Functional analysis of engrailed in Tribolium segmentation

Lim, Jinsung; Choe, Chong Pyo

doi:10.1016/j.mod.2019.103594

Cited by 7 publications

(13 citation statements)

References 42 publications

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“…In many arthropods, wg , en , and hh , interact positively as part of a regulatory network to establish segment polarity [ 30 – 34 , 43 – 45 , 50 , 52 , 57 ]. A segmentally reiterated pattern of gene expression emerges, which includes a stripe of wg expression positioned immediately in front of a stripe of en and hh expression.…”

Section: Discussionmentioning

confidence: 99%

Extensive loss of Wnt genes in Tardigrada

et al. 2021

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Background Wnt genes code for ligands that activate signaling pathways during development in Metazoa. Through the canonical Wnt (cWnt) signaling pathway, these genes regulate important processes in bilaterian development, such as establishing the anteroposterior axis and posterior growth. In Arthropoda, Wnt ligands also regulate segment polarity, and outgrowth and patterning of developing appendages. Arthropods are part of a lineage called Panarthropoda that includes Onychophora and Tardigrada. Previous studies revealed potential roles of Wnt genes in regulating posterior growth, segment polarity, and growth and patterning of legs in Onychophora. Unlike most other panarthropods, tardigrades lack posterior growth, but retain segmentation and appendages. Here, we investigated Wnt genes in tardigrades to gain insight into potential roles that these genes play during development of the highly compact and miniaturized tardigrade body plan. Results We analyzed published genomes for two representatives of Tardigrada, Hypsibius exemplaris and Ramazzottius varieornatus. We identified single orthologs of Wnt4, Wnt5, Wnt9, Wnt11, and WntA, as well as two Wnt16 paralogs in both tardigrade genomes. We only found a Wnt2 ortholog in H. exemplaris. We could not identify orthologs of Wnt1, Wnt6, Wnt7, Wnt8, or Wnt10. We identified most other components of cWnt signaling in both tardigrade genomes. However, we were unable to identify an ortholog of arrow/Lrp5/6, a gene that codes for a Frizzled co-receptor of Wnt ligands. Additionally, we found that some other animals that have lost several Wnt genes and are secondarily miniaturized, like tardigrades, are also missing an ortholog of arrow/Lrp5/6. We analyzed the embryonic expression patterns of Wnt genes in H. exemplaris during developmental stages that span the establishment of the AP axis through segmentation and leg development. We detected expression of all Wnt genes in H. exemplaris besides one of the Wnt16 paralogs. During embryo elongation, expression of several Wnt genes was restricted to the posterior pole or a region between the anterior and posterior poles. Wnt genes were expressed in distinct patterns during segmentation and development of legs in H. exemplaris, rather than in broadly overlapping patterns. Conclusions Our results indicate that Wnt signaling has been highly modified in Tardigrada. While most components of cWnt signaling are conserved in tardigrades, we conclude that tardigrades have lost Wnt1, Wnt6, Wnt7, Wnt8, and Wnt10, along with arrow/Lrp5/6. Our expression data may indicate a conserved role of Wnt genes in specifying posterior identities during establishment of the AP axis. However, the loss of several Wnt genes and the distinct expression patterns of Wnt genes during segmentation and leg development may indicate that combinatorial interactions among Wnt genes are less important during tardigrade development compared to many other animals. Based on our results, and comparisons to previous studies, we speculate that the loss of several Wnt genes in Tardigrada may be related to a reduced number of cells and simplified development that accompanied miniaturization and anatomical simplification in this lineage.

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Section: Discussionmentioning

confidence: 99%

Extensive loss of Wnt genes in Tardigrada

et al. 2021

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“…Abbreviations as in Fig. 2 of parasegmental grooves either (e.g., Brown et al 1994;Peterson et al 1998;Marie and Bacon 2000;Hughes and Kaufman 2002;Kettle et al 2003;Janssen et al 2004;Chipman et al 2004;Alwes and Scholtz 2006;O'Donnell and Jockusch 2010;Janssen 2012;Nakagaki et al 2015;Lim and Choe 2020).…”

