Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus

Berni, Mateus; Fontenele, Marcio; Tobias-Santos, Vitória; Caceres-Rodrigues, Aline; Mury, Flávia Borges; Vionette-do-Amaral, Raquel; Masuda, Hatisaburo; Sorgine, Marcos Henrique Ferreira; Fonseca, Rodrigo Nunes da; Araujo, Helena

doi:10.1186/2041-9139-5-38

Cited by 35 publications

(75 citation statements)

References 63 publications

(87 reference statements)

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“…We identified single-copy orthologs for the DV patterning genes, including most Toll and bone morphogenetic protein (BMP) pathway elements. The BMP type I receptor Sax, however, was not found in R. prolixus or in previous analyses (30). Our functional analysis showed that one of the rpToll genes (RPRC009262), similarly to that reported for hymenopterans (31,32), performs both DV and AP embryonic patterning roles (30), pointing to a potentially novel role that this pathway element might display during embryogenesis.…”

Section: Significancementioning

confidence: 57%

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

Mesquita

Vionette-Amaral

Lowenberger

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Rhodnius prolixus not only has served as a model organism for the study of insect physiology, but also is a major vector of Chagas disease, an illness that affects approximately seven million people worldwide. We sequenced the genome of R. prolixus, generated assembled sequences covering 95% of the genome (∼702 Mb), including 15,456 putative protein-coding genes, and completed comprehensive genomic analyses of this obligate blood-feeding insect. Although immune-deficiency (IMD)-mediated immune responses were observed, R. prolixus putatively lacks key components of the IMD pathway, suggesting a reorganization of the canonical immune signaling network. Although both Toll and IMD effectors controlled intestinal microbiota, neither affected Trypanosoma cruzi, the causal agent of Chagas disease, implying the existence of evasion or tolerance mechanisms. R. prolixus has experienced an extensive loss of selenoprotein genes, with its repertoire reduced to only two proteins, one of which is a selenocysteine-based glutathione peroxidase, the first found in insects. The genome contained actively transcribed, horizontally transferred genes from Wolbachia sp., which showed evidence of codon use evolution toward the insect use pattern. Comparative protein analyses revealed many lineage-specific expansions and putative gene absences in R. prolixus, including tandem expansions of genes related to chemoreception, feeding, and digestion that possibly contributed to the evolution of a blood-feeding lifestyle. The genome assembly and these associated analyses provide critical information on the physiology and evolution of this important vector species and should be instrumental for the development of innovative disease control methods.

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Section: Significancementioning

confidence: 57%

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

Mesquita

Vionette-Amaral

Lowenberger

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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320

418

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“…During early stages the polarity of the embryo and of the egg are coincident, but during the movements of anatrepsis they become everted regarding AP and DV axes. At later stages (stage 9 and 10 from Berni et al, ), katatrepsis reestablishes the coincidence of egg and embryonic polarity. Head and gnathal segments are displayed in blue, thoracic in yellow and abdominal in green.…”

Section: Embryonic Developmentmentioning

confidence: 92%

“…Knock‐down of Rp‐Dorsal , a transcription factor of the Toll pathway also did not change T. cruzi parasite levels (Mesquita et al ., ). The fact that the expression of the Iĸ‐B inhibitor Rp‐cactus is up‐regulated after Zymosan exposure (Berni et al ., ) indicates that the Dorsal pathway is indeed involved in immunity in hemiptera, although not stimulated by T. cruzi infection. Thus, T. cruzi probably developed active evasion or tolerance mechanisms, which is absent in the Rhodococcus symbiotic bacteria.…”

Section: Hemiptera Species For Developmental Studies and Their Relatimentioning

confidence: 96%

“…Such protocols are particularly desirable to study early stages of embryogenesis. Recently, different protocols have been developed to perform morphological analysis and in situ hybridization (Berni et al ., ; Lavore et al ., ) (Figure ) and a staging system for Rhodnius embryogenesis has been proposed, that will enable to relate research performed in different labs (Figure , (Berni et al ., ).…”

Section: Embryonic Developmentmentioning

confidence: 98%

“…(a) Nuclear DAPI stainings of successive embryonic stages. For details on the staging system see Berni et al, (). Scale bar 500 µm.…”

Section: Embryonic Developmentmentioning

confidence: 99%

See 2 more Smart Citations

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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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.

show abstract

Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus

Cited by 35 publications

References 63 publications

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

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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