Double abdomen in a short-germ insect: Zygotic control of axis formation revealed in the beetle<i>Tribolium castaneum</i>

Ansari, Salim; Troelenberg, Nicole; Dao, Van Anh; Richter, Tobias; Bucher, Gregor; Klingler, Martin

doi:10.1073/pnas.1716512115

Cited by 30 publications

(57 citation statements)

References 56 publications

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“…However, to the best of our knowledge a role for Axin in suppressing cWnt signaling in anterior cells in the early embryo has not been demonstrated except in T. castaneum (Ansari et al, 2018;Fu et al, 2012) and echinoids (this study). Axin expression in the egg and early embryo has been reported in the invertebrate chordate Amphioxus but there have been no functional studies done on Axin in this species (Onai, 2019).…”

Section: Axin Regulation Of the B-catenin Destruction Complex And Evomentioning

confidence: 71%

“…The current evidence from vertebrate and invertebrate taxa indicates that cWnt inhibition at the anterior pole of embryos by secreted factors is a relatively late event during embryogenesis. However, recent work in the short germ band insect Tribolium castaneum showed that there is an early inhibition of cWnt signaling at the future anterior end of embryos (Ansari et al, 2018;Fu et al, 2012;Pruhs et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Interestingly, the inhibition of cWnt signaling at the anterior end of early T. castaneum embryos appears to be mediated by Axin, a critical cytoplasmic component of the βcatenin destruction complex in the cWnt pathway (Ansari et al, 2018;Fu et al, 2012;Pruhs et al, 2017). The β-catenin destruction complex is a highly conserved negative regulator of cWnt signaling, and in addition to Axin, this complex is composed of three other major proteins: APC, the product of the adenomatous polyposis coli gene, Glycogen Synthase Kinase 3β (GSK-3β), and Casein Kinase 1a (CK1a).…”

Section: Introductionmentioning

confidence: 99%

“…Mutations in Axin and/or APC that lead to impaired βcatenin regulation can lead to increased levels of cWnt signaling (MacDonald et al, 2009;Nusse and Clevers, 2017). In T. castaneum TcAxin is maternally expressed at the anterior end of the unfertilized egg and downregulating Axin expression using RNAi resulted in the duplication of posterior structures at the anterior end of the embryo (Ansari et al, 2018;Fu et al, 2012;Pruhs et al, 2017). These studies have provided evidence that maternal Axin localized to the anterior end of T. castaneum eggs and early embryos downregulates cWnt signaling and blocks the formation of posterior structures at the anterior end.…”

Section: Introductionmentioning

confidence: 99%

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A dual role for Axin in establishing the anterior-posterior axis in the early sea urchin embryo

Sun

Peng

Wang

et al. 2020

Preprint

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The activation of Wnt/b-catenin (cWnt) signaling at the future posterior end of early embryos is a highly conserved mechanism for initiating pattern formation along the anterior-posterior (AP) axis in bilaterians. Moreover, in many bilaterian taxa, in addition, to activation of cWnt signaling at the posterior end, inhibition of cWnt signaling at the anterior end is required for normal development of anterior structures. In most cases, inhibition of cWnt signaling at the anterior end occurs around gastrulation and it is typically mediated by secreted factors that block signal transduction through the cWnt cell surface receptor-ligand complex. This phenomenon has been fairly well characterized, but the emerging role for intracellular inhibition of cWnt signaling in future anterior blastomeres-in cleavage stage embryos-to regulate correct AP patterning is less well understood. To investigate this process in an invertebrate deuterostome embryo we studied the function of Axin, a critical negative regulator of cWnt signaling, during early sea urchin embryogenesis. Sea urchin Axin is ubiquitously expressed in early embryos and by the blastula stage the expression of the gene becomes restricted to the posterior end of the embryo. Strikingly, knockdown of Axin protein levels using antisense Axin morpholinos (MO) led to ectopic nuclearization of b-catenin and activation of endomesoderm gene expression in anterior blastomeres in early embryos.These embryos developed a severely posteriorized phenotype that could be fully rescued by co-injection of Axin MO with wild-type Axin mRNA. Axin is known to negatively regulate cWnt by its role in mediating b-catenin stability within the destruction complex. Consistent with this function overexpression of Axin by mRNA injection led to the downregulation of nuclear b-catenin, inhibition of endomesoderm specification and a 3 strong anteriorization of embryos. Axin has several well-defined domains that regulate its interaction with b-catenin and the key regulators of the destruction complex, Adenomatous Polyposis Coli (APC), Glycogen Synthase Kinase 3b (GSK-3b), and Dishevelled (Dvl). Using Axin constructs with single deletions of the binding sites for these proteins we showed that only the GSK-3b binding site on Axin is required for its inhibition of cWnt in the sea urchin embryo. Strikingly, overexpression of the GSK-3bbinding domain alone led to embryos with elevated levels of endomesoderm gene expression and a strongly posteriorized phenotype. These results indicated that Axin has a critical global role in inhibiting cWnt signaling in the early sea urchin embryo, and moreover, that the interaction of Axin with GSK-3b is critical for this inhibition. These results also add to the growing body of evidence that Axin plays a global function in suppressing cWnt signaling in early embryos and indicates that modulation of Axin function may be a critical early step during patterning of the AP axis during bilaterian development

