The dynamic expression of extraembryonic marker genes in the beetle Tribolium castaneum reveals the complexity of serosa and amnion formation in a short germ insect

Sharma, Rahul; Beermann, Anke; Schröder, Reinhard

doi:10.1016/j.gep.2013.07.002

Cited by 14 publications

(15 citation statements)

References 36 publications

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“…4B1–B3). As the known serosal markers in Tribolium are mostly expressed throughout the tissue [15], [39], while the asymmetries seen here approximately correlate with the sites of serosal window closure and later serosal rupture, such regionalized expression will be key in future dissection of the serosa’s morphogenetic repertoire.…”

Section: Discussionmentioning

confidence: 74%

Visualizing Late Insect Embryogenesis: Extraembryonic and Mesodermal Enhancer Trap Expression in the Beetle Tribolium castaneum

2014

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The beetle Tribolium castaneum has increasingly become a powerful model for comparative research on insect development. One recent resource is a collection of piggyBac transposon-based enhancer trap lines. Here, we provide a detailed analysis of three selected lines and demonstrate their value for investigations in the second half of embryogenesis, which has thus far lagged behind research on early stages. Two lines, G12424 and KT650, show enhanced green fluorescent protein (EGFP) expression throughout the extraembryonic serosal tissue and in a few discrete embryonic domains. Intriguingly, both lines show for the first time a degree of regionalization within the mature serosa. However, their expression profiles illuminate distinct aspects of serosal biology: G12424 tracks the tissue’s rapid maturation while KT650 expression likely reflects ongoing physiological processes. The third line, G04609, is stably expressed in mesodermal domains, including segmental muscles and the heart. Genomic mapping followed by in situ hybridization for genes near to the G04609 insertion site suggests that the transposon has trapped enhancer information for the Tribolium orthologue of midline (Tc-mid). Altogether, our analyses provide the first live imaging, long-term characterizations of enhancer traps from this collection. We show that EGFP expression is readily detected, including in heterozygote crosses that permit the simultaneous visualization of multiple tissue types. The tissue specificity provides live, endogenous marker gene expression at key developmental stages that are inaccessible for whole mount staining. Furthermore, the nonlocalized EGFP in these lines illuminates both the nucleus and cytoplasm, providing cellular resolution for morphogenesis research on processes such as dorsal closure and heart formation. In future work, identification of regulatory regions driving these enhancer traps will deepen our understanding of late developmental control, including in the extraembryonic domain, which is a hallmark of insect development but which is not yet well understood.

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Section: Discussionmentioning

confidence: 74%

Visualizing Late Insect Embryogenesis: Extraembryonic and Mesodermal Enhancer Trap Expression in the Beetle Tribolium castaneum

2014

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“…The larval cuticle phenotype was inspected making use of their autofluorescence under UV light to visualize all cuticularised structures including the gut. In situ hybridizations and antibody staining on wild-type and RNAi embryos were performed as described previously [ 25 ]. Each probe/antibody was carefully titrated to ensure an optimal signal-to-background ratio.…”

Section: Methodsmentioning

confidence: 99%

The Roles of the Wnt-Antagonists Axin and Lrp4 during Embryogenesis of the Red Flour Beetle Tribolium castaneum

Prühs

Beermann

Schröder

2017

JDB

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In both vertebrates and invertebrates, the Wnt-signaling pathway is essential for numerous processes in embryogenesis and during adult life. Wnt activity is fine-tuned at various levels by the interplay of a number of Wnt-agonists (Wnt ligands, Frizzled-receptors, Lrp5/6 coreceptors) and Wnt-antagonists (among them Axin, Secreted frizzled and Lrp4) to define anterior–posterior polarity of the early embryo and specify cell fate in organogenesis. So far, the functional analysis of Wnt-pathway components in insects has concentrated on the roles of Wnt-agonists and on the Wnt-antagonist Axin. We depict here additional features of the Wnt-antagonist Axin in the flour beetle Tribolium castaneum. We show that Tc-axin is dynamically expressed throughout embryogenesis and confirm its essential role in head development. In addition, we describe an as yet undetected, more extreme Tc-axin RNAi-phenotype, the ectopic formation of posterior abdominal segments in reverse polarity and a second hindgut at the anterior. For the first time, we describe here that an lrp4 ortholog is involved in axis formation in an insect. The Tribolium Lrp4 ortholog is ubiquitously expressed throughout embryogenesis. Its downregulation via maternal RNAi results in the reduction of head structures but not in axis polarity reversal. Furthermore, segmentation is impaired and larvae develop with a severe gap-phenotype. We conclude that, as in vertebrates, Tc-lrp4 functions as a Wnt-inhibitor in Tribolium during various stages of embryogenesis. We discuss the role of both components as negative modulators of Wnt signaling in respect to axis formation and segmentation in Tribolium.

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“…Although Tc-Doc clears from the serosa during the SW stage (Fig. 2C), so too does Tc-zen1 (Sharma et al, 2013a), whereas Tczen2 does not affect Tc-Doc expression (Fig. S4A-D), indicating that such a repressive interaction is not conserved.…”

Section: Evolution Of Dorsocross Expression and Functionmentioning

confidence: 99%

Novel functions for Dorsocross in epithelial morphogenesis in the beetle Tribolium castaneum

Horn

Panfilio

2016

Development

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Epithelial morphogenesis, the progressive restructuring of tissue sheets, is fundamental to embryogenesis. In insects, not only embryonic tissues but also extraembryonic (EE) epithelia play a crucial role in shaping the embryo. In Drosophila, the T-box transcription factor Dorsocross (Doc) is essential for EE tissue maintenance and therefore embryo survival. However, Drosophila possesses a single amnioserosa, whereas most insects have a distinct amnion and serosa. How does this derived situation compare with Doc function in the ancestral context of two EE epithelia? Here, we investigate the Doc orthologue in the red flour beetle, Tribolium castaneum, which is an excellent model for EE tissue complement and for functional, fluorescent live imaging approaches. Surprisingly, we find that Tc-Doc controls all major events in Tribolium EE morphogenesis without affecting EE tissue specification or maintenance. These macroevolutionary changes in function between Tribolium and Drosophila are accompanied by regulatory network changes, where BMP signaling and possibly the transcription factor Hindsight are downstream mediators. We propose that the ancestral role of Doc was to control morphogenesis and discuss how Tc-Doc could provide spatial precision for remodeling the amnion-serosa border.

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The dynamic expression of extraembryonic marker genes in the beetle Tribolium castaneum reveals the complexity of serosa and amnion formation in a short germ insect

Cited by 14 publications

References 36 publications

Visualizing Late Insect Embryogenesis: Extraembryonic and Mesodermal Enhancer Trap Expression in the Beetle Tribolium castaneum

Visualizing Late Insect Embryogenesis: Extraembryonic and Mesodermal Enhancer Trap Expression in the Beetle Tribolium castaneum

The Roles of the Wnt-Antagonists Axin and Lrp4 during Embryogenesis of the Red Flour Beetle Tribolium castaneum

Novel functions for Dorsocross in epithelial morphogenesis in the beetle Tribolium castaneum

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