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

BACKGROUND: Insect embryonic dorso-ventral patterning depends greatly on two pathways: the Toll pathway and the Bone Morphogenetic Protein pathway. While the relative contribution of each pathway has been investigated in holometabolous insects, their role has not been explored in insects with a hemi...

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Autores principales: Berni, Mateus, Fontenele, Marcio Ribeiro, Tobias-Santos, Vitoria, Caceres-Rodrigues, Aline, Mury, Flavia Borges, Vionette-do-Amaral, Raquel, Masuda, Hatisaburo, Sorgine, Marcos, da Fonseca, Rodrigo Nunes, Araujo, Helena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4407881/
https://www.ncbi.nlm.nih.gov/pubmed/25908955
http://dx.doi.org/10.1186/2041-9139-5-38
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author Berni, Mateus
Fontenele, Marcio Ribeiro
Tobias-Santos, Vitoria
Caceres-Rodrigues, Aline
Mury, Flavia Borges
Vionette-do-Amaral, Raquel
Masuda, Hatisaburo
Sorgine, Marcos
da Fonseca, Rodrigo Nunes
Araujo, Helena
author_facet Berni, Mateus
Fontenele, Marcio Ribeiro
Tobias-Santos, Vitoria
Caceres-Rodrigues, Aline
Mury, Flavia Borges
Vionette-do-Amaral, Raquel
Masuda, Hatisaburo
Sorgine, Marcos
da Fonseca, Rodrigo Nunes
Araujo, Helena
author_sort Berni, Mateus
collection PubMed
description BACKGROUND: Insect embryonic dorso-ventral patterning depends greatly on two pathways: the Toll pathway and the Bone Morphogenetic Protein pathway. While the relative contribution of each pathway has been investigated in holometabolous insects, their role has not been explored in insects with a hemimetabolous type of development. The hemimetabolous insect Rhodnius prolixus, an important vector of Chagas disease in the Americas, develops from an intermediate germ band and displays complex movements during katatrepsis that are not observed in other orders. However, little is known about the molecular events that regulate its embryogenesis. Here we investigate the expression and function of genes potentially involved in the initial patterning events that establish the embryonic dorso-ventral axis in this hemipteran. RESULTS: We establish a staging system for early embryogenesis that allows us to correlate embryo morphology with gene expression profiles. Using this system, we investigate the role of Toll pathway genes during embryogenesis. Detailed analyses of gene expression throughout development, coupled with functional analyses using parental RNA interference, revealed that maternal Toll is required to establish germ layers along the dorso-ventral axis and for embryo placement along the anterior-posterior axis. Interestingly, knockdown of the Toll pathway effector Rp-dorsal appears to regulate the expression of the Bone Morphogenetic Protein antagonist Rp-short-gastrulation. CONCLUSIONS: Our results indicate that Toll signals are the initiating event in dorso-ventral patterning during Rhodnius embryogenesis, and this is the first report of a conserved role for Toll in a hemipteran. Furthermore, as Rp-dorsal RNA interference generates anteriorly misplaced embryos, our results indicate a novel role for Toll signals in establishment of the anterior-posterior axis in Rhodnius. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-5-38) contains supplementary material, which is available to authorized users.
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spelling pubmed-44078812015-04-24 Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus Berni, Mateus Fontenele, Marcio Ribeiro Tobias-Santos, Vitoria Caceres-Rodrigues, Aline Mury, Flavia Borges Vionette-do-Amaral, Raquel Masuda, Hatisaburo Sorgine, Marcos da Fonseca, Rodrigo Nunes Araujo, Helena EvoDevo Research BACKGROUND: Insect embryonic dorso-ventral patterning depends greatly on two pathways: the Toll pathway and the Bone Morphogenetic Protein pathway. While the relative contribution of each pathway has been investigated in holometabolous insects, their role has not been explored in insects with a hemimetabolous type of development. The hemimetabolous insect Rhodnius prolixus, an important vector of Chagas disease in the Americas, develops from an intermediate germ band and displays complex movements during katatrepsis that are not observed in other orders. However, little is known about the molecular events that regulate its embryogenesis. Here we investigate the expression and function of genes potentially involved in the initial patterning events that establish the embryonic dorso-ventral axis in this hemipteran. RESULTS: We establish a staging system for early embryogenesis that allows us to correlate embryo morphology with gene expression profiles. Using this system, we investigate the role of Toll pathway genes during embryogenesis. Detailed analyses of gene expression throughout development, coupled with functional analyses using parental RNA interference, revealed that maternal Toll is required to establish germ layers along the dorso-ventral axis and for embryo placement along the anterior-posterior axis. Interestingly, knockdown of the Toll pathway effector Rp-dorsal appears to regulate the expression of the Bone Morphogenetic Protein antagonist Rp-short-gastrulation. CONCLUSIONS: Our results indicate that Toll signals are the initiating event in dorso-ventral patterning during Rhodnius embryogenesis, and this is the first report of a conserved role for Toll in a hemipteran. Furthermore, as Rp-dorsal RNA interference generates anteriorly misplaced embryos, our results indicate a novel role for Toll signals in establishment of the anterior-posterior axis in Rhodnius. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-5-38) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-27 /pmc/articles/PMC4407881/ /pubmed/25908955 http://dx.doi.org/10.1186/2041-9139-5-38 Text en © Berni et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Berni, Mateus
Fontenele, Marcio Ribeiro
Tobias-Santos, Vitoria
Caceres-Rodrigues, Aline
Mury, Flavia Borges
Vionette-do-Amaral, Raquel
Masuda, Hatisaburo
Sorgine, Marcos
da Fonseca, Rodrigo Nunes
Araujo, Helena
Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
title Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
title_full Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
title_fullStr Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
title_full_unstemmed Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
title_short Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
title_sort toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran rhodnius prolixus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4407881/
https://www.ncbi.nlm.nih.gov/pubmed/25908955
http://dx.doi.org/10.1186/2041-9139-5-38
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