Dynamic BMP signaling polarized by Toll patterns the dorsoventral axis in a hemimetabolous insect

Sachs, Lena; Chen, Yen-Ta; Drechsler, Axel; Lynch, Jeremy A.; Panfilio, Kristen A.; Lässig, Michael; Berg, Johannes; Roth, Siegfried

doi:10.7554/elife.05502

Cited by 43 publications

(84 citation statements)

References 71 publications

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“…In the jewel wasp Nasonia vitripennis, representing the Hymenoptera (the outgroup to all other holometabolous insects), BMP patterns the entire axis, whereas Toll is only required locally to induce mesoderm formation (Özüak et al, 2014). In the milkweed bug Oncopeltus fasciatus (a hemimetabolous insect), Toll lacks all instructive roles for tissue specification; it only polarizes BMP signalling, which in turn patterns the DV axis (Sachs et al, 2015). Taken together, the DV gene regulatory network (GRN) of Tribolium deviates from that of Drosophila in many interesting ways, but has not diverged as much as the DV-GRN of more basally branching insects, making it a preferable choice for direct molecular comparisons with Drosophila.…”

Section: Introductionmentioning

confidence: 99%

“…Although the immune function of Toll is conserved from flies to vertebrates, a DV patterning function of Toll has not been observed outside the insects. Indeed, analysis of DV patterning in more basally branching insects indicates that during insect evolution Toll signalling progressively gained the complex morphogen function found in modern flies (Lynch and Roth, 2011;Özüak et al, 2014;Sachs et al, 2015). The red flour beetle Tribolium castaneum provides an interesting intermediate position within this evolutionary series.…”

Section: Introductionmentioning

confidence: 99%

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Genome wide identification ofTriboliumdorsoventral patterning genes

et al. 2016

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The gene regulatory network controlling dorsoventral axis formation in insects has undergone drastic evolutionary changes. In Drosophila, a stable long-range gradient of Toll signalling specifies ventral cell fates and restricts BMP signalling to the dorsal half of the embryo. In Tribolium, however, Toll signalling is transient and only indirectly controls BMP signalling. In order to gain unbiased insights into the Tribolium network, we performed comparative transcriptome analyses of embryos with various dorsoventral pattering defects produced by parental RNAi for Toll and BMP signalling components. We also included embryos lacking the mesoderm ( produced by Tctwist RNAi) and characterized similarities and differences between Drosophila and Tribolium twist loss-of-function phenotypes. Using stringent conditions, we identified over 750 differentially expressed genes and analysed a subset with altered expression in more than one knockdown condition. We found new genes with localized expression and showed that conserved genes frequently possess earlier and stronger phenotypes than their Drosophila orthologues. For example, the leucine-rich repeat (LRR) protein Tartan, which has only a minor influence on nervous system development in Drosophila, is essential for early neurogenesis in Tribolium and the Tc-zinc-finger homeodomain protein 1 (Tc-zfh1), the orthologue of which plays a minor role in Drosophila muscle development, is essential for maintaining early Tc-twist expression, indicating an important function for mesoderm specification.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genome wide identification ofTriboliumdorsoventral patterning genes

et al. 2016

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“…Interestingly, knockdown of Rp‐Toll2 displaces the position of the embryonic rudiment along the egg AP axis, in addition to alterations along the DV axis of the embryo (Berni et al ., ). In Oncopeltus it was shown that Of‐Toll knockdown also changes the position of DV gene expression territories along the AP axis (Sachs et al ., ). Therefore, it is possible that the AP and DV axes in Hemiptera are not independently established as in the model Diptera Drosophila melanogaster , but are rather integrated by common elements as also suggested for Apis mellifera (Wilson et al, ).…”

Section: Embryonic Developmentmentioning

confidence: 97%

“…A recent study in the Hemiptera Oncopeltus suggests that the Toll pathway only serves as a spatial cue to polarize BMP signals by enhancing the BMP inhibitor sog at the ventral side (Sachs et al ., ). Similarly to vertebrate and spider early patterning (reviewed in (Bier and De Robertis, ), Oncopeltus BMP is required for sog repression along the DV axis (Sachs et al ., ). In Rhodnius , Rp‐Toll knockdown results in loss of ventral mesoderm and mesodermal gene expression, as well as zygotic sog expression (Berni et al ., ).…”

Section: Embryonic Developmentmentioning

confidence: 97%

Rhodnius prolixus: From classical physiology to modern developmental biology

Fonseca

Berni

Tobias-Santos

et al. 2017

Genesis

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The hemiptera Rhodnius prolixus is a blood-feeding insect and a primary vector of Trypanosoma cruzi, the etiological agent of the Chagas disease. Over the past century, Rhodnius has been the subject of intense investigations, which have contributed to unveil important aspects of metabolism and physiology in insects. Recent technological innovations are helping dissect the genetic and molecular underpinnings of Rhodnius embryogenesis and organogenesis, thus fostering the use of this important species in the fields of developmental and evolutionary biology. Rhodnius represents also an excellent system to study development under stressful conditions, since the embryo must develop in the presence of a large amount of blood-derived reactive oxygen species. With a recently sequenced genome, small among other Hemiptera, and the identification of basic elements for all classical development pathways, functional studies in this species are revealing novel aspects of insect development and evolution. Here we review early studies on this model insect and how this paved the way for recent functional studies using the kissing bug.

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“…Notably, the A‐P and D‐V axes in Drosophila are distinct and are determined through different pathways (Hartenstein and Chipman, ). There is evidence to suggest that this distinction is not so clear in other insects (Berni et al, ; da Fonseca et al, ; Sachs et al, ; Wilson and Dearden, ).…”

Section: Introductionmentioning

confidence: 99%

Factors involved in early polarization of the anterior‐posterior axis in the milkweed bug Oncopeltus fasciatus

Ginzburg

Cohen

Chipman

2017

Genesis

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The axes of insect embryos are defined early in the blastoderm stage. Genes involved in this polarization are well known in Drosophila, but less so in other insects, such as the milkweed bug Oncopeltus fasciatus. Using quantitative PCR, we looked at differential expression of several candidate genes for early anterior-posterior patterning and found that none of them are expressed asymmetrically in the early blastoderm. We then used an RNA-Seq approach to identify novel candidate genes that might be involved in early polarization in Oncopeltus. We focused on transcription factors (TFs) as these are likely to be central players in developmental processes. Using both homology and domain based identification approaches, we were unable to find any TF encoding transcripts that are expressed asymmetrically along the anterior-posterior axis at early stages. Using a GO-term analysis of all asymmetrically expressed mRNAs, we found an enrichment of genes relating to mitochondrial function in the posterior at the earliest studied time-point. We also found a gradual enrichment of transcription related activities, giving us a putative time frame for the maternal to zygotic transition. Our dataset provides us with a list of new candidate genes in early development, which can be followed up experimentally.

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Dynamic BMP signaling polarized by Toll patterns the dorsoventral axis in a hemimetabolous insect

Cited by 43 publications

References 71 publications

Genome wide identification ofTriboliumdorsoventral patterning genes

Genome wide identification ofTriboliumdorsoventral patterning genes

Rhodnius prolixus: From classical physiology to modern developmental biology

Factors involved in early polarization of the anterior‐posterior axis in the milkweed bug Oncopeltus fasciatus

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