Section: Expression Of Engrailed Genes Reveals the Absence Of Clearly...mentioning

confidence: 99%

Lack of evidence for conserved parasegmental grooves in arthropods

2022

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In the arthropod model species Drosophila melanogaster, a dipteran fly, segmentation of the anterior–posterior body axis is under control of a hierarchic gene cascade. Segmental boundaries that form morphological grooves are established posteriorly within the segmental expression domain of the segment-polarity gene (SPG) engrailed (en). More important for the development of the fly, however, are the parasegmental boundaries that are established at the interface of en expressing cells and anteriorly adjacent wingless (wg) expressing cells. In Drosophila, both segmental and transient parasegmental grooves form. The latter are positioned anterior to the expression of en. Although the function of the SPGs in establishing and maintaining segmental and parasegmental boundaries is highly conserved among arthropods, parasegmental grooves have only been reported for Drosophila, and a spider (Cupiennius salei). Here, we present new data on en expression, and re-evaluate published data, from four distantly related spiders, including Cupiennius, and a distantly related chelicerate, the harvestman Phalangium opilio. Gene expression analysis of en genes in these animals does not corroborate the presence of parasegmental grooves. Consequently, our data question the general presence of parasegmental grooves in arthropods.

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“…Degrading segment boundaries are also occurred after depletion of Tc-en and Tc-hh, displaying similar compact segmental remnants as observed after knockdown of Tc-wg. The stripes marked by Tc-en in Tc-hh RNAi embryos are absent in the more anterior segments during elongation stage and irregular Tc-en expression along ventral midline is visible when the germ-band has been completely retracted (Bolognesi et al, 2008;Farzana and Brown, 2008;Lim and Choe, 2020). Particularly, in loss of Tc-hh function enbryis, the abnormalities of Tc-en stripes appears evident during retraction, which is different in comparison with Tc-GlyS and Tc-AGBE RNAi embryos.…”

Section: The Roles Of Tc-glys and Tc-agbe In Development Pattern Ante...mentioning

confidence: 85%

“…The expression is strongly disorganized in the head and trunk region after depletion of one of them. Knockdown of wg and hh both produce compact embryos with fused en stripes and shortened axis after germ-band retraction, suggesting that formation of A-P axis and segment boundaries are strictly controlled by the segment polarity gene circuit (Farzana and Brown, 2008;Lim and Choe, 2020;Ober and Jockusch, 2006). The Drosophila shaggy gene (sgg, also called zeste-white 3), is the homolog of GSK-3.…”

Section: Interactions Between Segment Polarity Genes Define Boundary ...mentioning

confidence: 99%

“…To test, whether the interaction of segment polarity genes was maintained after depletion of Tc-GlyS and Tc-AGBE, we investigated Tc-engrailed (Tc-en) expression which is regulated by Tc-wg in adjacent cells. Tc-en is co-expressed with Tc-hh in same cells of the posterior segmental compartments (Lim and Choe, 2020;Peifer and Bejsovec, 1992). During early embryogenesis, Tc-en expression in stripes was similar to expression pattern of Tc-hh, except for the labrum, ocular segment (oc) and growth zone ( showed that Tc-GlyS and Tc-AGBE were involved in maintaining the expression of the segment polarity genes Tc-wg, Tc-hh, and Tc-en at the parasegmental boundary while the formation appeared to be undisturbed (Choe et al, 2006;Ober and Jockusch, 2006).…”

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confidence: 99%

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Glycogen metabolism influences embryonic segmentation and appendages outgrowth during Tribolium castaneum embryogenesis

Wan¹

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Liu for providing me continuous support at all times, for bringing me so much fun.I was also conveying my heartfelt thanks to China Scholarship Council (CSC), Georg-August-University School of Science (GAUSS), Göttingen University for the financial and project support.Last and most importantly, I was extremely thankful to my parents whose constant love and support keep me motivated and confident. Deepest thanks to my wife, Dan Wang, for the unconditional love and support throughout the entire master, PhD time and every day. Testing whetherTc-GlyS and Tc-AGBE function via the Wnt and Hh pathways .

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Functional analysis of engrailed in Tribolium segmentation

Cited by 7 publications

References 42 publications

Extensive loss of Wnt genes in Tardigrada

Extensive loss of Wnt genes in Tardigrada

Lack of evidence for conserved parasegmental grooves in arthropods

Glycogen metabolism influences embryonic segmentation and appendages outgrowth during Tribolium castaneum embryogenesis

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