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Section: Axin Regulation Of the B-catenin Destruction Complex And Evomentioning

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

A dual role for Axin in establishing the anterior-posterior axis in the early sea urchin embryo

Sun

Peng

Wang

et al. 2020

Preprint

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“…On the other hand, global knock-downs increase the risk of secondary effects on muscle development, e.g., due to early effects of genes on developmental events prior to muscle development such as embryonic patterning, cell proliferation, etc.. These effects were minimized because the iBeetle screen included careful analyses of the larval cuticles with the aim to recover patterning genes as well Ansari et al 2018). Thus, even if some of the genes on our shortlist (Table 2) As for any other screen, it is clear that we missed many genes affecting Tribolium muscle development.…”

Section: Drosophilamentioning

confidence: 99%

A large scale systemic RNAi screen in the red flour beetleTribolium castaneumidentifies novel genes involved in insect muscle development

Schultheis

Weißkopf

Schaub

et al. 2018

Preprint

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Although muscle development has been widely studied in Drosophila melanogaster there are still many gaps in our knowledge, and it is not known to which extent this knowledge can be transferred to other arthropods. To help closing these gaps we participated in a large-scale RNAi screen that used the red flour beetle, Tribolium castaneum, as a screening platform. The effects of systemic RNAi were screened upon double-stranded RNA injections into appropriate muscle-GFP tester strains.Injections into larvae were followed by the analysis of the adult thoracic muscle patterns, and injections into pupae by the analysis of the late embryonic/larval muscle patterns. Herein we focus on the results of our pupal injection screen for late embryonic/larval muscle phenotypes, which covered 8.500 of a total of ~16.500 genes of the Tribolium genome. Apart from many genes known from Drosophila as regulators of muscle development, a collection of genes previously unconnected to muscle development yielded larval body wall and leg muscle phenotypes. We present the main candidates that remained after being processed through a series of verification and selection steps. Further, we discuss why distinct though overlapping sets of genes are revealed by the Drosophila and Tribolium screening approaches.

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Persistent Parental RNAi in the Beetle Tribolium castaneum Involves Maternal Transmission of Long Double‐Stranded RNA

2022

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Parental RNA interference (pRNAi) is a powerful and widely used method for gene‐specific knockdown. Yet in insects its efficacy varies between species, and how the systemic response is transmitted from mother to offspring remains elusive. Using the beetle Tribolium castaneum, an RT‐qPCR strategy to distinguish the presence of double‐stranded RNA (dsRNA) from endogenous mRNA is reported. It is found that injected dsRNA is directly transmitted into the egg and persists throughout embryogenesis. Despite this depletion of dsRNA from the mother, it is shown that strong pRNAi can persist for months before waning at strain‐specific rates. In seeking the receptor proteins for cellular uptake of long dsRNA into the egg, a phylogenomics profiling approach of candidate proteins is also presented. A visualization strategy based on taxonomically hierarchical assessment of orthology clustering data to rapidly assess gene age and copy number changes, refined by sequence‐based evidence, is demonstrated. Repeated losses of SID‐1‐like channel proteins in the arthropods, including wholesale loss in the Heteroptera (true bugs), which are nonetheless highly sensitive to pRNAi, are thereby documented. Overall, practical considerations for insect pRNAi against a backdrop of outstanding questions on the molecular mechanism of dsRNA transmission for long‐term, systemic knockdown are elucidated.

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Double abdomen in a short-germ insect: Zygotic control of axis formation revealed in the beetleTribolium castaneum

Cited by 30 publications

References 56 publications

A dual role for Axin in establishing the anterior-posterior axis in the early sea urchin embryo

A dual role for Axin in establishing the anterior-posterior axis in the early sea urchin embryo

A large scale systemic RNAi screen in the red flour beetleTribolium castaneumidentifies novel genes involved in insect muscle development

Persistent Parental RNAi in the Beetle Tribolium castaneum Involves Maternal Transmission of Long Double‐Stranded RNA

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