigm). However, the simultaneous formation of the segments in Drosophila is a derived mode of segmentation. Successive terminal addition of segments from a posteriorly localized presegmental zone is the ancestral mode of arthropod segmentation. This review focuses on the evolutionary conservation and divergence of the Genetic mechanisms of segmentation within arthropods. The more downstream levels of the segmentation Gene network (e.g., segment polarity Genes) appear to be more conserved than the more upstream levels (gap Genes, Notch/Delta signaling). Surprisingly, the basally branched arthropod groups also show similarities to mechanisms used in vertebrate somitoGenesis. Furthermore, it has become clear that the activation of pair rule Gene orthologs is a key step in the segmentation of all arthropods. Important findings of conserved and diverged aspects of segmentation from the last few years now allow us to draw an evolutionary scenario on how the mechanisms of segmentation could have evolved and led to the present mechanisms seen in various insect groups including dipterans like Drosophila.
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pair rule Gene orthologs in spider segmentation
Evolution & Development, 2005Co-Authors: Wim G.m. Damen, Ralf Janssen, Nikolamichael PrpicAbstract: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.PMID:16336415
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expression of pax group iii Genes suggests a single segmental periodicity for opisthosomal segment patterning in the spider cupiennius salei
Evolution & Development, 2005Co-Authors: Michael Schoppmeier, Wim G.m. DamenAbstract: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.
Ralf Janssen - One of the best experts on this subject based on the ideXlab platform.
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Gene expression analysis reveals that delta notch signalling is not involved in onychophoran segmentation
Development Genes and Evolution, 2016Co-Authors: Ralf Janssen, Graham E BuddAbstract:Delta/Notch (Dl/N) signalling is involved in the Gene regulatory network underlying the segmentation process in vertebrates and possibly also in annelids and arthropods, leading to the hypothesis that segmentation may have evolved in the last common ancestor of bilaterian animals. Because of seemingly contradicting results within the well-studied arthropods, however, the role and origin of Dl/N signalling in segmentation Generally is still unclear. In this study, we investigate core components of Dl/N signalling by means of Gene expression analysis in the onychophoran Euperipatoides kanangrensis, a close relative to the arthropods. We find that neither Delta or Notch nor any other investigated components of its signalling pathway are likely to be involved in segment addition in onychophorans. We instead suggest that Dl/N signalling may be involved in posterior elongation, another conserved function of these Genes. We suggest further that the posterior elongation network, rather than classic Dl/N signalling, may be in the control of the highly conserved segment polarity Gene network and the lower-level Pair-Rule Gene network in onychophorans. Consequently, we believe that the Pair-Rule Gene network and its interaction with Dl/N signalling may have evolved within the arthropod lineage and that Dl/N signalling has thus likely been recruited independently for segment addition in different phyla.
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Gene expression analysis reveals that Delta/Notch signalling is not involved in onychophoran segmentation
Development Genes and Evolution, 2016Co-Authors: Ralf Janssen, Graham E BuddAbstract:Delta/Notch (Dl/N) signalling is involved in the Gene regulatory network underlying the segmentation process in vertebrates and possibly also in annelids and arthropods, leading to the hypothesis that segmentation may have evolved in the last common ancestor of bilaterian animals. Because of seemingly contradicting results within the well-studied arthropods, however, the role and origin of Dl/N signalling in segmentation Generally is still unclear. In this study, we investigate core components of Dl/N signalling by means of Gene expression analysis in the onychophoran Euperipatoides kanangrensis , a close relative to the arthropods. We find that neither Delta or Notch nor any other investigated components of its signalling pathway are likely to be involved in segment addition in onychophorans. We instead suggest that Dl/N signalling may be involved in posterior elongation, another conserved function of these Genes. We suggest further that the posterior elongation network, rather than classic Dl/N signalling, may be in the control of the highly conserved segment polarity Gene network and the lower-level Pair-Rule Gene network in onychophorans. Consequently, we believe that the Pair-Rule Gene network and its interaction with Dl/N signalling may have evolved within the arthropod lineage and that Dl/N signalling has thus likely been recruited independently for segment addition in different phyla.
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deciphering the onychophoran segmentation Gene cascade Gene expression reveals limited involvement of pair rule Gene orthologs in segmentation but a highly conserved segment polarity Gene network
Developmental Biology, 2013Co-Authors: Ralf Janssen, Graham E BuddAbstract:The hallmark of the arthropods is their segmented body, although origin of segmentation, however, is unresolved. In order to shed light on the origin of segmentation we investigated orthologs of pair rule Genes (PRGs) and segment polarity Genes (SPGs) in a member of the closest related sister-group to the arthropods, the onychophorans. Our Gene expression data analysis suggests that most of the onychophoran PRGs do not play a role in segmentation. One possible exception is the even-skipped (eve) Gene that is expressed in the posterior end of the onychophoran where new segments are likely patterned, and is also expressed in segmentation-Gene typical transverse stripes in at least a number of newly formed segments. Other onychophoran PRGs such as runt (run), hairy/Hes (h/Hes) and odd-skipped (odd) do not appear to have a function in segmentation at all. Onychophoran PRGs that act low in the segmentation Gene cascade in insects, however, are potentially involved in segment-patterning. Most obvious is that from the expression of the pairberry (pby) Gene ortholog that is expressed in a typical SPG-pattern. Since this result suggested possible conservation of the SPG-network we further investigated SPGs (and associated factors) such as Notum in the onychophoran. We find that the expression patterns of SPGs in arthropods and the onychophoran are highly conserved, suggesting a conserved SPG-network in these two clades, and indeed also in an annelid. This may suggest that the common ancestor of lophotrochozoans and ecdysozoans was already segmented utilising the same SPG-network, or that the SPG-network was recruited independently in annelids and onychophorans/arthropods.
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expression of pair rule Gene orthologs in the blastoderm of a myriapod evidence for pair rule like mechanisms
BMC Developmental Biology, 2012Co-Authors: Ralf Janssen, Wim G.m. Damen, Graham E BuddAbstract:Background A hallmark of Drosophila segmentation is the stepwise subdivision of the body into smaller and smaller units, and finally into the segments. This is achieved by the function of the well-understood segmentation Gene cascade. The first molecular sign of a segmented body appears with the action of the pair rule Genes, which are expressed as transversal stripes in alternating segments. Drosophila development, however, is derived, and in most other arthropods only the anterior body is patterned (almost) simultaneously from a pre-existing field of cells; posterior segments are added sequentially from a posterior segment addition zone. A long-standing question is to what extent segmentation mechanisms known from Drosophila may be conserved in short-germ arthropods. Despite the derived developmental modes, it appears more likely that conserved mechanisms can be found in anterior patterning.
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pair rule Gene orthologs in spider segmentation
Evolution & Development, 2005Co-Authors: Wim G.m. Damen, Ralf Janssen, Nikolamichael PrpicAbstract: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.PMID:16336415
